PROTEIN PREPARATION

20190072565 ยท 2019-03-07

    Inventors

    Cpc classification

    International classification

    Abstract

    This disclosure relates to the field of protein preparation and mass spectrometry analysis. In some embodiments, the disclosure relates to compositions and methods for simplifying mass spectrometry analysis by reducing methionine oxidation of protein samples.

    Claims

    1. A method of preparing a polypeptide sample for separation and/or analysis, comprising contacting the polypeptide sample with at least one methionine sulfoxide reductase (MSR) enzyme under conditions suitable for reducing oxidized methionines in the polypeptide sample.

    2. The method of claim 1, wherein at least one methionine sulfoxide reductase enzyme is capable of reducing methionine-S-sulfoxide, or is capable of reducing methionine-R-sulfoxide, or is capable of reducing both methionine-S-sulfoxide and methionine-R-sulfoxide.

    3. The method of claim 1, wherein the method comprises contacting the polypeptide sample with at least one methionine sulfoxide reductase enzyme that is capable of reducing methionine-S-sulfoxide and at least one methionine sulfoxide reductase enzyme that is capable of reducing methionine-R-sulfoxide.

    4. The method of claim 1, wherein the method comprises contacting the polypeptide sample with at least one methionine sulfoxide reductase enzyme that is capable of reducing both methionine-S-sulfoxide and methionine-R-sulfoxide.

    5. (canceled)

    6. (canceled)

    7. The method of claim 4, wherein the MsrAB enzyme is derived from a methionine sulfoxide reductase from an organism selected from Neisseria, Lautropia, Cardiobacterium, Gammaproteobacteria, Pelistega, Marinospirillum, Basilea, Oligella, Alcagenaceae, Psychrobacter, Brackiella, Taylorella, Moraxella, Enhydrobacter, Fusobacterium, Helcococcus, Paenibacillus, Eremococcus, Methanobrevibacter, Methanomassiliicoccales, Methanocorpusculum, Thermoplasmatales, Methanometylophilus, Methanoculleus, and Methanocella.

    8. The method of claim 7, wherein the MsrAB enzyme is derived from a bacterial methionine sulfoxide reductase enzyme.

    9. The method of claim 8, wherein the methionine sulfoxide reductase enzyme is derived from a methionine sulfoxide reductase enzyme of Neisseria gonorrhoeae, Neisseria meningitides, Neisseria lactamica, Neisseria polysaccharea, Neisseria flavescens, Neisseria sicca, Neisseria nacacae, or Neisseria mucosa.

    10. The method of claim 1, wherein the methionine sulfoxide reductase enzyme comprises an amino acid sequence that is at least 70% identical to a sequence selected from SEQ ID NOs: 10 to 34.

    11. (canceled)

    12. (canceled)

    13. The method of claim 13, further comprising removing the methionine sulfoxide reductase enzyme following reduction of oxidized methionines in the polypeptide sample.

    14. The method of claim 1, wherein the methionine sulfoxide reductase enzyme is present at a weight ratio of between 1:100 and 1:2 enzyme:polypeptide.

    15. The method of claim 1, wherein the contacting occurs under reducing conditions.

    16. The method of claim 15, wherein the contacting occurs in the presence of dithiothreitol (DTT) and/or dithioerythritol (DTE).

    17. The method of claim 1, which is a method of preparing a sample for liquid chromatography.

    18. The method of claim 17, wherein the method further comprises subjecting polypeptides of the polypeptide sample to liquid chromatography.

    19. (canceled)

    20. The method of claim 1, which is a method of preparing a sample for capillary electrophoresis.

    21. The method of claim 20, wherein the method further comprises subjecting polypeptides of the polypeptide sample to capillary electrophoresis.

    22. The method of claim 1, which is a method of preparing a sample for mass spectrometry.

    23. (canceled)

    24. (canceled)

    25. (canceled)

    26. The method of claim 1, wherein the method comprises fragmenting the polypeptides by digestion with trypsin, chymotrypsin, AspN, GluC, LysC, LysN, ArgC, proteinase K, or thermolysin, or by chemical cleavage with CNBr.

    27.-35. (canceled)

    36. A method of producing a mass spectrometry spectra comprising contacting polypeptides of a polypeptide sample with at least one methionine sulfoxide reductase enzyme under conditions suitable for reducing oxidized methionines in the polypeptide sample, and injecting the polypeptides into a liquid chromatograph/mass spectrometer detection system or directly into a mass spectrometer detection system, wherein the polypeptides of the polypeptide sample have not been fragmented.

    37.-52. (canceled)

    53. A kit comprising at least one methionine sulfoxide reductase enzyme.

    54.-66. (canceled)

    Description

    BRIEF DESCRIPTION OF THE FIGURES

    [0032] FIG. 1 shows structures of oxidized methionine and reduction by methionine sulfoxide reductases. ROS is reactive oxygen species.

    [0033] FIG. 2 shows intact protein MS analysis of methionine oxidation of TurboLuc in the absence of peroxide treatment. Un-oxidized samples or samples treated with the Msrs ngMsrAB or nmMsrAB are presented.

    [0034] FIG. 3 shows intact protein MS analysis of methionine oxidation of TurboLuc following 10 peroxide treatment. Samples were oxidized alone or oxidized and then treated with the Msrs ngMsrAB or nmMsrAB.

    [0035] FIG. 4 shows intact protein MS analysis of methionine oxidation of TurboLuc following 25 peroxide treatment. Samples were oxidized alone or oxidized and then treated with the Msrs ngMsrAB or nmMsrAB.

    [0036] FIG. 5 shows intact protein MS analysis of methionine oxidation of TurboLuc following 75 peroxide treatment. Samples were oxidized alone or oxidized and then treated with the Msrs ngMsrAB or nmMsrAB.

    [0037] FIG. 6 shows intact protein MS analysis of methionine oxidation of TurboLuc following 100 peroxide treatment. Samples were oxidized alone or oxidized and then treated with the Msrs ngMsrAB or nmMsrAB.

    [0038] FIG. 7 shows intact protein MS analysis of methionine oxidation of TurboLuc following 500 peroxide treatment. Samples were oxidized alone or oxidized and then treated with the Msrs ngMsrAB or nmMsrAB.

    [0039] FIG. 8 outlines an exemplary procedure for shotgun proteomic analysis.

    [0040] FIG. 9 shows shotgun proteomic analysis results on methionine oxidation of a 6-protein sample. Reversal of methionine oxidation was measured for samples treated with ngMsrAB or nmMsrAB. The percentage of oxidized methionine and doubly oxidized methionine are presented for control (no oxidation), 1:25, 1:50, and 1:100 methionine:peroxide ratios. Met, methionine.

    [0041] FIGS. 10A and 10B present the protocol (A) and actual readout (B) of parallel reaction monitoring (PRM) of a representative experiment.

    [0042] FIGS. 11A and 11B present the effect of treatment with nmMsrAB and ngMsrAB on the disappearance of an oxidized peptide standard (SEQ ID No: 4) and appearance of the corresponding reduced peptide (SEQ ID No: 5) using PRM analysis.

    [0043] FIGS. 12A and 12B present the effect of treatment with nmMsrAB and ngMsrAB on the disappearance of an oxidized phosphopeptide (SEQ ID No: 6) and appearance of the corresponding reduced peptide (SEQ ID No: 7) using PRM analysis.

    [0044] FIGS. 13A and 13B present the effect of treatment with nmMsrAB and ngMsrAB on the disappearance of another oxidized phosphopeptide (SEQ ID No: 8) and corresponding appearance of a reduced phosphopeptide (SEQ ID No: 9) using PRM analysis.

    [0045] FIG. 14 shows the sequence of His-tagged/WQ MsrAB from Neisseria gonorrhoeae (SEQ ID NO: 1). The His tag/WQ protease site is shown in italics. A coommassie-stained gel showing the predominant expressed species is also shown. The terms ngMsrAB and ngMsrAB-T are used interchangeably.

    [0046] FIG. 15 shows the sequence of His-tagged/WQ MsrAB from Neisseria meningitidis (SEQ ID NO: 2). The His tag/WQ protease site is shown in italics. A coommassie-stained gel showing the predominant expressed species is also shown. The terms nmMsrAB and nmMsrAB-T are used interchangeably.

    [0047] FIG. 16 shows how the theoretical reversal of methionine oxidation results in a less convoluted spectrum in top down protein MS/MS analysis.

    DETAILED DESCRIPTION

    [0048] This description and exemplary embodiments should not be taken as limiting. For the purposes of this specification and appended claims, unless otherwise indicated, all numbers expressing quantities, percentages, or proportions, and other numerical values used in the specification and claims, are to be understood as being modified in all instances by the term about, to the extent they are not already so modified. Accordingly, unless indicated to the contrary, the numerical parameters set forth in the following specification and attached claims are approximations that may vary depending upon the desired properties sought to be obtained. At the very least, and not as an attempt to limit the application of the doctrine of equivalents to the scope of the claims, each numerical parameter should at least be construed in light of the number of reported significant digits and by applying ordinary rounding techniques.

    [0049] It is noted that, as used in this specification and the appended claims, the singular forms a, an, and the, and any singular use of any word, include plural referents unless expressly and unequivocally limited to one referent. As used herein, the term include and its grammatical variants are intended to be non-limiting, such that recitation of items in a list is not to the exclusion of other like items that can be substituted or added to the listed items.

    [0050] As used herein, the terms methionine sulfoxide reductase, Msr, MetSR, and Msr enzyme are used interchangeably to refer to a methionine sulfoxide reductase that is capable of reducing methionine-S-sulfoxide and/or methionine-R-sulfoxide. A Msr domain that is capable of reducing methionine-S-sulfoxide to methionine is referred to as an A domain. A Msr domain that is capable of reducing methionine-R-sulfoxide to methionine is referred to as an B domain. Thus, the terms methionine sulfoxide reductase, Msr, MetSR, and Msr enzyme refer generically to a methionine sulfoxide reductase enzyme that comprises a methionine sulfoxide reductase A domain alone, B domain alone, or both an A domain and a B domain. In some embodiments, a Msr is a MsrAB. In some embodiments, a Msr is a MsrA. In some embodiments, a Msr is a MsrB.

    [0051] As used herein, the terms methionine sulfoxide reductase AB, MsrAB, MetSR-AB, and MsrAB enzyme are used interchangeably to refer to a methionine sulfoxide reductase comprising a methionine sulfoxide reductase A domain and a methionine sulfoxide reductase B domain, wherein the reductase is capable of reducing both methionine-S-sulfoxide and methionine-R-sulfoxide. In some embodiments, the MsrAB enzyme comprises a thioredoxin (Trx) domain. In some such embodiments, the MsrAB enzyme may be referred to as a MsrAB-T enzyme.

    [0052] The terms methionine sulfoxide reductase A, MsrA, MetSR-A, and MsrA enzyme are used interchangeably to refer to a methionine sulfoxide reductase comprising a methionine sulfoxide reductase A domain, wherein the reductase is capable of reducing methionine-S-sulfoxide.

    [0053] The terms methionine sulfoxide reductase B, MsrB, MetSR-B, and MsrB enzyme are used interchangeably to refer to a methionine sulfoxide reductase comprising a methionine sulfoxide reductase A domain, wherein the reductase is capable of reducing methionine-R-sulfoxide.

    [0054] As used herein protein, peptide, and polypeptide are used interchangeably throughout to mean a chain of amino acids wherein each amino acid is connected to the next by a peptide bond. In some embodiments, when a chain of amino acids consists of about two to fifty amino acids, the term peptide is used. However, the term peptide should not be considered limiting unless expressly indicated.

    [0055] In cells, methionine sulfoxides are reduced back to methionine by stereospecific reductases MsrA and MsrB (FIG. 1). The observed methionine-sulfoxide proteome represents a steady-state condition in which oxidation, a chemical event, is balanced by reduction, an enzymatic process. The Msr system protects cells against oxidative damage by a reactive oxygen species (ROS)-scavenging mechanism in which methionine residues in proteins function as catalytic antioxidants, and the methionine sulfoxide reductase enzymes then repair the damage to the reversibly oxidized proteins. The enzymatic reversal of methionine oxidation with purified MsrA and MsrB enzymes has been demonstrated in vitro and detected by gel mobility shift, Western blotting with methionine sulfoxide-specific antibodies, and by MS analysis of intact proteins. While some Msr enzymes utilize DTT and other reducing agents in vitro without supplementary enzymes, other Msr enzymes rely on reducing enzymes, such as thioredoxin and thioredoxin reductase with NADPH and reducing buffer conditions (e.g. dithiothreitol, DTT) in the reaction to maintain Msr catalytic activity.

