A straightforward and efficient analytical pipeline for metaproteome characterization
Tóm tắt
The massive characterization of host-associated and environmental microbial communities has represented a real breakthrough in the life sciences in the last years. In this context, metaproteomics specifically enables the transition from assessing the genomic potential to actually measuring the functional expression of a microbiome. However, significant research efforts are still required to develop analysis pipelines optimized for metaproteome characterization. This work presents an efficient analytical pipeline for shotgun metaproteomic analysis, combining bead-beating/freeze-thawing for protein extraction, filter-aided sample preparation for cleanup and digestion, and single-run liquid chromatography-tandem mass spectrometry for peptide separation and identification. The overall procedure is more time-effective and less labor-intensive when compared to state-of-the-art metaproteomic techniques. The pipeline was first evaluated using mock microbial mixtures containing different types of bacteria and yeasts, enabling the identification of up to over 15,000 non-redundant peptide sequences per run with a linear dynamic range from 104 to 108 colony-forming units. The pipeline was then applied to the mouse fecal metaproteome, leading to the overall identification of over 13,000 non-redundant microbial peptides with a false discovery rate of <1%, belonging to over 600 different microbial species and 250 functionally relevant protein families. An extensive mapping of the main microbial metabolic pathways actively functioning in the gut microbiome was also achieved. The analytical pipeline presented here may be successfully used for the in-depth and time-effective characterization of complex microbial communities, such as the gut microbiome, and represents a useful tool for the microbiome research community.
Tài liệu tham khảo
citation_journal_title=Environ Microbiol; citation_title=The application of two-dimensional polyacrylamide gel electrophoresis and downstream analyses to a mixed community of prokaryotic microorganisms; citation_author=P Wilmes, PL Bond; citation_volume=6; citation_publication_date=2004; citation_pages=911-920; citation_doi=10.1111/j.1462-2920.2004.00687.x; citation_id=CR1
citation_journal_title=Nat Rev Microbiol; citation_title=Functional analysis of natural microbial consortia using community proteomics; citation_author=NC VerBerkmoes, VJ Denef, RL Hettich, JF Banfield; citation_volume=7; citation_publication_date=2009; citation_pages=196-205; citation_doi=10.1038/nrmicro2080; citation_id=CR2
citation_journal_title=Proteomics; citation_title=Environmental proteomics: analysis of structure and function of microbial communities; citation_author=T Schneider, K Riedel; citation_volume=10; citation_publication_date=2010; citation_pages=785-798; citation_doi=10.1002/pmic.200900450; citation_id=CR3
citation_journal_title=Curr Opin Microbiol; citation_title=Microbial metaproteomics: identifying the repertoire of proteins that microorganisms use to compete and cooperate in complex environmental communities; citation_author=RL Hettich, R Sharma, K Chourey, RJ Giannone; citation_volume=15; citation_publication_date=2012; citation_pages=373-380; citation_doi=10.1016/j.mib.2012.04.008; citation_id=CR4
citation_journal_title=J Proteomics; citation_title=Metaproteomics of our microbiome - developing insight in function and activity in man and model systems; citation_author=CA Kolmeder, WM de Vos; citation_volume=97; citation_publication_date=2014; citation_pages=3-16; citation_doi=10.1016/j.jprot.2013.05.018; citation_id=CR5
citation_journal_title=J Transl Med; citation_title=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; citation_author=DE Fouts, R Pieper, S Szpakowski, H Pohl, S Knoblach, MJ Suh, ST Huang, I Ljungberg, BM Sprague, SK Lucas, M Torralba, KE Nelson, SL Groah; citation_volume=10; citation_publication_date=2012; citation_pages=174; citation_doi=10.1186/1479-5876-10-174; citation_id=CR6
