A straightforward and efficient analytical pipeline for metaproteome characterization

Microbiome

Volumn 2, Issue 1, 2014, Pages

  Tanca, Alessandro ^a   Palomba, Antonio ^b   Pisanu, Salvatore ^a   Deligios, Massimo ^b   Fraumene, Cristina ^a   Manghina, Valeria ^b   Pagnozzi, Daniela ^a   Addis, Maria F ^a   Uzzau, Sergio ^a,b  

^a Porto Conte Ricerche Srl   (Italy)

^b UNIVERSITY OF SASSARI   (Italy)

Author keywords

Gut microbiota; LC MS MS; Mass spectrometry; Metaproteomics; Microbial community; Mouse; Protein extraction; Proteomic methods; Shotgun proteomics; Single run liquid chromatography

Indexed keywords

MEMBRANE PROTEIN; PROTEOME;

ARTICLE; COLONY FORMING UNIT; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; EXTRACTION; FREEZE THAWING; LACTOBACILLUS ACIDOPHILUS; LIQUID CHROMATOGRAPHY; MICROBIAL COMMUNITY; MICROBIOME; NONHUMAN; OPEN READING FRAME; PASTEURELLA MULTOCIDA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY;

EID: 84938483628     PISSN: None     EISSN: 20492618     Source Type: Journal    
DOI: 10.1186/s40168-014-0049-2     Document Type: Article

References (68)