    [0056] In some embodiments, the invention relates to the use of methionine sulfoxide reductase enzyme to reverse methionine oxidation in proteins and peptides prior to purification or analysis, such as liquid chromatography and/or mass spectrometry. In some embodiments, sample variability and complexity is reduced by the reversal of methionine oxidation and consolidation of multiple peptide species. In some embodiments, this enables easier interpretation of data, better sensitivity, and/or more accurate quantitation of proteins and peptides in samples, including biological samples.

    [0057] In some embodiments, nucleic acids encoding the Msr proteins are provided. In some embodiments, Msr proteins are provided which have enzymatic activity in a reducing buffer. Further, in some embodiments, methods for treating protein and peptide samples prior to MS analysis are provided. The present disclosure demonstrates that Msr proteins effectively reverse methionine oxidation and improve protein or peptide sample quality and MS results.

    [0058] In some embodiments, the reversal of methionine oxidation reduces the number of proteoforms with different masses and the consolidation into fewer intact masses increases the intensity and signal to noise of each form. See, e.g., FIGS. 2 to 7. In some instances, each intact mass may be composed of multiple forms of a protein with the same total number of oxidized methionines but at different positions. Such proteoforms appear as one intact mass but can produce a complex combination of unique fragment ions during MS/MS. This increased complexity complicates the data analysis and reduces the sensitivity because of the dilution of signal across many species. In some embodiments, the reversal of methionine oxidation by the methods described herein reduces sample complexity, reduces the data analysis time, and improves the quality and confidence in the results. See FIG. 16.

    [0059] In some instances, it is found that 10-30% of methionines are oxidized in complex proteomic samples after reduction, alkylation, fragmentation (e.g., digestion), and desalting. Methionine oxidation may occur in the cell before lysis, during cell lysis, and/or during the subsequent sample preparation or analysis. In some embodiments, since methionine sulfoxide reductase can be functional during the reduction of protein disulfides in a mass spectrometry workflow, it may be possible to reduce cysteine disulfides and oxidized methionine simultaneously. See FIG. 8. In some embodiments, after fragmentation (e.g., digestion), peptide samples are analyzed by mass spectrometry (MS), and the resulting spectra are compared with theoretical spectra from known proteins to determine the peptides and proteins in a sample. To avoid missing peptides, in some instances, MS database searches permit methionine oxidation as a variable modification, but such inclusion may double the database search time. Thus, in some embodiments, the methods provided herein can simplify the MS database searches and reduce the database search time. That is, in some embodiments, by reversing methionine oxidation, sample complexity is reduced, improving the database search scores, e.g., by reducing the degrees of freedom and number of false positive hits, and shortening the database search time by eliminating the need to search for methionine oxidation as a variable modification.

    [0060] Targeted quantitation of proteins with mass spectrometry is typically performed by quantifying specific unique peptides of the protein. In some embodiments, known amounts of isotope-labeled (e.g., heavy isotope-labeled) versions of these targeted peptides can be used as internal standards for absolute quantitation. In some instances, when choosing peptides for targeted MS assays, peptides containing methionine are avoided because of the potential for oxidation and the resulting variability in quantitative measurements. The avoidance of methionine-containing peptides limits the choice of peptides that can be used to quantify proteins, and may prevent the quantitation of specific peptides of interest, such as when methionine-containing peptides also contain important signaling or regulatory modifications, such as phosphorylation, methylation, acetylation, or ubiquitinylation. In some embodiments, treatment using methionine sulfoxide reductases according to the methods described herein can reverse methionine oxidation and permit the targeted quantification of methionine-containing peptides. See, e.g., FIGS. 11 to 13. In some embodiments, methionine oxidation can be removed without altering other modifications, so methionine sulfoxide reductase treatment permits methionine-containing peptides to be monitored with targeted MS assays that may be otherwise difficult or impossible to measure. See, e.g., FIG. 13.

    [0061] Nonlimiting exemplary Msr enzymes are described herein, and include MsrABs comprising the sequences of SEQ ID NOs: 10-34, and MsrABs that are at least 70%, at least 80%, at least 90%, at least 91%, at least 92%, at least 93%, at least 94%, at least 95%, at least 96%, at least 97%, at least 98%, at least 99%, or 100% identical to a sequence selected from SEQ ID NOs: 10-34.

    [0062] In some embodiments, the Msr enzyme is derived from a bacterial Msr enzyme. In some embodiments, the Msr enzyme is derived from a bacteria selected from Neisseria, Lautropia, Cardiobacterium, Gammaproteobacteria, Pelistega, Marinospirillum, Basilea, Oligella, Alcagenaceae, Psychrobacter, Brackiella, Taylorella, Moraxella, Enhydrobacter, Fusobacterium, Helcococcus, Paenibacillus, and Eremococcus. One skilled in the art can identify Msr enzymes from various bacterial sources. In some embodiments, the Msr enzyme is derived from a bacterial MsrAB enzyme, i.e., a bacterial enzyme comprising a methionine sulfoxide reductase A domain and a methionine sulfoxide reductase B domain. The bacterial Msr enzyme may optionally comprise a thioredoxin domain. In some embodiments, the Msr enzyme is derived from a Neisseria bacteria. In some embodiments, the Msr enzyme is derived from Neisseria gonorrhoeae, Neisseria meningitides, Neisseria lactamica, Neisseria polysaccharea, Neisseria flavescens, Neisseria sicca, Neisseria macacae, or Neisseria mucosa.

    [0063] In this application, ng denotes an MsrAB enzyme from Neisseria gonorrhoeae (e.g., ngMsrAB or ngMsrAB-T). In this application, nm denotes an MsrAB enzyme from Neisseria meningitides (e.g., nmMsrAB or nmMsrAB-T).

    [0064] In some embodiments, the Msr enzyme comprises an amino acid sequence that is at least 70%, at least 80%, at least 90%, at least 91%, at least 92%, at least 93%, at least 94%, at least 95%, at least 96%, at least 97%, at least 98%, at least 99%, or 100% identical to a sequence selected from SEQ ID NOs: 10-34.

    [0065] In some embodiments, the Msr enzyme is from a nonbacterial organism. In some embodiments, the Msr enzyme is derived from an Msr enzyme of an organism selected from Methanobrevibacter, Methanomassiliicoccales, Methanocorpusculum, Thermoplasmatales, Methanometylophilus, Methanoculleus, Methanocella, and the like. In some such embodiments, the Msr enzyme is an MsrAB enzyme. One skilled in the art can identify suitable MsrAB enzymes for use in the present methods. In some embodiments, the Msr enzyme from a non-Neisseriaceae bacteria or nonbacterial organism comprises an amino acid sequence that is at least 70%, at least 80%, or at least 90%, at least 91%, at least 92%, at least 93%, at least 94%, at least 95%, at least 96%, at least 97%, at least 98%, at least 99%, or 100% identical to a sequence selected from SEQ ID Nos: 10-34.

    [0066] In some embodiments, the Msr enzyme is an MsrA enzyme or an MsrB enzyme. One skilled in the art can identify suitable MsrA and/or MsrB enzymes for use in the methods described herein. In some embodiments, the MSR-A comprises a peptide-methionine (S)-S-oxide reductase. In some embodiments, an MsrA is derived from an MsrA enzyme of an organism selected from Haloarcula, Halococcus, Haloferax, Natronococcus, Natronomonas, and Natrinema. Nonlimiting exemplary such MsrA enzymes can be found in various protein databases and include, for example, MsrA enzymes under accession numbers WP_049944603.1, WP_005043086.1, WP_058572480.1, WP_015322392.1, WP_015408133.1, and WP_006431385.1. In some embodiments, an MsrA is at least 70%, at least 80%, or at least 90%, at least 91%, at least 92%, at least 93%, at least 94%, at least 95%, at least 96%, at least 97%, at least 98%, at least 99%, or 100% identical to an MsrA enzyme under accession number WP_049944603.1, WP_005043086.1, WP_058572480.1, WP_015322392.1, WP_015408133.1, or WP_006431385.1. In some embodiments, the Msr-B comprises a peptide-methionine (R)-S-oxide reductase. In some embodiments, an MsrB is derived from an MsrB enzyme of an organism selected from Haloarcula, Halococcus, Haloferax, Natronococcus, Natronomonas, Natrinema, and Candidatus Halobonum. Nonlimiting exemplary such MsrB enzymes can be found in various protein databases and include, for example, MsrB enzymes under accession numbers WP_004963222.1, WP_049996544.1, WP_007275637.1, WP_008423757.1, WP_015408129.1, WP_007109050.1, and WP_023395429.1. In some embodiments, an MsrB is at least 70%, at least 80%, or at least 90%, at least 91%, at least 92%, at least 93%, at least 94%, at least 95%, at least 96%, at least 97%, at least 98%, at least 99%, or 100% identical to an MsrA enzyme under accession number WP_004963222.1, WP_049996544.1, WP_007275637.1, WP_008423757.1, WP_015408129.1, WP_007109050.1, or WP_023395429.1. In some embodiments, MsrA and MsrB are derived from MsrA and MsrB enzymes of the same organism. In some embodiments, MsrA and MsrB are derived from MsrA and MsrB enzymes of the different organisms. In some embodiments, MsrA and MsrB are derived from MsrA and MsrB enzymes of organisms of the same genus, but different species.

    [0067] As used herein, an Msr enzyme that is derived from an Msr enzyme of a particular organism or of a particular sequence may be modified, such as by truncation or addition of amino acids (such as addition of a tag sequence and/or protease sequence for removal of the tag) relative to the parental Msr enzyme, but retains at least MsrA or MsrB activity. In some embodiments, the Msr enzyme derived from an Msr enzyme of a particular organism or of a particular sequence retains at least 50% of the MsrA or MsrB activity (but not necessarily both) of the parental enzyme.

    [0068] In some embodiments, a method comprises contacting a polypeptide sample with a mixture of different Msr's. In some embodiments, a single Msr is used. In some embodiments, when a mixture of Msrs is used, the mixture comprises at least one MsrA and at least one MsrB. In some embodiments, a method comprises contacting a polypeptide sample with an MsrAB, with or without additional Msrs. In some embodiments, an MsrAB may be used in conjunction with an MsrA and/or an MsrB.

    [0069] In some embodiments, an Msr:protein ratio (w/w) of 1:100 to 1:2 in used. In some embodiments, an Msr:protein ratio (w/w) of 1:2, 1:4, 1:10, 1:20, 1:25, 1:50, 1:66, 1:75 or 1:100 is used. In some embodiments, the Msr used is at a concentration of about 100 ng/ml-1 mg/ml, or about 100 ng/ml-500 g/ml, or about 100 ng/ml-100 g/ml, or about 1 g/ml-1 mg/ml, or about 1 g/ml-500 g/ml, or about 1 g/ml-100 g/ml, or about 10 g/mg-1 mg/ml, or about 10 g/mg-500 g/ml, or about 10 g/mg-100 g/ml. In some embodiments, the method comprises contacting a polypeptide sample with at least one Msr under conditions suitable for reduction of methionine sulfoxides for 10 minutes to 48 hours, or 30 minutes to 48 ours, or 30 minutes to 24 hours, or 30 minutes to 16 hours, or 1 hour to 48 hours, or 1 hour to 24 hours, or 1 hour to 16 hours, or 1 to 8 hours, or 1 to 6 hours, or 1 to 4 hours. In some embodiments, the Msr reaction is incubated at a temperature between 20 C. and 45 C., or between 20 C. and 40 C., or between 22 C. and 40 C., or between 25 C. and 37 C. In some embodiments, the Msr reaction is incubated at 37 C. or 30 C.

    [0070] In some embodiments, contacting the Msr with the polypeptide sample occurs under reducing conditions. In some embodiments, contacting of the Msr with the protein sample occurs in the presence of dithiothreitol (DTI) or dithioerythritol (DTE).

    [0071] In some embodiments, the Msr reaction is terminated. In some embodiments the Msr is removed following reduction of oxidized methionines in the protein sample. In some embodiments the Msr is removed by spinning or pelleting of the sample. In some such embodiments, the Msr enzyme is bound to a solid support, such as a resin or bead. The step to terminate the Msr reaction may occur before, after, or concurrently with a treatment to fragment (e.g., digest) the protein sample.

    [0072] Described herein are uses of methionine sulfoxide reductase (Msr) enzymes in the preparation of protein samples before purification or analysis, such as for liquid chromatography and/or mass spectrometry analysis. The reduction of oxidized methionine residues using Msr enzymes is shown to improve liquid chromatography and/or mass spectrometry data and simplify analysis.