citation_journal_title=J Proteome Res; citation_title=Direct cellular lysis/protein extraction protocol for soil metaproteomics; citation_author=K Chourey, J Jansson, N VerBerkmoes, M Shah, KL Chavarria, LM Tom, EL Brodie, RL Hettich; citation_volume=9; citation_publication_date=2010; citation_pages=6615-6622; citation_doi=10.1021/pr100787q; citation_id=CR7
citation_journal_title=ISME J; citation_title=Shotgun metaproteomics of the human distal gut microbiota; citation_author=NC Verberkmoes, AL Russell, M Shah, A Godzik, M Rosenquist, J Halfvarson, MG Lefsrud, J Apajalahti, C Tysk, RL Hettich, JK Jansson; citation_volume=3; citation_publication_date=2009; citation_pages=179-189; citation_doi=10.1038/ismej.2008.108; citation_id=CR8
citation_journal_title=Saline Systems; citation_title=Metaproteomic analysis of Chesapeake Bay microbial communities; citation_author=J Kan, TE Hanson, JM Ginter, K Wang, F Chen; citation_volume=1; citation_publication_date=2005; citation_pages=7; citation_doi=10.1186/1746-1448-1-7; citation_id=CR9
citation_journal_title=Soil Biol Biochem; citation_title=Soil metaproteomics – comparative evaluation of protein extraction protocols; citation_author=KM Keiblinger, IC Wilhartitz, T Schneider, B Roschitzki, E Schmid, L Eberl, K Riedel, S Zechmeister-Boltenstern; citation_volume=54; citation_publication_date=2012; citation_pages=14-24; citation_doi=10.1016/j.soilbio.2012.05.014; citation_id=CR10
citation_journal_title=Anal Chem; citation_title=Method development for metaproteomic analyses of marine biofilms; citation_author=DH Leary, WJ Hervey, RW Li, JR Deschamps, AW Kusterbeck, GJ Vora; citation_volume=84; citation_publication_date=2012; citation_pages=4006-4013; citation_doi=10.1021/ac203315n; citation_id=CR11
citation_journal_title=ISME J; citation_title=Functional metaproteome analysis of protein extracts from contaminated soil and groundwater; citation_author=D Benndorf, GU Balcke, H Harms, M von Bergen; citation_volume=1; citation_publication_date=2007; citation_pages=224-234; citation_doi=10.1038/ismej.2007.39; citation_id=CR12
citation_journal_title=Appl Soil Ecol; citation_title=The potential of soil protein-based methods to indicate metal contamination; citation_author=I Singleton, G Merrington, S Colvan, JS Delahunty; citation_volume=23; citation_publication_date=2003; citation_pages=25-32; citation_doi=10.1016/S0929-1393(03)00004-0; citation_id=CR13
citation_journal_title=J Microbiol Methods; citation_title=Direct extraction of catalytic proteins from natural microbial communities; citation_author=OA Ogunseitan; citation_volume=28; citation_publication_date=1997; citation_pages=55-63; citation_doi=10.1016/S0167-7012(96)00962-1; citation_id=CR14
citation_journal_title=ISME J; citation_title=Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions; citation_author=T Schneider, KM Keiblinger, E Schmid, K Sterflinger-Gleixner, G Ellersdorfer, B Roschitzki, A Richter, L Eberl, S Zechmeister-Boltenstern, K Riedel; citation_volume=6; citation_publication_date=2012; citation_pages=1749-1762; citation_doi=10.1038/ismej.2012.11; citation_id=CR15
citation_journal_title=Appl Environ Microbiol; citation_title=Metaproteomics approach to study the functionality of the microbiota in the human infant gastrointestinal tract; citation_author=ES Klaassens, WM de Vos, EE Vaughan; citation_volume=73; citation_publication_date=2006; citation_pages=1388-1392; citation_doi=10.1128/AEM.01921-06; citation_id=CR16
citation_journal_title=PLoS One; citation_title=Comparative metaproteomics and diversity analysis of human intestinal microbiota testifies for its temporal stability and expression of core functions; citation_author=CA Kolmeder, M de Been, J Nikkilä, I Ritamo, J Mättö, L Valmu, J Salojärvi, A Palva, A Salonen, WM de Vos; citation_volume=7; citation_publication_date=2012; citation_pages=e29913; citation_doi=10.1371/journal.pone.0029913; citation_id=CR17