1. Wilmes P, Bond PL. The application of two-dimensional polyacrylamide gel electrophoresis and downstream analyses to a mixed community of prokaryotic microorganisms. Environ Microbiol 2004, 6:911-920. 10.1111/j.1462-2920.2004.00687.x, 15305916.
2. VerBerkmoes NC, Denef VJ, Hettich RL, Banfield JF. Functional analysis of natural microbial consortia using community proteomics. Nat Rev Microbiol 2009, 7:196-205. 10.1038/nrmicro2080, 19219053.
3. Schneider T, Riedel K. Environmental proteomics: analysis of structure and function of microbial communities. Proteomics 2010, 10:785-798. 10.1002/pmic.200900450, 19953545.
4. Hettich RL, Sharma R, Chourey K, Giannone RJ. Microbial metaproteomics: identifying the repertoire of proteins that microorganisms use to compete and cooperate in complex environmental communities. Curr Opin Microbiol 2012, 15:373-380. 10.1016/j.mib.2012.04.008, 22632760.
5. Kolmeder CA, de Vos WM. Metaproteomics of our microbiome - developing insight in function and activity in man and model systems. J Proteomics 2014, 97:3-16. 10.1016/j.jprot.2013.05.018, 23707234.
6. Fouts DE, Pieper R, Szpakowski S, Pohl H, Knoblach S, Suh MJ, Huang ST, Ljungberg I, Sprague BM, Lucas SK, Torralba M, Nelson KE, Groah SL. Integrated next-generation sequencing of 16S rDNA and metaproteomics differentiate the healthy urine microbiome from asymptomatic bacteriuria in neuropathic bladder associated with spinal cord injury. J Transl Med 2012, 10:174. 10.1186/1479-5876-10-174, 22929533.
7. Chourey K, Jansson J, VerBerkmoes N, Shah M, Chavarria KL, Tom LM, Brodie EL, Hettich RL. Direct cellular lysis/protein extraction protocol for soil metaproteomics. J Proteome Res 2010, 9:6615-6622. 10.1021/pr100787q, 20954746.
8. Verberkmoes NC, Russell AL, Shah M, Godzik A, Rosenquist M, Halfvarson J, Lefsrud MG, Apajalahti J, Tysk C, Hettich RL, Jansson JK. Shotgun metaproteomics of the human distal gut microbiota. ISME J 2009, 3:179-189. 10.1038/ismej.2008.108, 18971961.
9. Kan J, Hanson TE, Ginter JM, Wang K, Chen F. Metaproteomic analysis of Chesapeake Bay microbial communities. Saline Systems 2005, 1:7. 10.1186/1746-1448-1-7, 16176596.
10. Keiblinger KM, Wilhartitz IC, Schneider T, Roschitzki B, Schmid E, Eberl L, Riedel K, Zechmeister-Boltenstern S. Soil metaproteomics - comparative evaluation of protein extraction protocols. Soil Biol Biochem 2012, 54:14-24. 10.1016/j.soilbio.2012.05.014, 23125465.
11. Leary DH, Hervey WJ, Li RW, Deschamps JR, Kusterbeck AW, Vora GJ. Method development for metaproteomic analyses of marine biofilms. Anal Chem 2012, 84:4006-4013. 10.1021/ac203315n, 22468925.
12. Benndorf D, Balcke GU, Harms H, von Bergen M. Functional metaproteome analysis of protein extracts from contaminated soil and groundwater. ISME J 2007, 1:224-234. 10.1038/ismej.2007.39, 18043633.
13. Singleton I, Merrington G, Colvan S, Delahunty JS. The potential of soil protein-based methods to indicate metal contamination. Appl Soil Ecol 2003, 23:25-32. 10.1016/S0929-1393(03)00004-0.
14. Ogunseitan OA. Direct extraction of catalytic proteins from natural microbial communities. J Microbiol Methods 1997, 28:55-63. 10.1016/S0167-7012(96)00962-1.
15. Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G, Roschitzki B, Richter A, Eberl L, Zechmeister-Boltenstern S, Riedel K. Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J 2012, 6:1749-1762. 10.1038/ismej.2012.11, 22402400.
16. Klaassens ES, de Vos WM, Vaughan EE. Metaproteomics approach to study the functionality of the microbiota in the human infant gastrointestinal tract. Appl Environ Microbiol 2006, 73:1388-1392. 10.1128/AEM.01921-06, 17158612.
17. Kolmeder CA, de Been M, Nikkilä J, Ritamo I, Mättö J, Valmu L, Salojärvi J, Palva A, Salonen A, de Vos WM. Comparative metaproteomics and diversity analysis of human intestinal microbiota testifies for its temporal stability and expression of core functions. PLoS One 2012, 7:e29913. 10.1371/journal.pone.0029913, 22279554.