    [0073] Mass spectrometry (MS) is a primary technique for analysis of proteins on the basis of their mass-to-charge ratio (m/z). MS techniques generally include ionization of compounds and optional fragmentation of the resulting ions, as well as detection and analysis of the m/z of the ions and/or fragment ions followed by calculation of corresponding ionic masses. A mass spectrometer generally includes an ionizer and an ion detector. Mass spectrometry, mass spec, mass spectroscopy, and MS are used interchangeably throughout.

    [0074] The methods disclosed herein may be applied to any type of MS analysis. The invention is not limited by the specific equipment or analysis used. The use of any equipment with the intent of analyzing the m/z of a sample would be included in the definition of mass spectrometry. Non-limiting examples of MS analysis and/or equipment that may be used include electrospray ionization, ion mobility, time-of-flight, tandem, ion trap, and Orbitrap. The invention is neither limited by the type of ionizer or detector used in the MS analysis nor by the specific configuration of the MS. The invention is not limited to use with the specific equipment and analysis described in the Examples.

    [0075] In some embodiments, the invention comprises use of an Msr enzyme for preparing a protein sample for top-down MS analysis, wherein the protein sample is contacted with an Msr enzyme prior to MS analysis. In some embodiments, the protein sample is intact (e.g., not fragmented) when contacted with an Msr enzyme. In some embodiments, the protein sample is not intact (e.g., fragmented) prior to Msr enzyme contact. In some embodiments, the invention comprises use of an Msr enzyme for preparing a protein sample for MS analysis, wherein the MS analysis comprises the step of disassociating intact protein or protein complexes. In some embodiments, the use comprises internal fragmentation of the proteins of the sample. The internal fragmentation step may be accomplished by way of Collision Induced Dissociation (CID), Electron Capture Dissociation (ECD), Electron Transfer Dissociation (ETD), or Surface Induced Dissociation (SID), for example. In some embodiments, the disassociating step is prior to Msr enzyme contact, whereas in some embodiments the disassociating step is after Msr enzyme contact.

    [0076] In top-down mass spectrometry analysis, intact proteins and/or protein complexes are subjected to fragmentation inside the mass spectrometer. In some instances, top-down analysis preserves the post-translationally modified forms of proteins. Further, in some instances, top-down analysis may provide close to 100% sequence coverage and may facilitate the study of coordinated regulation of multiple modification sites within a single protein. In some embodiments, top-down analysis has the ability to detect protein degradation products, sequence variants, and combination of post-translational modifications and their locations within the intact protein. Methionine oxidation presents a problem for top-down analysis because it increases sample complexity data analysis dramatically. For example, in some instances, each oxidized methionine can split the MS signal (e.g., into non-oxidized and oxidized peaks), a problem that is magnified by the number of methionines in a protein.

    [0077] In bottom-up mass spectrometry analysis, proteins in a sample are fragmented, for example, by enzymatic digestion using enzymes such as trypsin, and then identified, in some embodiments, using high performance liquid chromatography combined with mass spectrometry. In some embodiments, proteins are denatured, reduced to remove disulfide bonds, and then free cysteines are alkylated to prevent formation of new disulfide bonds. In some embodiments, the proteins are then fragmented. In some embodiments, the resulting peptides are then separated by liquid chromatography. Mass spectrometry may then be used to identify the peptides, e.g., by matching the fragmentation pattern to theoretical tandem mass spectrometry databases.

    [0078] Use of an Msr enzyme for preparing a protein sample may be combined with any other steps taken to prepare samples for MS analysis.

    [0079] In some embodiments, proteins within the sample are separated from other components of samples. In some embodiments, the proteins in the sample are not fragmented. In some embodiments, proteins in the sample are subjected to liquid chromatography before or after reduction of methionine sulfoxides according to the present methods. In some embodiments, proteins in the sample are subjected to capillary electrophoresis before or after reduction of methionine sulfoxides according to the present methods.

    [0080] In some embodiments, liquid chromatography (LC) is used for physical separation of protein samples. When LC is performed at relatively high pressure, it may be termed high performance liquid chromatography (HPLC). Nonlimiting exemplary LC includes reversed phase LC (RP-LC) and normal phase LC (NP-LC). In some embodiments, capillary electrophoresis (CE) is used for physical separation of protein samples.

    [0081] In some embodiments, LC may be used in conjunction with MS. In some such embodiments, an LC system may be linked to an MS (i.e., LC-MS or HPLC-MS), see Thompson M, AMC Technical Brief #34, 2008. In some embodiments, capillary electrophoresis (CE) may be used in conjunction with MS. In some embodiments, the LC-MS ionization technique is electrospray ionization (ESI), atmospheric pressure chemical ionization (APCI), or atmospheric pressure photoionization (APPI), see Basics of LCIMS, Agilent Technologies, 2001. Any type of mass analyzer may be used for LC-MS, including quadrupole, time-of-flight, ion trap, or Fourier transform-ion cyclotron resonance (FT-ICR or FT-MS). In some embodiments, LC-MS includes internal fragmentation during the MS analysis.

    [0082] In some embodiments, the protein sample comprises fragmented protein. In some embodiments, the fragmented protein sample includes proteins or peptides of a size that can be analyzed by the selected method. In some embodiments, a fragmented protein sample comprises peptide of 5 to 100 amino acids in length. In some embodiments, the protein sample comprises predominantly peptides of between 2-100, 5-100, 5-90, 5-80, 5-70, 5-60, 5-50, 5-40, 5-30, 10-90, 10-80, 10-70, 10-60, 10-50, 10-40, 10-30, or 10-20 amino acids in length. In some embodiments, the protein fragments comprises predominantly peptides of 5 to 50 amino acids in length.

    [0083] In some embodiments, the protein sample comprises protein fragments. In some such embodiments, the protein fragments are generated by an enzyme. In some embodiments, the protein sample comprises fragmented protein (e.g., protease-digested protein fragments).

    [0084] In some embodiments, a method provided herein comprises use of an Msr for preparing a protein sample for bottom-up MS analysis. In some embodiments, the protein sample contacted with the Msr is fragmented before or after treatment with the Msr.

    [0085] In some embodiments, a method provided herein comprises use of an Msr for preparing a protein sample for top-down MS analysis. In some embodiments, the protein is contacted with the Msr enzyme prior to fragmentation.

    [0086] In some embodiments, protein samples are denatured or solubilized before fragmentation.

    [0087] In some embodiments, the fragmentation protocol uses chemical cleavage. In some embodiments, the chemical cleavage uses CNBr. In some embodiments, the fragmentation protocol is done using an enzyme. In some embodiments, the fragmentation protocol uses MS-grade commercially available proteases. Examples of proteases that may be used to digest samples include trypsin, endoproteinase GluC, endoproteinase ArgC, pepsin, chymotrypsin, LysN protease, LysC protease, GluC protease, AspN protease, proteinase K, and thermolysin. In some embodiments, a mixture of different proteases are used and the individual results are combined together after the digestion and analysis. In some embodiments, the digestion is incomplete in order to see larger, overlapping peptides. In some embodiments, the antibody digestion is performed with IdeS, IdeZ, pepsin, or papain to generate large antibody domains for middle-down protein characterization. In some embodiments, the fragmentation protocol uses trypsin that is modified. In some embodiments, a protein:protease ratio (w/w) of 10:1, 20:1, 25:1, 50:1, 66:1, or 100:1 may be used. In some embodiments, the trypsin used is at a concentration of about 100 ng/ml-1 mg/ml, or about 100 ng/ml-500 g/ml, or about 100 ng/ml-100 g/ml, or about 1 g/ml-1 mg/ml, or about 1 g/ml-500 g/ml, or about 1 g/ml-100 g/ml, or about 10 g/mg-1 mg/ml, or about 10 g/mg-500 g/ml, or about 10 g/mg-100 g/ml. In some embodiments, the digestion step is for 10 minutes to 48 hours, or 30 minutes to 48 ours, or 30 minutes to 24 hours, or 30 minutes to 16 hours, or 1 hour to 48 hours, or 1 hour to 24 hours, or 1 hour to 16 hours, or 1 to 8 hours, or 1 to 6 hours, or 1 to 4 hours. In some embodiments, the digestion step is incubated at a temperature between 20 C. and 45 C., or between 20 C. and 40 C., or between 22 C. and 40 C., or between 25 C. and 37 C. In some embodiments, the digestion step is incubated at 37 C. or 30 C. In some embodiments, a step is included to end the digestion step. The step to end the digestion protocol may be addition of a stop solution or a step of spinning or pelleting of a sample. The step to end the digestion step may occur before, after, or concurrently with treatment with the Msr. In some embodiments, the digestion is followed by guanidation.

    [0088] In some embodiments, the fragmentation protocol includes use of protein gels. In some embodiments, the fragmentation protocol comprises in-gel digestion. An exemplary commercially available kit for performing in-gel digestion is the In-Gel Tryptic Digestion Kit (Thermo Fisher Cat#89871).

    [0089] In some embodiments, the fragmentation protocol is carried out in solution. An exemplary commercially available kit for performing in-solution digestion is the In-Solution Tryptic Digestion and Guanidiation Kit (Thermo Fisher Cat#89895).

    [0090] In some embodiments, the fragmentation protocol uses beads. In some embodiments, the fragmentation protocol comprises on-bead digestion. In some embodiments, agarose beads or Protein G beads are used. In some embodiments, magnetic beads are used.

    [0091] In some embodiments, protein samples are separated using liquid chromatography before MS analysis. In some embodiments, fragmented samples are separated using liquid chromatography before MS analysis.

    [0092] In some embodiments, kits are provided, comprising at least one methionine sulfoxide reductase (Msr) enzyme. In some embodiments, the at least one methionine sulfoxide reductase enzyme is capable of reducing methionine-S-sulfoxide, or is capable of reducing methionine-R-sulfoxide, or is capable of reducing both methionine-S-sulfoxide and methionine-R-sulfoxide. In some embodiments, the kit comprises at least one methionine sulfoxide reductase enzyme that is capable of reducing methionine-S-sulfoxide and at least one methionine sulfoxide reductase enzyme that is capable of reducing methionine-R-sulfoxide. In some such embodiments, the kit comprises an MsrA enzyme and an MsrB enzyme. In some embodiments, the kit comprises at least one methionine sulfoxide reductase enzyme that is capable of reducing both methionine-S-sulfoxide and methionine-R-sulfoxide, such as an MsrAB enzyme.

    [0093] Nonlimiting exemplary Msr enzymes that may be included in kits are described herein, and include, for example, MsrAB enzymes derived from a methionine sulfoxide reductase from an organism selected from Neisseria, Lautropia, Cardiobacterium, Gammaproteobacteria, Pelistega, Marinospirillum, Basilea, Oligella, Alcagenaceae, Psychrobacter, Brackiella, Taylorella, Moraxella, Enhydrobacter, Fusobacterium, Helcococcus, Paenibacillus, Eremococcus, Methanobrevibacter, Methanomassiliicoccales, Methanocorpusculum, Thermoplasmatales, Methanometylophilus, Methanoculleus, and Methanocella. In some embodiments, the MsrAB enzyme is derived from a bacterial enzyme. In some embodiments, the methionine sulfoxide reductase enzyme is derived from a methionine sulfoxide reductase enzyme of Neisseria gonorrhoeae, Neisseria meningitides, Neisseria lactamica, Neisseria polysaccharea, Neisseria flavescens, Neisseria sicca, Neisseria macacae, or Neisseria mucosa. In some embodiments, the methionine sulfoxide reductase enzyme comprises an amino acid sequence that is at least 70%, at least 80%, at least 90%, at least 91%, at least 92%, at least 93%, at least 94%, at least 95%, at least 96%, at least 97%, at least 98%, at least 99%, or 100% identical to a sequence selected from SEQ ID NOs: 10 to 34. In some embodiments, the one or more Msr enzymes in a kit may be bound to a solid support, such as a resin or bead.

    [0094] Kits may further comprises one or more additional reagents for preparing a polypeptide sample for liquid chromatography. Kits may further comprises one or more additional reagents for preparing a polypeptide sample for mass spectrometry analysis. In some embodiments, a kit comprises at least one reagent for fragmenting a polypeptide sample for mass spectrometry analysis. Nonlimiting exemplary reagents for fragmenting a polypeptide sample include trypsin, chymotrypsin, AspN, GluC, LysC, LysN, ArgC, proteinase K, thermolysin, and CNBr.

    EXAMPLES

    [0095] The following examples are provided to illustrate certain disclosed embodiments and are not to be construed as limiting the scope of this disclosure in any way.