citation_journal_title=Electrophoresis; citation_title=Optimisation of protein extraction and 2-DE for metaproteomics of microbial communities from anaerobic wastewater treatment biofilms; citation_author=F Abram, E Gunnigle, V O’Flaherty; citation_volume=30; citation_publication_date=2009; citation_pages=4149-4151; citation_doi=10.1002/elps.200900474; citation_id=CR18
citation_journal_title=Appl Environ Microbiol; citation_title=Metaproteomics analysis reveals the adaptation process for the chicken gut microbiota; citation_author=Y Tang, A Underwood, A Gielbert, MJ Woodward, L Petrovska; citation_volume=80; citation_publication_date=2014; citation_pages=478-485; citation_doi=10.1128/AEM.02472-13; citation_id=CR19
citation_journal_title=J Proteome Res; citation_title=Coupling a detergent lysis/cleanup methodology with intact protein fractionation for enhanced proteome characterization; citation_author=R Sharma, BD Dill, K Chourey, M Shah, NC Verberkmoes, RL Hettich; citation_volume=11; citation_publication_date=2012; citation_pages=6008-6018; citation_id=CR20
citation_journal_title=Electrophoresis; citation_title=Comparison of protein precipitation methods for various rat brain structures prior to proteomic analysis; citation_author=E Fic, S Kedracka-Krok, U Jankowska, A Pirog, M Dziedzicka-Wasylewska; citation_volume=31; citation_publication_date=2010; citation_pages=3573-3579; citation_doi=10.1002/elps.201000197; citation_id=CR21
citation_journal_title=J Chromatogr A; citation_title=Comparison of protein precipitation methods for sample preparation prior to proteomic analysis; citation_author=L Jiang, L He, M Fountoulakis; citation_volume=1023; citation_publication_date=2004; citation_pages=317-320; citation_doi=10.1016/j.chroma.2003.10.029; citation_id=CR22
citation_journal_title=J Proteome Res; citation_title=Metaproteome analysis and molecular genetics of rat intestinal microbiota reveals section and localization resolved species distribution and enzymatic functionalities; citation_author=S-B Haange, A Oberbach, N Schlichting, F Hugenholtz, H Smidt, M von Bergen, H Till, J Seifert; citation_volume=11; citation_publication_date=2012; citation_pages=5406-5417; citation_doi=10.1021/pr3006364; citation_id=CR23
citation_journal_title=Environ Microbiol; citation_title=Microbiota from the distal guts of lean and obese adolescents exhibit partial functional redundancy besides clear differences in community structure; citation_author=M Ferrer, A Ruiz, F Lanza, SB Haange, A Oberbach, H Till, R Bargiela, C Campoy, MT Segura, M Richter, M von Bergen, J Seifert, A Suarez; citation_volume=15; citation_publication_date=2013; citation_pages=211-226; citation_doi=10.1111/j.1462-2920.2012.02845.x; citation_id=CR24
citation_journal_title=ISME J; citation_title=Protein-SIP enables time-resolved analysis of the carbon flux in a sulfate-reducing, benzene-degrading microbial consortium; citation_author=M Taubert, C Vogt, T Wubet, S Kleinsteuber, MT Tarkka, H Harms, F Buscot, H-H Richnow, M von Bergen, J Seifert; citation_volume=6; citation_publication_date=2012; citation_pages=2291-2301; citation_doi=10.1038/ismej.2012.68; citation_id=CR25
citation_journal_title=J Proteome Res; citation_title=Comparative study of workflows optimized for in-gel, in-solution, and on-filter proteolysis in the analysis of plasma membrane proteins; citation_author=W Choksawangkarn, N Edwards, Y Wang, P Gutierrez, C Fenselau; citation_volume=11; citation_publication_date=2012; citation_pages=3030-3034; citation_doi=10.1021/pr300188b; citation_id=CR26
citation_journal_title=Nat Methods; citation_title=Universal sample preparation method for proteome analysis; citation_author=JR Wiśniewski, A Zougman, N Nagaraj, M Mann; citation_volume=6; citation_publication_date=2009; citation_pages=359-362; citation_doi=10.1038/nmeth.1322; citation_id=CR27