18. Abram F, Gunnigle E, O'Flaherty V. Optimisation of protein extraction and 2-DE for metaproteomics of microbial communities from anaerobic wastewater treatment biofilms. Electrophoresis 2009, 30:4149-4151. 10.1002/elps.200900474, 19960479.
19. Tang Y, Underwood A, Gielbert A, Woodward MJ, Petrovska L. Metaproteomics analysis reveals the adaptation process for the chicken gut microbiota. Appl Environ Microbiol 2014, 80:478-485. 10.1128/AEM.02472-13, 24212578.
20. Sharma R, Dill BD, Chourey K, Shah M, Verberkmoes NC, Hettich RL. Coupling a detergent lysis/cleanup methodology with intact protein fractionation for enhanced proteome characterization. J Proteome Res 2012, 11:6008-6018. 23126408.
21. Fic E, Kedracka-Krok S, Jankowska U, Pirog A, Dziedzicka-Wasylewska M. Comparison of protein precipitation methods for various rat brain structures prior to proteomic analysis. Electrophoresis 2010, 31:3573-3579. 10.1002/elps.201000197, 20967768.
22. Jiang L, He L, Fountoulakis M. Comparison of protein precipitation methods for sample preparation prior to proteomic analysis. J Chromatogr A 2004, 1023:317-320. 10.1016/j.chroma.2003.10.029, 14753699.
23. Haange S-B, Oberbach A, Schlichting N, Hugenholtz F, Smidt H, von Bergen M, Till H, Seifert J. Metaproteome analysis and molecular genetics of rat intestinal microbiota reveals section and localization resolved species distribution and enzymatic functionalities. J Proteome Res 2012, 11:5406-5417. 10.1021/pr3006364, 23016992.
24. Ferrer M, Ruiz A, Lanza F, Haange SB, Oberbach A, Till H, Bargiela R, Campoy C, Segura MT, Richter M, von Bergen M, Seifert J, Suarez A. Microbiota from the distal guts of lean and obese adolescents exhibit partial functional redundancy besides clear differences in community structure. Environ Microbiol 2013, 15:211-226. 10.1111/j.1462-2920.2012.02845.x, 22891823.
25. Taubert M, Vogt C, Wubet T, Kleinsteuber S, Tarkka MT, Harms H, Buscot F, Richnow H-H, von Bergen M, Seifert J. Protein-SIP enables time-resolved analysis of the carbon flux in a sulfate-reducing, benzene-degrading microbial consortium. ISME J 2012, 6:2291-2301. 10.1038/ismej.2012.68, 22791237.
26. Choksawangkarn W, Edwards N, Wang Y, Gutierrez P, Fenselau C. Comparative study of workflows optimized for in-gel, in-solution, and on-filter proteolysis in the analysis of plasma membrane proteins. J Proteome Res 2012, 11:3030-3034. 10.1021/pr300188b, 22500775.
27. Wiśniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods 2009, 6:359-362. 10.1038/nmeth.1322, 19377485.
28. Perez-Cobas AE, Gosalbes MJ, Friedrichs A, Knecht H, Artacho A, Eismann K, Otto W, Rojo D, Bargiela R, von Bergen M, Neulinger SC, Däumer C, Heinsen FA, Latorre A, Barbas C, Seifert J, dos Santos VM, Ott SJ, Ferrer M, Moya A. Gut microbiota disturbance during antibiotic therapy: a multi-omic approach. Gut 2013, 62:1591-1601. 10.1136/gutjnl-2012-303184, 23236009.
29. Ram RJ, Verberkmoes NC, Thelen MP, Tyson GW, Baker BJ, Blake RC, Shah M, Hettich RL, Banfield JF. Community proteomics of a natural microbial biofilm. Science 2005, 308:1915-1920. 10.1126/science. 1109070, 15879173.
30. Köcher T, Pichler P, Swart R, Mechtler K. Analysis of protein mixtures from whole-cell extracts by single-run nanoLC-MS/MS using ultralong gradients. Nat Protoc 2012, 7:882-890. 10.1038/nprot.2012.036, 22498708.
31. Thakur SS, Geiger T, Chatterjee B, Bandilla P, Frohlich F, Cox J, Mann M. Deep and highly sensitive proteome coverage by LC-MS/MS without prefractionation. Mol Cell Proteomics 2011, 10:M110.003699. 10.1074/mcp.M110.003699, 21586754.
32. Nagaraj N, Kulak NA, Cox J, Neuhauser N, Mayr K, Hoerning O, Vorm O, Mann M. System-wide perturbation analysis with nearly complete coverage of the yeast proteome by single-shot ultra HPLC runs on a bench top Orbitrap. Mol Cell Proteomics 2012, 11:M111.013722. 10.1074/mcp.M111.013722, 22021278.
33. Pirmoradian M, Budamgunta H, Chingin K, Zhang B, Astorga-Wells J, Zubarev RA. Rapid and deep human proteome analysis by single-dimension shotgun proteomics. Mol Cell Proteomics 2013, 12:3330-3338. 10.1074/mcp.O113.028787, 23878402.