    Example 1. Intact Protein Analysis and Top-Down Analysis of Methionine Oxidation of TurboLuc by Hydrogen Peroxide

    [0096] Methionine oxidation causes signal splitting of mass spectrometry (MS) of intact proteins, thus leading to increases in data complexities. Means of reducing methionine oxidation may thus improve MS data. Therefore, a model system was developed to study methionine oxidation and reduction that uses H.sub.2O.sub.2, which has been described as a means of monitoring methionine oxidation of methionine-rich proteins (see Le D T et al., Biochemistry 47(25):6685-6694 (2008) and Liang et al., BMC Biochemistry 13:21 (2012)).

    [0097] As shown in FIG. 1, oxidized methionines (i.e., methionine-S-sulfoxide and methionine-R-sulfoxide) can be reduced by methionine sulfoxide reductases (Msrs), such as MetSR-A and MetSR-B. The ability of Msr treatment to improve MS data by reduction of methionine oxidation was investigated using a variety of MS procedures.

    [0098] Turboluciferase (TurboLuc, SEQ ID No: 3) was selected for optimization of methionine oxidation and reduction reactions due to its compatibility with mass spectrometry. Initial experiments showed that treatment of 5 g/ml of TurboLuc with 1 mM, 10 mM, or 100 mM hydrogen peroxide reduced the activity of TurboLuc by greater than 1000-fold using the TurboLuc flash assay (data not shown), indicating that TurboLuc was susceptible to oxidation.

    [0099] For standardization of oxidation, a systematic ratio of moles of peroxide to moles of methionine must be maintained. Therefore, a concentration of 18 M TurboLuc was used for all experiments. As there are three moles of methionine per mole of TurboLuc, the methionine concentration in experiments was 54 M.

    [0100] A variety of oxidation conditions were assessed by determining the number of moles of methionine in a sample and adding different ratios of moles of peroxide to each. After oxidation, each sample had DIT added to a final concentration of 5 mM while keeping the solution at a neutral pH and either ngMsrAB or nmMsrAB were added. Ratios of methionine:peroxide of 10:1, 1:1, 1:10, 1:25, 1:75, 1:100, and 1:500 were examined using the following conditions:

    TABLE-US-00001 ngMsrAB-T or TLuc amount Molar Ratio Peroxide final nmMsrAB-T (g) (Sample:Peroxide) concentration added (g) 45 1:0 0 11.25 45 10:1 5.4 M 11.25 45 1:1 54 M 11.25 45 1:10 540 M 11.25 45 1:25 1.35 mM 11.25 45 1:50 2.7 mM 11.25 45 1:75 4.05 mM 11.25 45 1:100 5.4 mM 11.25 45 1:500 27 mM 11.25

    [0101] The incubation with hydrogen peroxide was at 37 C. for 1 hour. The sample was spun down using a using a 3K MWCO buffer exchange protein concentrator (Fisher, Product #11345402) for 1 hour at 16,000g. The sample was then buffer exchanged into a slightly basic solution of 50 mM Tris-HCl buffer and appropriate water to create a concentration of 0.5 g/L.

    [0102] Reduction reactions were performed by reacting the oxidized sample with methionine sulfoxide reductase (Msr) enzymes, using either ngMsrAB (SEQ ID No: 1) or nmMsrAB (SEQ ID No: 2). As shown in FIG. 14, SEQ ID No: 1 is an N-terminal histidine tagged protein with a WQ domain fused to the full-length MsrAB from Neisseria gonorrhoeae, also known as ngMsrAB. As shown in FIG. 15, SEQ ID No: 2 is an N-terminal histidine tagged protein with a WQ domain fused to the full-length MsrAB from Neisseria meningitides, also known as nmMsrAB. The Msr enzyme fusion proteins of SEQ ID Nos: 1 and 2 were expressed, purified, and used for determining the effect of methionine reduction on MS profiles. Coomassie gels shown in FIGS. 14 and 15 indicate that a predominant protein of the expected molecular weight was obtained for SEQ ID No: 1 (ngMsrAB) and SEQ ID No: 2 (nmMsrAB).

    [0103] To perform the reduction reactions, one of the two Msrs (either ngMsrAB [SEQ ID No: l] or nmMsrAB [SEQ ID No: 2]) was added to the oxidized TurboLuc solution at an enzyme:sample protein ratio of 1:4 and DTI of a final concentration of 5 mM. Both enzymes were used in separate experiments as shown below.

    TABLE-US-00002 Starting ngMsrAB-T nmMsrAB-T 5 mM DTT Samples Sample volume added volume added (from 100 mM (Methionine:Peroxide) Volume (45 g) (11.25 g total) (11.25 g total) Stock) Control 90 l 7.5 l 4.9 l Control 90 l 3.41 l 4.67 l 1:25 90 l 7.5 l 4.9 l 1:25 90 l 3.41 l 4.67 l 1:50 90 l 7.5 l 4.9 l 1:50 90 l 3.41 l 4.67 l 1:100 90 l 7.5 l 4.9 l 1:100 90 l 3.41 l 4.67 l

    [0104] The samples plus Msr were incubated at 37 C. for 2 hours with gentle vortexing throughout. Samples were cleaned using 3K MWCO concentrators, and the volume was brought up to 200 l with 0.1% formic acid.

    [0105] Half of the cleaned-up intact protein sample was diluted to 40% acetonitrile (ACN), 60% 0.1% formic acid for direct injection into the Orbitrap XL mass spectrometer. Manual selection of peaks and MS/MS fragmentation were performed.

    [0106] The other half of the cleaned-up intact protein sample was injected onto a ProSwift RP-4H 100 m25 cm monolithic column and separated by a gradient of water and acetonitrile in 0.1% formic acid. Automatic fragmentation was performed using data dependent analysis. Data analysis and visualization were done using ProSight Lite v1.2 Build 1.2.5595.15524 software that allows identification and characterization via intact protein analysis and top-down analysis.

    [0107] FIG. 2 shows MS data in the absence of hydrogen peroxide for un-oxidized samples and for samples treated with ngMsrAB or nmMsrAB. Peaks corresponding to native TurboLuc and oxidized TurboLuc are indicated with boxes. These data indicate a relatively low level of baseline methionine oxidation of TurboLuc.

    [0108] TurboLuc samples reacted with 10 peroxide treatment (10:1 peroxide:methionine, corresponding to 540 M H.sub.2O.sub.2) are shown in FIG. 3. The 10:1 peroxide to methionine reaction conditions did not produce pronounced differences from those obtained in the absence of hydrogen peroxide (FIG. 2). In addition, the 10:1 and 1:1 methionine to peroxide reaction conditions showed no detectable methionine oxidation (data not shown).

    [0109] FIG. 4 indicates that 25 peroxide treatment (25:1 peroxide:methionine corresponding to 1.35 mM H.sub.2O.sub.2) increased methionine oxidation of TurboLac. This is apparent in new peaks in spectrum region corresponding to oxidized TurboLac as well as larger relative abundance of the peaks corresponding to oxidized TurboLuc. Treatment with ngMsrAB or nmMsrAB (at a ratio of 1:4 of enzyme to sample) counteracted the effect of 25 peroxide treatment, and the MS data obtained with these samples were similar to those shown in FIG. 2 for un-oxidized sample not reacted with hydrogen peroxide.

    [0110] Data on increasingly concentrated hydrogen peroxide treatment are shown for 75 peroxide treatment (4.05 mM H.sub.2O.sub.2, FIG. 5), 100 peroxide treatment (5.4 mM H.sub.2O.sub.2, FIG. 6), and 500 peroxide treatment (27 mM H.sub.2O.sub.2, FIG. 7). Data with 75-500 peroxide treatment show increases in oxidized methionines in TurboLuc, as well as other modifications to TurboLuc such as oxidation of other amino acids, in oxidized samples that were not reduced. Treatment with ngMsrAB and nmMsrAB counteracted the effect of higher peroxide treatment on methionine oxidation of TurboLuc (for example, see FIG. 5), but treatment with these Msr enzymes did not affect doubly oxidized methionine sulfone or oxidation of other amino acids (for example, see FIG. 7) due to their specificity for methionine. Thus, higher levels of peroxide treatment produced other modifications that could not be counteracted by Msr treatment, such as oxidation of other amino acids, and that led to significant splitting of the signal.

    [0111] Data presented in FIGS. 4-7 outline successful conditions for reduction of methionine oxidation of TurboLac with Msr treatment using LC-MS for intact protein analysis. In all experiments, there was successful reversal of methionine oxidation of TurboLuc following peroxide treatment with use of the Msr enzymes ngMsrAB and nmMsrAB. The present protocol indicates that the hybrid Msr treatment is a novel means to improve MS analysis of intact proteins due to the reduction of methionine oxidation. Therefore, top-down proteomic analysis can be significantly improved by this novel use of Msr enzymes, such as ngMsrAB and nmMsrAB, to reduce the complexity of data induced by peak splitting of oxidized methionines.

    [0112] The protocol for top-down analysis of intact proteins was performed as follows. First, 24.6 l of 0.5M dithiothreitol (DTT) was added to 1.23 mL of 700 g/ml of whole protein to make a final DIT concentration of 10 mM and incubated for 1 hour at room temperature. Next, 126 l of 0.5M iodoacetamide (IAM) was added to the mixture to make a final IAM concentration of 50 mM, and the mixture was incubated in dark at room temperature for 20 minutes. Then, 126 l of 0.5M IAM was added to make a final IAM concentration of 50 mM, and the mixture was further incubated in dark at room temperature for 20 minutes. Next, 54.3 l of 0.5M DIT was added to bring its final concentration to 20 mM, and the mixture was incubated for 5 minutes at room temperature.

    [0113] The sample was spun down using a using a 3K MWCO buffer exchange protein concentrator (Fisher, Product #11345402) for 1 hour at 16,000g. The sample was then buffer exchanged into a slightly basic solution of 50 mM Tris-HCl buffer and appropriate water to create a concentration of 0.333 g/L. The preceding procedures were used to create a 500 l sample of 5 g/ml for each condition from a 10 g/ml TurboLuc stock sample for further steps for reduction of the methionines or for a control oxidized sample.

    [0114] FIG. 16 is a theoretical image presenting the tandem mass spectrometry (MS/MS) spectra for a native and Msr-treated protein. The theoretical native protein shows multiple oxidized (ox) peaks, while the Msr-treated protein contains a predominant peak that is non-oxidized. The starred region in the upper panels shows the m/z (mass-to-charge ratio) region selected for MS fragmentation. The lower panels show that the native protein has an MS/MS that is convoluted due to the large number of oxidized precursors that are shifting many of the MS/MS peaks by 16 Da for each oxidized methionine whereas proteins can have dozens of potentially oxidizable methionines. The number of oxidized methionines is indicative of the shift in m/z from the number (N) of 16 Da mass shifts. In contrast, the Msr-treated sample of the same protein shows a cleaner MS/MS spectrum, due to the fact that there is only one dominant precursor non-oxidized peak that was present in the m/z range selected for fragmentation.

    Example 2. Shotgun Proteomic Analysis Coupled with Reversal of Methionine Oxidation

    [0115] Next, reversal of methionine oxidation via Msr treatment together with shotgun proteomic analysis was investigated using a 6-protein standard (Thermo Scientific Pierce 6 Protein Digest, equimolar, LC-MS grade, Product 88342). Analysis of the 6-protein digested standard stored in liquid indicated that it was highly oxidized due to the long-term liquid storage.

    [0116] The process of shotgun proteomic analysis is outlined in FIG. 8. Proteins were digested and the resulting peptides were separated by LC followed by mass spectrometry.

    [0117] The Pierce 6 Protein Digest, equimolar, LC-MS grade (product #88342) was used as a complex digestion mixture with an estimated methionine concentration for oxidation and subsequent reduction by ngMsrAB or nmMsrAB. In addition, a non-oxidized peptide mixture was set-aside as a control to be reduced by ngMsrAB or nmMsrAB later in the protocol. The following conditions for the oxidation reactions are as follows:

    TABLE-US-00003 Sample Peroxide Volume Peroxide Concentration (l) Volume (Stock - Methionine:Peroxide Water (100 g) (l) 50.4 mM) ratio (l) 212.7 7.5 1.25 mM 1:25 79.8 212.7 15 2.52 mM 1:50 72.3 212.7 30 5.04 mM 1:100 57.3

    [0118] The incubation with hydrogen peroxide was at 37 C. for 1 hour. Then the sample was acidified as needed to obtain a pH4 before solid-phase extraction (SPE). SPE was performed using C18 (Sep-Pak vac 1 cc, C-18 cartridges) to clean up the peptide mixture and remove the peroxide using the following protocol. The column was washed with 1 ml of 80% acetonitrile, then equilibrated using 1 ml of 0.1% trifluoroacetic acid (TFA). Sample was then added and washed with 2.2 ml of 0.1% formic acid in water.