citation_journal_title=Gut; citation_title=Gut microbiota disturbance during antibiotic therapy: a multi-omic approach; citation_author=AE Perez-Cobas, MJ Gosalbes, A Friedrichs, H Knecht, A Artacho, K Eismann, W Otto, D Rojo, R Bargiela, M von Bergen, SC Neulinger, C Däumer, FA Heinsen, A Latorre, C Barbas, J Seifert, VM dos Santos, SJ Ott, M Ferrer, A Moya; citation_volume=62; citation_publication_date=2013; citation_pages=1591-1601; citation_doi=10.1136/gutjnl-2012-303184; citation_id=CR28
citation_journal_title=Science; citation_title=Community proteomics of a natural microbial biofilm; citation_author=RJ Ram, NC Verberkmoes, MP Thelen, GW Tyson, BJ Baker, RC Blake, M Shah, RL Hettich, JF Banfield; citation_volume=308; citation_publication_date=2005; citation_pages=1915-1920; citation_doi=10.1126/science. 1109070; citation_id=CR29
citation_journal_title=Nat Protoc; citation_title=Analysis of protein mixtures from whole-cell extracts by single-run nanoLC-MS/MS using ultralong gradients; citation_author=T Köcher, P Pichler, R Swart, K Mechtler; citation_volume=7; citation_publication_date=2012; citation_pages=882-890; citation_doi=10.1038/nprot.2012.036; citation_id=CR30
citation_journal_title=Mol Cell Proteomics; citation_title=Deep and highly sensitive proteome coverage by LC-MS/MS without prefractionation; citation_author=SS Thakur, T Geiger, B Chatterjee, P Bandilla, F Frohlich, J Cox, M Mann; citation_volume=10; citation_publication_date=2011; citation_pages=M110.003699; citation_doi=10.1074/mcp.M110.003699; citation_id=CR31
citation_journal_title=Mol Cell Proteomics; citation_title=System-wide perturbation analysis with nearly complete coverage of the yeast proteome by single-shot ultra HPLC runs on a bench top Orbitrap; citation_author=N Nagaraj, NA Kulak, J Cox, N Neuhauser, K Mayr, O Hoerning, O Vorm, M Mann; citation_volume=11; citation_publication_date=2012; citation_pages=M111.013722; citation_doi=10.1074/mcp.M111.013722; citation_id=CR32
citation_journal_title=Mol Cell Proteomics; citation_title=Rapid and deep human proteome analysis by single-dimension shotgun proteomics; citation_author=M Pirmoradian, H Budamgunta, K Chingin, B Zhang, J Astorga-Wells, RA Zubarev; citation_volume=12; citation_publication_date=2013; citation_pages=3330-3338; citation_doi=10.1074/mcp.O113.028787; citation_id=CR33
citation_journal_title=Anal Chem; citation_title=Urine sample preparation in 96-well filter plates for quantitative clinical proteomics; citation_author=Y Yu, MJ Suh, P Sikorski, K Kwon, KE Nelson, R Pieper; citation_volume=86; citation_publication_date=2014; citation_pages=5470-5477; citation_doi=10.1021/ac5008317; citation_id=CR34
citation_journal_title=Proteomics; citation_title=Mycobacterial proteome extraction: comparison of disruption methods; citation_author=MD Lanigan, JA Vaughan, BJ Shiell, GJ Beddome, WP Michalski; citation_volume=4; citation_publication_date=2004; citation_pages=1094-1100; citation_doi=10.1002/pmic.200300672; citation_id=CR35
citation_journal_title=J Microbiol Methods; citation_title=Improved detection of microbial DNA after bead-beating before DNA isolation; citation_author=R de Boer, R Peters, S Gierveld, T Schuurman, M Kooistra-Smid, P Savelkoul; citation_volume=80; citation_publication_date=2010; citation_pages=209-211; citation_doi=10.1016/j.mimet.2009.11.009; citation_id=CR36
citation_journal_title=J Microbiol Methods; citation_title=Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: effective recovery of bacterial and archaeal DNA using mechanical cell lysis; citation_author=A Salonen, J Nikkila, J Jalanka-Tuovinen, O Immonen, M Rajilic-Stojanovic, RA Kekkonen, A Palva, WM de Vos; citation_volume=81; citation_publication_date=2010; citation_pages=127-134; citation_doi=10.1016/j.mimet.2010.02.007; citation_id=CR37
citation_journal_title=Yeast; citation_title=Rapid DNA, RNA and protein extraction protocols optimized for slow continuously growing yeast cultures; citation_author=K Sasidharan, C Amariei, M Tomita, DB Murray; citation_volume=29; citation_publication_date=2012; citation_pages=311-322; citation_doi=10.1002/yea.2911; citation_id=CR38