34. Yu Y, Suh MJ, Sikorski P, Kwon K, Nelson KE, Pieper R. Urine sample preparation in 96-well filter plates for quantitative clinical proteomics. Anal Chem 2014, 86:5470-5477. 10.1021/ac5008317, 24797144.
35. Lanigan MD, Vaughan JA, Shiell BJ, Beddome GJ, Michalski WP. Mycobacterial proteome extraction: comparison of disruption methods. Proteomics 2004, 4:1094-1100. 10.1002/pmic.200300672, 15048990.
36. de Boer R, Peters R, Gierveld S, Schuurman T, Kooistra-Smid M, Savelkoul P. Improved detection of microbial DNA after bead-beating before DNA isolation. J Microbiol Methods 2010, 80:209-211. 10.1016/j.mimet.2009.11.009, 19995580.
37. Salonen A, Nikkila J, Jalanka-Tuovinen J, Immonen O, Rajilic-Stojanovic M, Kekkonen RA, Palva A, de Vos WM. Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: effective recovery of bacterial and archaeal DNA using mechanical cell lysis. J Microbiol Methods 2010, 81:127-134. 10.1016/j.mimet.2010.02.007, 20171997.
38. Sasidharan K, Amariei C, Tomita M, Murray DB. Rapid DNA, RNA and protein extraction protocols optimized for slow continuously growing yeast cultures. Yeast 2012, 29:311-322. 10.1002/yea.2911, 22763810.
39. Erickson AR, Cantarel BL, Lamendella R, Darzi Y, Mongodin EF, Pan C, Shah M, Halfvarson J, Tysk C, Henrissat B, Raes J, Verberkmoes NC, Fraser CM, Hettich RL, Jansson JK. Integrated metagenomics/metaproteomics reveals human host-microbiota signatures of Crohn's disease. PLoS One 2012, 7:e49138. 10.1371/journal.pone.0049138, 23209564.
40. Meyer F, Paarmann D, D'Souza M, Olson R, Glass E, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA. The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 2008, 9:386. 10.1186/1471-2105-9-386, 18803844.
41. Del Chierico F, Petrucca A, Mortera SL, Vernocchi P, Rosado MM, Pieroni L, Carsetti R, Urbani A, Putignani L. A metaproteomic pipeline to identify newborn mouse gut phylotypes. J Proteomics 2014, 97:17-26. 10.1016/j.jprot.2013.10.025, 24176786.
42. Krych L, Hansen CH, Hansen AK, van den Berg FW, Nielsen DS. Quantitatively different, yet qualitatively alike: a meta-analysis of the mouse core gut microbiome with a view towards the human gut microbiome. PLoS One 2013, 8:e62578. 10.1371/journal.pone.0062578, 23658749.
43. Noinaj N, Guillier M, Barnard TJ, Buchanan SK. TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 2010, 64:43-60. 10.1146/annurev.micro.112408.134247, 20420522.
44. Krewulak KD, Vogel HJ. TonB or not TonB: is that the question?. Biochem Cell Biol 2011, 89:87-97. 10.1139/O10-141, 21455261.
45. Miethke M, Marahiel MA. Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 2007, 71:413-451. 10.1128/MMBR.00012-07, 17804665.
46. Noinaj N, Easley NC, Oke M, Mizuno N, Gumbart J, Boura E, Steere AN, Zak O, Aisen P, Tajkhorshid E, Evans RW, Gorringe AR, Mason AB, Steven AC, Buchanan SK. Structural basis for iron piracy by pathogenic Neisseria . Nature 2012, 483:53-58. 10.1038/nature10823, 22327295.
47. Hansen JJ, Huang Y, Peterson DA, Goeser L, Fan TJ, Chang EB, Sartor RB. The colitis-associated transcriptional profile of commensal Bacteroides thetaiotaomicron enhances adaptive immune responses to a bacterial antigen. PLoS One 2012, 7:e42645. 10.1371/journal.pone.0042645, 22880065.
48. Yamada T, Letunic I, Okuda S, Kanehisa M, Bork P. iPath2.0: interactive pathway explorer. Nucleic Acids Res 2011, 39:W412-W415. 10.1093/nar/gkr313, 21546551.
49. Drake HL, Gossner AS, Daniel SL. Old acetogens, new light. Ann N Y Acad Sci 2008, 1125:100-128. 10.1196/annals.1419.016, 18378590.
50. Rey FE, Faith JJ, Bain J, Muehlbauer MJ, Stevens RD, Newgard CB, Gordon JI. Dissecting the in vivo metabolic potential of two human gut acetogens. J Biol Chem 2010, 285:22082-22090. 10.1074/jbc.M110.117713, 20444704.
51. Ragsdale SW, Pierce E. Acetogenesis and the Wood-Ljungdahl pathway of CO(2) fixation. Biochim Biophys Acta 2008, 1784:1873-1898. 10.1016/j.bbapap.2008.08.012, 18801467.
52. Deplancke B, Hristova KR, Oakley HA, McCracken VJ, Aminov R, Mackie RI, Gaskins HR. Molecular ecological analysis of the succession and diversity of sulfate-reducing bacteria in the mouse gastrointestinal tract. Appl Environ Microbiol 2000, 66:2166-2174. 10.1128/AEM.66.5.2166-2174.2000, 10788396.