    [0119] The clean peptide sample was collected with 300 L 80% acetonitrile, and SpeedVac was used to dry the sample. The sample was re-suspended in 700 l of 0.1% formic acid, and a peptide concentration assay was done to determine the peptide concentration for further steps.

    [0120] After the peptide concentration was determined, Tris-HCl was added to a final concentration of 50 mM to produce a basic pH and appropriate water to create a concentration of 0.333 g/L. Samples were treated with ngMsrAB and nmMsrAB using the following conditions.

    TABLE-US-00004 5 mM Sample DTT Volume (from Samples (l) ngMsrAB-T nmMsrAB-T 100 mM (Methionine:Peroxide) (30 g) volume (l) volume (l) Stock) Control 90 l 7.5 l 4.9 l Control 90 l 3.41 l 4.67 l 1:25 90 l 7.5 l 4.9 l 1:25 90 l 3.41 l 4.67 l 1:50 90 l 7.5 l 4.9 l 1:50 90 l 3.41 l 4.67 l 1:100 90 l 7.5 l 4.9 l 1:100 90 l 3.41 l 4.67 l

    [0121] The peptide mixtures were then injected onto a C18 column (Acclaim PepMap 100 75 m100 m C18) and separated by a gradient of water and acetonitrile in 0.1% formic acid. The resulting liquid flow was infused into the Orbitrap XL mass spectrometer via electrospray ionization utilizing data dependent analysis for collection of MS/MS spectra.

    [0122] The resulting raw data were processed using Thermo Proteome Discoverer 1.4, and a database search was performed matching theoretical spectra to experimental spectra. For the database search, oxidation was selected as a variable modification or oxidation was not selected at all.

    [0123] FIG. 9 outlines the percentage of methionine oxidation seen with different methionine:peroxide ratios. Results are presented both for oxidized methionine (O) and doubly oxidized methionine (D). In addition, the ratio of oxidized methionines to total methionines is presented for each condition. For each methionine:peroxide ratio, one sample was included that did not include either ngMsrAB or nmMsrAB and thus provided a measure of 100% methionine oxidation for those conditions. As shown in FIG. 9, data confirmed high levels of methionine oxidation in all samples that were not treated with ngMsrAB or nmMsrAB.

    [0124] Treatment of samples with ngMsrAB or nmMsrAB at, 1:25, 1:50, and 1:100 methionine:peroxide ratios, as well as unoxidized control samples, were evaluated. Substantial reversal of methionine oxidation was seen with all methionine:peroxide ratios with approximately 80% reversal for all reaction ratios greater than 1:100. In contrast, the DTI control did not show any reversal of methionine oxidation, which confirms the specificity of treatment with ngMsrAB or nmMsrAB. In addition, there was approximately 70% sequence coverage with no loss of coverage based on the methionine reduction.

    [0125] There was an approximately 20% residual methionine oxidation even following treatment with ngMsrAB or nmMsrAB. This oxidation may be due to the electrospray ionization (ESI) using in the LC analysis, which has been shown to cause oxidation of solution-phase proteins (see Kim K et al., EuPA Open Proteomics 8:40-47 (2015)).

    [0126] These results with shotgun proteomics analysis following Msr treatment confirm the ability to reproducibly reduce methionine oxidation of a highly oxidized sample. Critically, this reduction of methionine oxidation occurred without sample loss. Normally, methionine oxidation is included as a permitted variable modification, compromising database searches following shotgun proteomic analysis. Therefore, treatment with ngMsrAB or nmMsrAB is a novel means to simplify and improve database searching for large shotgun discovery proteomics experiments by reducing the data variability induced by methionine oxidation.

    Example 3. Targeted Protein Analysis of Methionine Reduction by Parallel Reaction Monitoring

    [0127] Based on the results using shotgun proteomics, targeted protein analysis following reduction of methionine oxidation was investigated using parallel reaction monitoring (PRM). The basis of PRM is a targeted proteomics strategy where all fragmentation products of a target peptide are simultaneously monitored under conditions that offer high resolution and mass accuracy, as outlined in FIG. 10A (see also Peterson A C, et al., Molecular & Cellular Proteomics 11:1475-1488 (2012)). In PRM, the mass spectrometer isolates a target peptide ion and subjects it to fragmentation, followed by simultaneous analysis of the masses of all fragment ions. FIG. 10B shows representative experimental data wherein intensity is plotted against retention time to give a readout of the masses of all fragment ions.

    [0128] Quantitative PRM analysis was done using the Q Exactive HF Hybrid Quadrupole-Orbitrap Mass Spectrometer (QE-HF) (Thermo Fisher). The sample used to validate methionine reduction by Msr treatment was a 3-peptide mix prepared from commercially prepared peptide standards that included SEQ ID Nos: 4, 6, and 8 as listed in the following table.

    TABLE-US-00005 Sequenceandpost-translational SEQIDNos. modifications SEQIDNo:4 RTTSFAESCKPVQQPSAFGSMKV WhereinCindicatesacarbamidomethyl C,and WhereinMindicatesanoxidizedM SEQIDNo:5 RTTSFAESCKPVQQPSAFGSMKV WhereinCindicatesacarbamidomethyl C SEQIDNo:6 RTTSFAESCKPVQQPSAFGSMKV WhereinSindicatesaphosphorylated S, WhereinCindicatesacarbamidomethyl C,and WhereinMindicatesanoxidizedM SEQIDNo:7 RTTSFAESCKPVQQPSAFGSMKV WhereinSindicatesaphosphorylated S,and WhereinCindicatesacarbamidomethyl C SEQIDNo:8 RTESITATSPASMVGGKPGSFRV WhereinSindicatesaphosphorylated S,and WhereinMindicatesanoxidizedM SEQIDNo:9 RTESITATSPASMVGGKPGSFRV WhereinSindicatesaphosphorylatedS

    [0129] The three oxidized heavy peptides including both phosphorylated and non-phosphorylated peptides (100 fmol/l) were mixed with a digested 6-protein mix background matrix (40 ng/l, as described in Example 2) and IM tetraethylammonium bromide (TEAB) to a concentration of 2 mM to produce a slightly basic pH.

    [0130] The amount of sample, enzyme, water, and DTT added are shown below for each sample reacted with ngMsrAB or nmMsrAB:

    TABLE-US-00006 5 mM DTT Sample Enzyme from 100 mM Volume Volume stock Sample (l) (l) Water (l) Sample mix 100 7 l Control Sample mix 100 1 5.05 with ngMsrAB, 1 Sample mix 100 2.27 5.11 with nmMsrAB, 1 Sample mix 100 1 5.05 with ngMsrAB15 Sample mix 100 2.27 5.11 with nmMsrAB, 15

    [0131] The ratio of enzyme:protein was 1:4, and DTT had a final concentration of 5 mM for all reactions. Samples were incubated at 37 C. for 2 hours with gentle vortexing throughout. The resulting peptide mixture was then injected onto a C18 column (Easy-Spray PepMap C18, 3 m, 75 m150 cm) and separated by a gradient of water and acetonitrile in 0.1% formic acid.

    [0132] The resulting liquid flow was infused into the Q Exactive HF mass spectrometer via electrospray ionization utilizing parallel reaction monitoring for collection of targeted spectra. The resulting raw data were processed and visualized using Skyline 3.1.0.7382 open source PRM analysis software.

    [0133] FIG. 11A shows the disappearance of methionine oxidation of one peptide in the mix (SEQ ID No: 4) following treatment with ngMsrAB or nmMsrAB, while FIG. 11B shows the appearance of the peptide reduced at the methionine residue with treatment (SEQ ID No: 5). In FIGS. 11A and 11B, the bar graph areas show the cumulative area under the curve of individual b-ion and y-ion fragments (shown with different gray-scale shading) following treatment with ngMsrAB or nmMsrAB. These data indicate that greater than 90% reduction of an oxidized methionine is produced by treatment with the Msrs ngMsrAB or nmMsrAB, with a corresponding increase in the peptide with a reduced methionine. Note that oxidation of the cysteine residue of SEQ ID No: 4 and 5 was not affected by treatment with Msrs, as ngMsrAB or nmMsrAB are specific for reduction of oxidized methionines.

    [0134] Next, Msr treatment was performed on the phosphoprotein SEQ ID No: 6, wherein there is a phosphorylated serine residue in addition to an oxidized methionine and cysteine residue. Treatment of SEQ ID No: 6 with ngMsrAB or nmMsrABT produced a disappearance of SEQ ID No: 6 (as shown in FIG. 12A) and the appearance of the phosphopeptide SEQ ID No: 7 that retained phosphorylation of the serine and oxidation of cysteine residues, but had reduction of the methionine residue (as shown in FIG. 12B). These data indicate that Msr treatment with ngMsrAB or nmMsrAB can produce a quantitative reduction of methionine oxidation with high specificity such that other post-translational modifications (including cysteine oxidation and serine phosphorylation) are maintained.

    [0135] The specificity of Msr treatment was further confirmed with the third peptide in the 3-peptide mix, SEQ ID No: 8, which is also a phosphopeptide (i.e., the second phosphopeptide). SEQ ID No: 8 has both a phosphorylated serine and an oxidized methionine residue. As shown in FIG. 13A, Msr treatment with ngMsrAB or nmMsrAB produced a disappearance of SEQ ID No: 8. In contrast, FIG. 13B shows that these treatments caused the appearance of a reduced phophopeptide that lacked an oxidated methionine but maintained the serine phosphorylation (SEQ ID No: 9). These data confirm that Msr treatment with ngMsrAB or nmMsrAB is specific for reduction of oxidized methionine residues while maintaining the serine phosphorylation of treated peptides.

    [0136] As noted above, FIG. 16 is a theoretical image presenting the tandem mass spectrometry (MS/MS) spectra for a native and Msr-treated protein. The theoretical native protein shows multiple oxidized (ox) peaks, while the Msr-treated protein contains a predominant peak that is non-oxidized. The starred region in the upper panels shows the m/z (mass-to-charge ratio) region selected for MS fragmentation. The lower panels show that the native protein has an MS/MS that is convoluted due to the large number of oxidized precursors that are shifting many of the MS/MS peaks by 16 Daltons (Da) for each oxidized methionine whereas proteins can have dozens of potentially oxidizable methionines. The number of oxidized methionines is indicative of the shift in m/z from the number (N) of 16 Da mass shifts. In contrast, the Msr-treated sample of the same protein shows a cleaner MS/MS spectrum, due to the fact that there is only one dominant precursor non-oxidized peak that was present in the m/z range selected for fragmentation.

    [0137] The data in FIGS. 11, 12, and 13 indicate that Msr treatment with ngMsrAB or nmMsrAB can overcome variable oxidation of methionine residues in targeted analysis.

    [0138] The results described herein demonstrate that treatment with methionine sulfoxide reductase can simplify mass spectrometry analysis by reducing the occurrence of oxidized methionine, and the resulting analysis complexity.