53. Barton LL, Fauque GD. Biochemistry, physiology and biotechnology of sulfate-reducing bacteria. Adv Appl Microbiol 2009, 68:41-98. 10.1016/S0065-2164(09)01202-7, 19426853.
54. Muyzer G, Stams AJ. The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 2008, 6:441-454. 18461075.
55. Carbonero F, Benefiel AC, Alizadeh-Ghamsari AH, Gaskins HR. Microbial pathways in colonic sulfur metabolism and links with health and disease. Front Physiol 2012, 3:448. 10.3389/fphys.2012.00448, 23226130.
56. Willis CL, Cummings JH, Neale G, Gibson GR. Nutritional aspects of dissimilatory sulfate reduction in the human large intestine. Curr Microbiol 1997, 35:294-298. 10.1007/s002849900257, 9462959.
57. Daniel H, Moghaddas Gholami A, Berry D, Desmarchelier C, Hahne H, Loh G, Mondot S, Lepage P, Rothballer M, Walker A, Böhm C, Wenning M, Wagner M, Blaut M, Schmitt-Kopplin P, Kuster B, Haller D, Clavel T. High-fat diet alters gut microbiota physiology in mice. ISME J 2014, 8:295-308. 10.1038/ismej.2013.155, 24030595.
58. McNulty NP, Wu M, Erickson AR, Pan C, Erickson BK, Martens EC, Pudlo NA, Muegge BD, Henrissat B, Hettich RL, Gordon JI. Effects of diet on resource utilization by a model human gut microbiota containing Bacteroides cellulosilyticus WH2, a symbiont with an extensive glycobiome. PLoS Biol 2013, 11:e1001637. 10.1371/journal.pbio.1001637, 23976882.
59. Seifert J, Herbst FA, Halkjaer Nielsen P, Planes FJ, Jehmlich N, Ferrer M, von Bergen M. Bioinformatic progress and applications in metaproteogenomics for bridging the gap between genomic sequences and metabolic functions in microbial communities. Proteomics 2013, 13:2786-2804. 23625762.
60. Tanca A, Palomba A, Deligios M, Cubeddu T, Fraumene C, Biosa G, Pagnozzi D, Addis MF, Uzzau S. Evaluating the impact of different sequence databases on metaproteome analysis: insights from a lab-assembled microbial mixture. PLoS One 2013, 8:e82981. 10.1371/journal.pone.0082981, 24349410.
61. Cantarel BL, Erickson AR, VerBerkmoes NC, Erickson BK, Carey PA, Pan C, Shah M, Mongodin EF, Jansson JK, Fraser-Liggett CM, Hettich RL. Strategies for metagenomic-guided whole-community proteomics of complex microbial environments. PLoS One 2011, 6:e27173. 10.1371/journal.pone.0027173, 22132090.
62. Scupham AJ, Presley LL, Wei B, Bent E, Griffith N, McPherson M, Zhu F, Oluwadara O, Rao N, Braun J, Borneman J. Abundant and diverse fungal microbiota in the murine intestine. Appl Environ Microbiol 2006, 72:793-801. 10.1128/AEM.72.1.793-801.2006, 16391120.
63. Hoffmann C, Dollive S, Grunberg S, Chen J, Li H, Wu GD, Lewis JD, Bushman FD. Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PLoS One 2013, 8:e66019. 10.1371/journal.pone.0066019, 23799070.
64. Apajalahti JH, Sarkilahti LK, Maki BR, Heikkinen JP, Nurminen PH, Holben WE. Effective recovery of bacterial DNA and percent-guanine-plus-cytosine-based analysis of community structure in the gastrointestinal tract of broiler chickens. Appl Environ Microbiol 1998, 64:4084-4088. 9758849.
65. Wilke A, Harrison T, Wilkening J, Field D, Glass EM, Kyrpides N, Mavrommatis K, Meyer F. The M5nr: a novel non-redundant database containing protein sequences and annotations from multiple sources and associated tools. BMC Bioinformatics 2012, 13:141. 10.1186/1471-2105-13-141, 22720753.
66. Tanca A, Biosa G, Pagnozzi D, Addis MF, Uzzau S. Comparison of detergent-based sample preparation workflows for LTQ-Orbitrap analysis of the Escherichia coli proteome. Proteomics 2013, 13:2597-2607. 10.1002/pmic.201200478, 23784971.
67. Olsen JV, de Godoy LM, Li G, Macek B, Mortensen P, Pesch R, Makarov A, Lange O, Horning S, Mann M. Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics 2005, 4:2010-2021. 10.1074/mcp.T500030-MCP200, 16249172.
68. Mesuere B, Devreese B, Debyser G, Aerts M, Vandamme P, Dawyndt P. Unipept: tryptic peptide-based biodiversity analysis of metaproteome samples. J Proteome Res 2012, 11:5773-5780. 23153116.