    TABLE-US-00007 TABLEOFSEQUENCES SEQ IDNO Description Sequence 1 MsrABfromNeisseria HHHHHHSSGLVPRGSHMWELQLALGACSPKIVDAGAATVP gonorrhoeae,withHis HTLSTLKTADNRPASVYLKKDKPTLIKFWASWCPLCLSEL tag/WQproteasesite GQAEKWAQDAKFSSANLITVASPGFLHEKKDGEFQKWYAG LNYPKLPVVTDNGGTIAQNLNISVYPSWALIGKDGDVQRI VKGSINEAQALALIRNPNADLGSLKHSFYKPDTQKKDSAI MNTRTIYLAGGCFWGLEAYFQRIDGVVDAVSGYANGNTEN PSYEDVSYRHTGHAETVKVTYDADKLSLDDILQYYFRVVD PTSLNKQGNDTGTQYRSGVYYTDPAEKAVIAAALKREQQK YQLPLVVENEPLKNFYDAEEYHQDYLIKNPNGYCHIDIRK ADEPLPGKTKAAPQGKGFDAATYKKPSDAELKRTLTEEQY QVTQNSATEYAFSHEYDHLFKPGIYVDVVSGEPLFSSADK YDSGCGWPSFTRPIDAKSVTEHDDFSFNMRRTEVRSRAAD SHLGHVFPDGPRDKGGLRYCINGASLKFIPLEQMDAAGYG ALKGKVK 10 MsrABfromNeisseria LALGACSPKIVDAGAATVPHTLSTLKTADNRPASVYLKKD gonorrhoeae KPTLIKFWASWCPLCLSELGQAEKWAQDAKFSSANLITVA SPGFLHEKKDGEFQKWYAGLNYPKLPVVTDNGGTIAQNLN ISVYPSWALIGKDGDVQRIVKGSINEAQALALIRNPNADL GSLKHSFYKPDTQKKDSAIMNTRTIYLAGGCFWGLEAYFQ RIDGVVDAVSGYANGNTENPSYEDVSYRHTGHAETVKVTY DADKLSLDDILQYYFRVVDPTSLNKQGNDTGTQYRSGVYY TDPAEKAVIAAALKREQQKYQLPLVVENEPLKNFYDAEEY HQDYLIKNPNGYCHIDIRKADEPLPGKTKAAPQGKGFDAA TYKKPSDAELKRTLTEEQYQVTQNSATEYAFSHEYDHLFK PGIYVDVVSGEPLFSSADKYDSGCGWPSFTRPIDAKSVTE HDDFSFNMRRTEVRSRAADSHLGHVFPDGPRDKGGLRYCI NGASLKFIPLEQMDAAGYGALKGKVK 2 MsrABfromNeisseria HHHHHHSSGLVPRGSHMWELQLALGACSPKIVDAGAATVP meningitides,withHis HTLSTLKTADNRPASVYLKKDKPTLIKFWASWCPLCLSEL tag/WQproteasesite GQTEKWAQDAKFSSANLITVASPGFLHEKKDGDFQKWYAG LNYPKLPVVTDNGGTIAQSLNISVYPSWALIGKDSDVQRI VKGSINEAQALALIRDPNADLGSLKHSFYKPDTQKKDSKI MNTRTIYLAGGCFWGLEAYFQRIDGVVDAVSGYANGNTKN PSYEDVSYRHTGHAETVKVTYDADKLSLDDILQYFFRVVD PTSLNKQGNDTGTQYRSGVYYTDPAEKAVIAAALKREQQK YQLPLVVENEPLKNFYDAEEYHQDYLIKNPNGYCHIDIRK ADEPLPGKTKTAPQGKGFDAATYKKPSDAELKRTLTEEQY QVTQNSATEYAFSHEYDHLFKPGIYVDVVSGEPLFSSADK YDSGCGWPSFTRPIDAKSVTEHDDFSYNMRRTEVRSHAAD SHLGHVFPDGPRDKGGLRYCINGASLKFIPLEQMDAAGYG ALKGKVK 11 MsrABfromNeisseria LALGACSPKIVDAGAATVPHTLSTLKTADNRPASVYLKKD meningitides KPTLIKFWASWCPLCLSELGQTEKNAQDAKFSSANLITVA SPGFLHEKKDGDFQKWYAGLNYPKLPVVTDNGGTIAQSLN ISVYPSWALIGKDSDVQRIVKGSINEAQALALIRDPNADL GSLKHSFYKPDTQKKDSKIMNTRTIYLAGGCFWGLEAYFQ RIDGVVDAVSGYANGNTKNPSYEDVSYRHTGHAETVKVTY DADKLSLDDILQYFFRVVDPTSLNKQGNDTGTQYRSGVYY TDPAEKAVIAAALKREQQKYQLPLVVENEPLKNFYDAEEY HQDYLIKNPNGYCHIDIRKADEPLPGKTKTAPQGKGFDAA TYKKPSDAELKRTLTEEQYQVTQNSATEYAFSHEYDHLFK PGIYVDVVSGEPLFSSADKYDSGCGWPSFTRPIDAKSVTE HDDFSYNMRRTEVRSHAADSHLGHVFPDGPRDKGGLRYCI NGASLKFIPLEQMDAAGYGALKGKVK 12 Methioninesulfoxide FALGACSPKIADAEAATVPHTLSTLKTADNRPADVYLKKD reductase,Neisseria KPTLIKFWASWCPLCLSELGQTEKWAQDAKFGSANLITVA lactamica SPGFLHEKKDGDFQKWYAGLNYPKLPVVTDNGGTIAQSLN ISVYPSWALIGKDGDVQRIVKGSINEAQALALIRDPNADL GSLKHSFYKPDTQKKDSKIMNTRTIYLAGGCFWGLEAYFQ RIDGVVDAVSGYANGNTKNPSYEDVSYRHTGHAETVKVTY DADKLSLDDILQYYFRVVDPTSLNKQGNDTGTQYRSGVYY TDPAEKAVIAAALKREQQKYKLPLVVENEPLKNFYDAEEY HQDYLIKNPNGYCHIDIRKADEPLPGKTKTAPQGKGFDAA TYKKPSDAELKRTLTEEQYQVTQKSATEYAFSHEYDHLFK PGIYVDVVSGEPLFSSADKYDSGCGWPSFTRPIDAKSVTE HDDFSFNMRRTEVRSHAADSHLGHVFPDGPRDKGGLRYCI NGASLKFIPLEQMDAAGYGALKGKVK 13 Methioninesulfoxide FALGACSPKIADAEAATVPHTLSTLKTADNRPADVYLKKD reductase,Neisseria KPTLIKFWASWCPLCLSELGQTEKWAODAKFGSANLITVA polysaccharea SPGFLHEKKDGDFQKWYAGLNYPKLPVVTDNGGTIAQSLN ISVYPSWALIGKDGDVQRIVKGSINEAQALALIRDPNADL GSLKHSFYKPDTQKKDSKIMNTRTIYLAGGCFWGLEAYFQ RIDGVVDAVSGYANGNTKNPSYEDVSYRHTGHAETVKVTY DADKLSLDDILQYYFRVVDPTSLNKQGNDTGTQYRSGVYY TDPAEKTVIAAALKREQQKYKLPLVVENEPLKNFYDAEEY HQDYLIKNPNGYCHIDIRKADEPLPGKTKTAPQGKGFDAA TYKKPSDAELKRTLTEEQYQVTQHSATEYAFSHEYDHLFK PGIYVDVVSGEPLFSSADKYDSGCGWPSFTRPIDAKSVTE HDDFSYNMRRTEVRSHAADSHLGHVFPDGPRDKGGLRYCI NGASLKFIPLEQMDAAGYGALKGKVK 14 Methioninesulfoxide FALGACSPKTADAGAATVPHTLSTLKTADNRPAGVYLKKD reductase,Neisseria KPTLIKFWASWCPLCLSELGQTEKWAQDAKFGSANLITVA flavescens SPGFLHEKKDGDFQKWYAGLNYPKLPVVTDNGGTIAQSLN ISVYPSWALIGKDGDVQRIVKGSINEAQALALIRDPNADL GSLKHSFYKPDTQKKDSKIMNTRTIYLAGGCFWGLEAYFQ RIDGVVDAVSGYANGNTKNPSYEDVSYRHTGHAETVKVTY DADRLSLDDILQYYFRVVDPTSLNKQGNDTGTQYRSGVYY TDPAEKAVIAAALKREQQKYKLPLVVENEPLKNFYDAEEY HQDYLIKNPNGYCHIDIRKADEPLAGKTQTAPQGKGFDAA TYKKPSDAELKRTLTEEQYQVTQHSATEYAFSHEYDHLFK PGIYVDVVSGEPLFSSADKYDSGCGWPSFTRPIDAKSVTE HNDFSYNMRRTEVRSHAADSHLGHVFPDGPRDKGGLRYCI NGASLKFIPLEQMDAAGYGALKGKVK 15 Methioninesulfoxide FALGACSPKIADAEAATVPHTLSTLKTADNRPASVYLKKD reductase,Neisseria KPTLIKFWASWCPLCLSELGQTEKWAQDKRFSSANLITVA sicca SPGFLHEKKDGDFQKWYAGLNYPKLPVVTDNGGTIAQSLN ISVYPSWALIGKDGDVQRIVKGSINEAQALALIRDPNADL GRLKNAFYKPDTQKKDSKIMNTRTIYLAGGCFWGLEAYFQ RIDGVVDAVSGYANGKTKNPSYEDVSYRDTGHAETVKVTY DADKLSLDDILQYYFRVVDPTSLNKQGNDTGTQYRSGVYY TDPAEKAVIAAALKREQQKYKQPLVVENEPLKNFYDAEEY HQDYLIKNPNGYCHIDIRKADEPLPGKTKAAPQGKGFDAA TYKKPSDAELKRILTEEQYQVTQKSATEYAFSHEYDHLFK PGIYVDVVSGEPLFSSADKFDSGCGWPSFTRPINAAAVTE HDDFSYNMRRTEVRSHAADSHLGHVFPDGPKDKGGLRYCI NGASLKFIPLEQMDAAGYGALKGKVK 16 Methioninesulfoxide FALGACSPKIADAEAATVPHTLSTLKTADNRPASVYLRKD reductase,Neisseria KPTLIKFWASWCPLCLSELGQTEKWAQDKRFSSANLITVA macacae SPGFLHEKKDGDFQKWYAGLNYPKLPVVTDNGGTIAQSLN ISVYPSWALIGKDGDVQRIVKGSINEAQALALIRDPNADL GRLKNAFYKPDTQKKDSKIMNTRTIYLAGGCFWGLEAYFQ RIDGVVDAVSGYANGKTKNPSYEDVSYRDTGHAETVKVTY DADKLSLDDILQYYFRVVDPTSLNKQGNDTGTQYRSGVYY TDPAEKAVIAAALKREQQKYKQPLVVENEPLKNFYDAEEY HQDYLIKNPNGYCHIDIRKADEPLPGKTKAAPQGKGFDAA TYKKPSDAELKRILTEEQYQVTQKSATEYAFSHEYDHLFK PGIYVDVVSGEPLFSSADKFDSGCGWPSFTRPINAAAVTE HDDFSYNMRRTEVRSHAADSHLGHVFPDGPKDKGGLRYCI NGASLKFIPLEQMDAAGYGALKGKVK 17 Methioninesulfoxide FALGACSPKIADAEAATVPHTLSTLKTADNRPASVYLKKD reductase,Neisseria KPTLIKFWASWCPLCLSELGQTEKWAQDKRFSSANLITVA mucosa SPGFLHEKKDGDFQKWYAGLNYPKLPVVTDNGGTIAQSLN ISVYPSWALIGKDGDVQRIVKGSINEAQALALIRDPNADL GRLKNAFYKPDTQKKDSKIMNTRTIYLAGGCFWGLEAYFQ RIDGVVDAVSGYANGKTKNPSYEDVSYRDTGHAETVKVTY DADKLSLDDILQYYFRVVDPTSLNKQGNDTGTQYRSGVYY TDPAEKAVIAAALKREQQKYKQPLVIENEPLKNFYDAEEY HQDYLIKNPNGYCHIDIRKADEPLPGKTKAAPQGKGFDAA TYKKPSDAELKRILTEEQYQVTQKSATEYAFSHEYDHLFK PGIYVDVVSGEPLFSSADKFDSGCGWPSFTRPINAAAVTE HDDFTYNMRRTEVRSHAADSHLGHVFADGPQDKGGLRYCI NGASLKFIPLEQMDAAGYGALKGKVK 18 Methioninesulfoxide LALGACSSKIMDTEAATVPQALSSLKTPDNRPASVFLKKD reductase,Neisseria KPTLIKFWASWCPLCLSELGQTEKWAQDTKFGSANLITVA flavescens SPGFLHEKKDGDFQKWYAGLNYPKLPVVTDNGGTIAQSLN ISVYPSWALIGKDGDVQRIVKGSINEAQALALIRDPNADL GRLKNSFYKPDTQKKDSAIMNTRTIYLAGGCFWGLEAYFQ RIDGVVDAVSGYANGKTENPSYEDVSYRDTGHAETVKVTY DADKLSLDDILQYFFRVVDPTSLNKQGNDTGTQYRSGVYY TDPAEKAVIAAALKREQQKYKQPLVVENEPLKNFYDAEEY HQDYLIKNPNGYCHIDIRKADEPLPGKTKAAPQGKGFDAA TYKKPGAAELKRLLTEEQYQVTQNSATEYAFSHEYDHLFK PGIYVDVVSGEPLFSSADKFDSGCGWPSFTHPINASAVTE HDDFSYNMRRTEVRSHAADSHLGHVFPDGPKDKGGLRYCI NGASLKFIPLEQMDAAGYGALKGKVK 19 Methioninesulfoxide MIMRRLLTPRNLLLLVLLAVMFWSFYSGASPSHGTPPASA reductase,Lautropia DKAATAQGGGAAGAAQASDGAPEQPVGLPLAYLQKLKDVA mirabilis DKPATTYIKPGRPTLVKFWASWCPLCLSELADTNAWATDE RFSSAVNLVTLASPGFLHEKPQADFVTWYGGLDYPAMPVL LDVGGLLARQLGVRVYPSWVLLDADGGVARVVRGRLSEAQ ALALIEDPEADLARLAQAERASFYQPDSQKSSKVMNTKTI YLAGGCFWGVEAYFQRIPGVVDAVSGYANGRTQNPSYEDV IRGAGHAETVKVTYDADRLSLADILQYYFRIIDPTSLNKQ GNDRGAQYRTGVYYTDAADKATIQQALDALQQKYSRPLVV ENLPLQNFYEAEEYHQDYLAKNPNGYCHIDVRKADEPLPG KPAGNPPAAAAVGRGFDVASYRKASDAELKQRLSAEQYRV TQQSGTERAFTHEYDHLFAPGIYVDVVSGQPLFSSKDKFD SGCGWPSFTRPIQPSAVTEHEDLSYNMRRVEVRSQAADSH LGHVFPDGPRDKGGLRYCINGASLRFIPLEKMAEEGYGNL VDAVK 20 Methioninesulfoxide MKNPRQTLCSLIACVLFAGAVAPLPVLADAHASRAEAPLP reductase, HQLQQRLLALKDPRDQPAADYLDQSKPTLIKFWASWCPLC Cardiobacierium LATLEETQAWRGDKAFAGVNLVTIASPDHLGENDEATFKE hominis WYRGLDYPNLPVLVNNGGDIARDIGVAVYPSWALLDKNGN VARVIKGHINREQALALLANPQAELAQPAQKFYKPKPKGA TNMNTKTIHLAGGCFWGLEAYFERIPGVVDAVSGYANGKT KNPSYEDVSHRGTGHAETVKVTYDPERISLDDLLRYYFRV VDPTSLNQQGNDRGVQYRSGVYYTDPAERATIEKAFAEEQ KKHQKPLVVENLPLDNFYEAEEYHQDYLAKNPNGYCHIDI RKADIPLEKPAATAPAPAQTDANGEPVIDAAKYHKPDAAE LKQKLDAQAYEVTQNSATERAFSHEYDHLFAPGLYVDVVS GEPLFSSADKFQSGCGWPSFTKPINRAVVTEHDDTSYNMH RTEIRSRVADAHLGHVFPDGPKDKGGLRYCINGASLKFIP LAEMEKAGYGDLVDAVKKGEKL 21 Methioninesulfoxide MKNPRQTLCSLIACVLFAGAVAPLPVLADAHASRAEAPLP reductase, HQLQQRLLALKDPRDKPAADYLDQSKPTLIKFWASWCPLC Gammaproteobacteria LATLEETQAWRGDKAFAGVNLVTIASPDHLGENDEATFKE WYRGLDYPNLPVLVNNGGDIARDIGVAVYPSWALLDKNGN VARVIKGHINREQALALLANPQAELAQPAQKFYKPKPKGA TNMNTKTIHLAGGCFWGLEAYFERIPGVVDAVSGYANGKT KNPSYEDVSHRGTGHAETVKVTYDPERISLDDILRYYFRV VDPTSLNQQGNDRGVQYRSGVYYTDPAERATIEKAFAEEQ KKHQKPLVVENLPLDNFYEAEEYHQDYLAKNPNGYCHIDI RKADIPLEKPAATAPAPAQTDANGEPVIDATKYHKPDAAE LKKKLDAQAYEVTQNSATERAFSHEYDHLFAPGLYVDVVS GEPLFSSADKFQSGCGWPSFTKPINRAVVTEHDDTSYNMH RTEIRSRVADAHLGHVFPDGPKDKGGLRYCINGASLKFIP LAEMAKAGYGDLVDAVKKGEKL 22 Methioninesulfoxide MKSPLAKANKPNFFQQLTQLQPVTNGSSNMQFNNNRPTLV reductase, KLWASWCPLCLSELELTQSWANDPDFAQVNLTTLASPGVL Marinospirillum GELSLEEFKQWYAGLDYPDLPLQLDPSGELVKKLGVQVYP insulare SWAVLDAQGNLQRVVKGSINKAQALALIANPEADLKQLQT TFYQPKQPAQALPINTQSVYLAGGCFWGVEGYFERIDGVV DAVSGYANGRTENPSYEDVIYRNTGHAETVKVTYNSDKLS LDDILVYFFRIIDPTSLNKQGNDRGTQYRTGIYTTDPAEQ RLVATALARLEEEYTQPILVENLPLSGFYEAEEYHQDYLL KNPNGYCHVDLNKADIPLPNQLTNQSTDKNTPKPFDPNNF QKPDTASLKQRLTSEQFHVTQNNGTERAFTHEYDDLFEPG LYVDIVSGEPLFSSKDKYQAGCGWPSFVKPIEENALVEVV DTSYNMRRIEVRSRLADSHLGHVFPDGPKDRGGLRYCING ASLKFIPLAEMQAQGYGDWQALIN 23 methioninesulfoxide MPFLYFLRTIILGIMALYSSTLFAQTINFNALKDINNQKA reductase,Pelistega NFYIKNNKPTVVKFWASWCPLCLGELEQTEQWVQDKDFAM indica VNMVTLASPGYLGEKKAADFSQWALSLPYKKLPILIDTEQ TIAKSLNIRVYPSWVLLDSNGQLVKVVKGTLSKEQLLGVI KNPDAPIQKASTTFYKADTNSEHKKPIRTETIYLAGGCFW GLEGYFQRIPGVIDAVSGYANGNTQNPSYEDVVYRHTGHA ETVKVTYDIDKLSFADILEYYFRVIDPTSLNQQGNDKGTQ YRTGIYYTKADYQPLIAEAIKKEQTKYKKPIVVENKPLAN FYPAEEYHQDYLLKNPNGYCHIDLNKADEPLSTPSPKGFN MKEYKKPSQSELRQRLTPEQYRVTQESGTEYAFSHEYDEL FAPGLYVDIVSGQPLFSSDDKFNSHCGWPSFTQPIEKTVV TEHKDFSHNMYRIEVRSQAADSHLGHVFPDGPADRGGLRY CINGASLRFIPYADLDKEGYGEWKDKIKQK 24 methioninesulfoxide MKKIFALCVTLGIALVTLAFAKLPNSSTDKATQGADDKAF reductase,Basilea TYLLSLDDIHQQPAKQLIDTNRPTLVKLWASWCSSCLSEL psittacipulmonis DEVEAWSKDKRFKAINFVTVVSPSLYSEKNKDDFTKWFLS LDYPQTKVLLDTKGTLSRTLNIRAYPSWALFDEKGHLVRV IKGSISKVQALALIDNPQADLKSVQEKANRVTKKEVIDPM YQKTIYLAGGCFWGVEAYFERIDGVIDAVSGYANGRTENP KYEDVIYRHTGHAETVKVTFDTRRLSLADILQYYFRVIDP TSLNKQGNDRGTQYRTGVYYTDEKDKAVIDAALANEQKKY TKPLVVENLPLRNFYLAEDYHQDYLKKNPNGYCHIDISLA DRPLERGTNIDKPVRFWETYEKPSDNELRQQLSNEQYRIT QKNGTEYAFSHAYDHLFEPGLYVDIVSGEPLFTSTDKYDS GCGWPSFTQPIQAQAITEHEDLSYNMRRIEVRSRYADSHL GHVFPDGPSDKGGLRYCINGASLRFIPLEQMAAEGYAEFI PLIKKP 25 methioninesulfoxide MVQKIPHFFLSILFLTLTVLSLPAQSFSFSTKQHLGPRLE reductase,Oligella KLNDVQGVKATEFLQTSRPTLVKFWASWCPLCLATLEETR ureolytica DWRLDPDFSNTDIVTLASPGYLKEQSPKDFRQWYQGVNIE HLPVLVNDGGDLTREIGVSVYPSWALLDAQGRLQRVIKGH ITKEQALGLIADKDFDIQRSAPTFYRPSTDTAQQQKDKSN LMNSKEIYLAGGCFWGVEAYFERIPGVLDAISGYANGNTQ NPTYEQVIYMGTGHAETVKVVYDPERVDLETILRHFFRII DPTSLNRQGNDRGTQYRTGIYYTDASDAALITAALAREQS KWQKPLVVENEALDAFYVAEEYHQDYLAKNPNGYCHVDLN LVDQPLEKEEFELEMKSGENTQTMQNLKSEIRINPADYSV PSDEELRQKLSPLEYQVTQQNATERAFTHSYDNLYEPGIY VDIVSGEPLFSSDDKYDSGCGWPSFTKPIVPEVVTEHLDT TYNMQRIETRSRVADAHLGHVFPDGPRDRGGLRYCINGAS LKFIPKAEMAAAGYGDLLPLVSDK 26 methioninesulfoxide MHTLFRILSTLLFLSLSFFSFSAHSVGVSSQPHVGQRIAK reductase, LKDFQDKPATDYLKKGQPSLVKFWASWCPLCLATLEETRD Alcaligenaceae WRLDPDFAGVNIISLASPGYLNEQSPKEFRQWYRGVNFDN LPVIVNDGGELTRAIGISAYPSWGLIDAEGRLQRVIKGHI TKEQALALVADKDYEIKRKTPDFYRPSKDTAQQQKDKANL MKTKEIYLAGGCFWGVEAYFERIPGVVNAVSGYANGKTRQ PTYEQVIYMNTGHAETVKVVYDPERIDLETILRHYLRIID PTSLNRQGNDRGTQYRTGIYYSEPSDKDIITAVLAREQSK WERPIVVENQPLIAFDEAEEYHQDYLAKNPNGYCHIDLNL VDKPLAEEKTPLNLQNGSNTKAMQEHNAQSSITVNPADYH VPKEEELRKTLSPLSYQVTQQNATERAFTHPYDHLFEAGI YVDIVSGEPLFSSDDKYDSGCGWPSFTKPIVPEVITEHLD TSYNMQRIETRSRVADAHLGHVFPDGPRDRGGLRYCINGA ALKFIPKAEMEAAGYGYLLPLVSDK 27 methioninesulfoxide MSYKNNQKNSNHEEIKKPRSSSWLKNVSAFSMTTVLSAGI reductase, LVACGQMSNAESSASSSTKSGSQNTGVTSSRDMLPSDMLK Psychrobacterpiscatorii QMQALPQLTKGLGDTGAAVIDPNKPTLVKFWASWCPLCLG TLEETETWRTDPKFSGLNVVTVASPGHLNEKADGEFSTWY AGVQADYPKLPVLTDPSGELINKLGVQVYPSWAILDKNGN LVHLVKGNISAEQAYALAENAGNGFAELKAGNAKPANAQA SDNNKIETIKQKDGVYYNETGKPINTRSIYLAGGCFWGVE AYMERVDGVIDAVSGYANGDTANPSYEQVIRGSGHAETVK VTYDADKTDLDTILKYYFRVVDPTSLNKQGNDRGVQYRSG VYYTDKEDKAVIDAALKRVQSKYEQKVVVENEPLDNFYLA EMYHQDYLAKNPNGYCHIDLSLADDKPEGAARTKLAPVET IAETLDPKRYAKFDKDALKNTLTKAQYNITQEAGTERAFS HEYDDLFAPGIYVDVVSGEPLFLSTDKYQSGCGWPSFTKP IDIQVITQHQDTAFNMVRTEVRSRVADSHLGHVFPDGPKD RGGLRYCINGGALQFIPVDVMPQSGYAPLVKLVKS 28 methioninesulfoxide MLKQRQLPRFRSLGLSLSVLAVLLGLHSTRVLAAPQSQVA reductase,Brackiella PNSDLRSALGQLTTVTGQSGQNYLRADRPTLVKFWASWCP oedipodis LCLASLHETSAWSRDQDFAAFNIVSVAAPGYFNELPLEQF KHWFAGVDEADKKGLVVLLNEGGQLTRRLGIAAYPSWALL DRQGRLQRIVKGQLSKEQALGLLTNKDYSLKPAPKSFYKK SSASQQDSATLMNTKTIYLAGGCFWGVEAYFERIPGVVDA VSGYANGKSRHPSYEDVVYRNTGHAETVAVTYDPKQINLA QLLTHYFRLINPTSLNQQGNDRGTQYRTGIYYTDTADKAV ISRALADLQHHYKAPIVVENQPLAAFDKAEDYHQDYLAKN PNGYCHIDLRQADQPLSQEELKQVQHIQDATQTDASAPKS PELTPQRFKVPSPEELKKTLSPLAYDVTQNNATERAFTSE LDHVFEPGIYVDVVSGEPLFSSTDKFDSGCGWPSFTKPIK ADLITEHSDHSYNMIRTEVRSHTANSHLGHVFNDGPKDKG GLRYCINGAALKFIPKDKMQEAGYGDYLQYVK 29 methioninesulfoxide MGKFLKVLFSVFLVAATQIACSQAKSNSTLSQLKDVDNKS reductase,Taylorella FNIDSSKPTLIKFWASWCPLCLGELPDVENWYKDEAFKGV asinigenitalis NLVTIASPSYLSEKKEEAFKNWAKQSGIYKSGSFPIYVDP KGSHAKKWGIKVYPSWVLLDKNQQVQRIIKGSISKKQALA LINNKDANLMETEKKYYKESNNGESKIPLRTETIYLAGGC FWGVEAYFQKIPGIVDAVSGYANGNVENPHYRLVTTGTTG FTETVKITYDIDKIGIQEILAHYFRIIDPTSLNKQGNDRG TQYRTGIYYEKPEYKEIVAKALEDLQKKYSEPVVVENMQL KNFYMAEEYHQDYLIKNPNGYCHIDLSLADKPLEGVKKMK KGFDEASYVKPSDEELRKTLTPEQYRVTQEEGTEFAFSHE YDNLFEPGIYVDVVSGEPLFSSDDKYNSGCGWPSFSKPIE DDNIHEKKDFKIGYPRTEVRSSAADSHLGHVFNDGPKELG GLRYCINGASLRFIPYSEMKEQGYEEWMDKVKPIKGGATE VNKK 30 methioninesulfoxide MTKPRLRSHACAISLGIFASLSMLSACGKPNDIQTQSVTH reductase,Moraxella QDMLPSDTLAQLSALPQLTQGLGDTGKSVIDPNKPTLVKF catarrhalis WASWCPLCLSTLQETHDWRGDPNLAGFNIITVASPTHLNE KNTQDFTNWYQVLQADYPNLPVLIDSSGQLIKSLGIQVYP SWAILDKNGQLVYLSKGNLSVEQVSYLAKNPQALNELKAQ SHQTAMPTKDKDGVHYNDQGMPLNTKTIYLAGGCFWGVEA YFERIDGVVDAVSGYANGDETLKNPSYEQVIAGSGHAETV KVVYDADKMDLDTLLRYYFRIIDPTSVNKQGNDRGIQYRT GVYYTDPSDKAIIDNALNELQQKYKAPIVVENLPLSHFAL AEDYHQDYLTKNPNGYCHVDLSLANDKIVSKAQTLPKAST IQEALDPKRYQAFDKDNLKNTLTKAQYDITQNAGTERAFS HAYDHLFDDGLYVDIVSGEPLFLSTDKYNSGCGWPSFTKP IDPQVITEHTDTSYNMVRTEVRSRTADSHLGHVFPDGPKA RGGLRYCINGDALKFIPKADMDKHGYGALLPLIKPAQP 31 methioninesulfoxide MFLIKNLLECQLTAIFDALQIDEKCTMVNFPQSAKNLTIT reductase, LLISSLLLLGCQKMNAKENATYAGAASKADVLPTDTLATL Enhydrobacter QGLSQINPKLGKMGRHVIDPNKPTVVKFWASWCPLCLATL aerosaccus QESDAWAKQYPDMNVISVVSPGHLSEKSSQDFQTWYTVLA KDYANLAVLMDNNGKLIKQFGVQVYPSFAILDKQGNLLKL VKGNLTPTQIQALSDNASNDFAELKALNQAKTPYSQTAQA HEQANNQASKQAASIKALAPINHNGVYYQADGKTPIRTHT IYLAGGCFWGLEAYMERVDGVVDAISGYANGNSANPSYEQ VIAGSGHAETVKVIYDIDKTNLATLLAYYVRVIDPTSLNK QGNDRGAQYRTGIYYTDANDKPIIDKTLADLAKKYPQKIV VENKPLANFYDAENYHQDYLSKNPNGYCHIDINLANQKIP VIKSLAPATTVTEALNPSRYQNYDKNVKSRLTQAQYDVTQ NAATERAFSHQYDHLFAKGLYVDIVSGEPLFLSTDKYDSG CGWPSFTKPISANVITTSTDSSFNMTRTEVRSRVANSHLG HVFDDGPKDKGGLRYCINGDALQFIALADMQAAGYGALMP LVK 32 methioninesulfoxide MKKFYKIFLTFLFLIGGTMVFANRRGIENFELKTLDGKEY reductase, TLPKGKKVYLKAWASWCPICLSSLEELDSFTKEEDRIEIV Fusobacterium TVVFPGKSGEMSKEEFKKWYSSLGYKNIKVLVDEKGELLK mortiferum KARIRAFPTSIFIDETGEIKGVVPGQLPKEQILKIMGVDS QKKEEVVKKEDNVPVTSKNEGQKIEEIYLAGGCFWGVEAY MERIYGVVDAVSGYANGKTENPRYEDVVYRDTGHAETVKV TYDSNKISLSTLLEYYFRIVDPTSLNKQGNDRGTQYRTGI YYIKAEDEKVVTQALENLQKKYDKKVVIENKPLENFYLAE EYHQDYLKKNPNGYCHIDLNKANDIIVDASKYKKLSDKEL REKLSEKEYRITQLNDTERAFDNEYWNFFEPGIYVDITTG EPLFSSKDKYNSMCGWPSFTKPISEDVVTYHTDRSFNMVR TEVRSRVGDAHLGHVFEDGPKDKGGLRYCINSGALNFIPV DEMEKEGYGYLLKLVK 33 methioninesulfoxide MKKRFLLIVFAVIFSITACTSKRDVTNSDEKKKDEIRKQI reductase,Helcococcus DEIISQHQNENNDENPNDSIDYSKTKLKTIYLAGGCFWGV sueciensis EAYMEKVYGVADVVSGYANGNTENPTYEDVLYKNTEHAET VKVDYDPEKISLEKILDYYLLVVDPTSLNKQGNDRGTQYR SGVYFTDENERKIIEERLKKEQEKYKDKIVVEVQKLENFY EAEEYHQDYLKKNPNGYCHIDISKANEIIIDQSKYPKPSD EELKKKLTEAQYRVTQENDTEHAFSNEYWDNKEKGIYVDV ATGEPLFGSTDKYDSGCGWPSFTKPISKEVVTYHKDFSFN MERTEVRSRSGDSHLGHVFDDGPKESGGLRFCINSASIRF IPLEDMEKEGYGYLTHIIK 34 methioninesulfoxide MKKILLLMVLAATLLVTAYIVKANTTHNELANSEMTNKEM reduclase,Eremococcus THNEMKNDDTRNKIDEIITQQQKKSADENPNDAVDYSKAE coleocola LKTIYLAGGCFWGVEAYLEKVYGVADVVSGYANGDTENPT YEDVSYKNSGHAETVKVDYDPARISLEQILDYYLLVVDPT SMNRQGNDRGLQYRSGVYYTDESERKIIEERLNKEQAKYE DKIVVEVEKLDNFYEAEEYHQDYLKKNPNGYCHIDISKAN EVIIDQSKYPKPSDEELKKKLTDVQYKVTQENDTEHAFSN EYWDNKDKGIYVDVATGEPLFSSTDKFDSGCGWPSFSKPI AKEVVTYHTDLSYNMKRTEVRSRSGNSHLGHVFEDGPKEL GGLRYCINSASIRFVPLEEMEQEGYGYLTHLIK 3 TurboLuc MEAEAERGKLPGKKLPLEVLIELEANARKAGCTRGCLTCL SKIKCTAKMKKYIPGRCADYGGDKKIGQAGIVGAIVDIPE ISGFKEMEPMEQFIAQVDRCADCTTGCLKGLANVKCSDLL KKWLPGRCATFADKIQSEVDNIKGLAGD 4 Peptide1 RTTSFAESCKPVQQPSAFGSMKV, WhereinCindicatesancarbamidomethylC,and WhereinAindicatesanoxidizedM 5 Peptide1,reduced RTTSFAESCKPVQQPSAFGSMKV WhereinCindicatesancarbamidomethylC 6 Peptide2 RTTSFAESCKPVQQPSAFGSMKV WhereinSindicatesaphosphorylatedS, WhereinCindicatesancarbamidomethylC,and WhereinMindicatesanoxidizedM 7 Peptide2,reduced RTTSFAESCKPVQQPSAFGSMKV WhereinSindicatesaphosphorylatedS,and WhereinCindicatesanoxidizedC 8 Peptide3 RTESITATSPASMVGGKPGSFRV WhereinSindicatesaphosphorylatedS,and WhereinMindicatesanoxidizedM 9 Peptide3,reduced RTESITATSPASMVGGKPGSFRV WhereinSindicatesaphosphorylatedS 35 Msr-A,accession# mteqatfaggcfwctesvfkqidgvtdvvsgyagghvadp WP_049944603.1 syeavcreetghaecvqltydpeevsyedllavhftthtp ttkdregndvgtqyrsavfyhdeaqretvealieeiepgy dsdivtevepletfypaeeyhqdyfeknpdqsycqltipp kieklkqkhaella 36 Msr-A,accession# mateteratlaggcfwcieapmeeldgvhdvtsgyagght WP_005043086.1 enptyravcsgdtghaevvqieydpdriayedlldvlftv hdptqlnrqgpdvgtqyrsaifthdesqhetaaayidald aeggyddpvvteiepletfyeaseehqnyyeknpedaycs fhaqpkiekvrekfaekta 37 Msr-A,accession# messqtatfgggcfwcieaafkeldgisdvtsgyaggtve WP_058572480.1 nptyeqvcsgttghaeviqveydpsvvdydelldvffavh dptqlnrqgpdvgtqyrsivlyhdddqrrlaeayvealdd sydddvvtelapfetfyeaeayhqdyfeknpndaycqfha spkiekvrekfadklan 38 Msr-A,accession# meratfgggcfwcveaafeqlegvdsvtsgyagghtedpt WP_015322392.1 yeavcsgstghaevvqveynpdeiayedllevfftvhdpt tkdregpdvqsqyrsaiyahdeaqletaeafadeleaegl yegivteiepldtfyeaeqyhqnyfeknpndaycsmhaap kvetvrekfgenvapeh 39 Msr-A,accession# msdashddeletatlgggcfwcveavlkeldgvrsvtsgy WP_015408133.1 agghvedpsyeavcrgetghaevvqvafapetiafrdlle vfftihtpttlnregpdvgsqyrsavyyhndeqrrvvesv igeleplydddivtevepletfypaeeyhqdyfdknpsdt yctvnvnpklsklrekhaella 40 Msr-A,accession# meratfgggcfwcteaamkelegvdsvtsgyagghtedps WP_006431385.1 yrevcsgntghaevvqveydpdaigydellevffathdpt qlnrqgpdvgtqyrsivlyhdddqrtqaeayidaldseyd ddvvtelepletfyraeekhqdyfeknpndayctmhaapk vekvrekfaenvaaeh 41 Msr-B,accession# mseseeelpdkdeewreilsdeeyrilresgteprfssdl WP_004963222.1 idvedegvftcagcgtelfdsdrkfesetgwpsfwdvyqe gnvetradnshgmertevicaecgghlghvfddgpepsgk rycingaaldfese 42 Msr-B,accession# msnepattgelpetdeewrevltdeeyeilreqgtepkfs WP_049996544.1 gelldqhddgtfvcagcgtelfssdtkfesktgwpsfsdv adegnvelrrdtshgmertevvcatcgghlghvfddgpep tgkrycinsaalgfdgdes 43 Msr-B,accession# msdsefslsesewrerlsedayrvlreqgteprfsgehvd WP_007275637.1 rsddgvyrcagcgtelfdsetkydsncgwpsfyaaedsni elrrdlshgmdrtevvcstcgghlghvfddgpeptgkrfc insaaldfeadee 44 Msr-B,accession# msnepdvptddgewreeltdeqyrilreagteapfsgeyv WP_008423757.1 dhkddgsyacvgcgttlfdsetkfdsgcgwpsfsdvdddr vetrldtshgmrrtevlcancgghlghvfddgpeptgkry cinsavlefdge 45 Msr-B,accession# mdsklpqtdaewrevltdeeyrilreqgtepkfsgehlga WP_015408129A.1 dadgvyrcagcgaelfdsetkfdsnsgwpsfydaeegave lredrshgmvrtevvcarceghlghvfedgpdptgqrycm nsvalefddea 46 Msr-B,accession# msdesdhvptndeewrerlsdeeyrilreagtetpfsgey WP_007109050.1 vdhkadgsyacagcgaelfdsetkfdsgcgwpsfydaddd rietrtdtshgmrrtevvcancgghlghvfddgpeptgkr ycinsvalefde 47 Msr-B,accession# msetdetptderrsdeslpetddewrerlsdeeyeilrer WP_023395429.1 gtearfsgehvdrdddgvyecagcgtvifdsgtkydsgcg wpsfyaaddskvtlrdddrhgmsrvevlcancdghlghvf qdgpeptgerfcinsvaldfesrerad