citation_journal_title=PLoS One; citation_title=Integrated metagenomics/metaproteomics reveals human host-microbiota signatures of Crohn’s disease; citation_author=AR Erickson, BL Cantarel, R Lamendella, Y Darzi, EF Mongodin, C Pan, M Shah, J Halfvarson, C Tysk, B Henrissat, J Raes, NC Verberkmoes, CM Fraser, RL Hettich, JK Jansson; citation_volume=7; citation_publication_date=2012; citation_pages=e49138; citation_doi=10.1371/journal.pone.0049138; citation_id=CR39
citation_journal_title=BMC Bioinformatics; citation_title=The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes; citation_author=F Meyer, D Paarmann, M D’Souza, R Olson, E Glass, M Kubal, T Paczian, A Rodriguez, R Stevens, A Wilke, J Wilkening, RA Edwards; citation_volume=9; citation_publication_date=2008; citation_pages=386; citation_doi=10.1186/1471-2105-9-386; citation_id=CR40
citation_journal_title=J Proteomics; citation_title=A metaproteomic pipeline to identify newborn mouse gut phylotypes; citation_author=F Del Chierico, A Petrucca, SL Mortera, P Vernocchi, MM Rosado, L Pieroni, R Carsetti, A Urbani, L Putignani; citation_volume=97; citation_publication_date=2014; citation_pages=17-26; citation_doi=10.1016/j.jprot.2013.10.025; citation_id=CR41
citation_journal_title=PLoS One; citation_title=Quantitatively different, yet qualitatively alike: a meta-analysis of the mouse core gut microbiome with a view towards the human gut microbiome; citation_author=L Krych, CH Hansen, AK Hansen, FW van den Berg, DS Nielsen; citation_volume=8; citation_publication_date=2013; citation_pages=e62578; citation_doi=10.1371/journal.pone.0062578; citation_id=CR42
citation_journal_title=Annu Rev Microbiol; citation_title=TonB-dependent transporters: regulation, structure, and function; citation_author=N Noinaj, M Guillier, TJ Barnard, SK Buchanan; citation_volume=64; citation_publication_date=2010; citation_pages=43-60; citation_doi=10.1146/annurev.micro.112408.134247; citation_id=CR43
citation_journal_title=Biochem Cell Biol; citation_title=TonB or not TonB: is that the question?; citation_author=KD Krewulak, HJ Vogel; citation_volume=89; citation_publication_date=2011; citation_pages=87-97; citation_doi=10.1139/O10-141; citation_id=CR44
citation_journal_title=Microbiol Mol Biol Rev; citation_title=Siderophore-based iron acquisition and pathogen control; citation_author=M Miethke, MA Marahiel; citation_volume=71; citation_publication_date=2007; citation_pages=413-451; citation_doi=10.1128/MMBR.00012-07; citation_id=CR45
citation_journal_title=Nature; citation_title=Structural basis for iron piracy by pathogenic Neisseria; citation_author=N Noinaj, NC Easley, M Oke, N Mizuno, J Gumbart, E Boura, AN Steere, O Zak, P Aisen, E Tajkhorshid, RW Evans, AR Gorringe, AB Mason, AC Steven, SK Buchanan; citation_volume=483; citation_publication_date=2012; citation_pages=53-58; citation_doi=10.1038/nature10823; citation_id=CR46
citation_journal_title=PLoS One; citation_title=The colitis-associated transcriptional profile of commensal Bacteroides thetaiotaomicronenhances adaptive immune responses to a bacterial antigen; citation_author=JJ Hansen, Y Huang, DA Peterson, L Goeser, TJ Fan, EB Chang, RB Sartor; citation_volume=7; citation_publication_date=2012; citation_pages=e42645; citation_doi=10.1371/journal.pone.0042645; citation_id=CR47
citation_journal_title=Nucleic Acids Res; citation_title=iPath2.0: interactive pathway explorer; citation_author=T Yamada, I Letunic, S Okuda, M Kanehisa, P Bork; citation_volume=39; citation_publication_date=2011; citation_pages=W412-W415; citation_doi=10.1093/nar/gkr313; citation_id=CR48
citation_journal_title=Ann N Y Acad Sci; citation_title=Old acetogens, new light; citation_author=HL Drake, AS Gossner, SL Daniel; citation_volume=1125; citation_publication_date=2008; citation_pages=100-128; citation_doi=10.1196/annals.1419.016; citation_id=CR49
citation_journal_title=J Biol Chem; citation_title=Dissecting the in vivometabolic potential of two human gut acetogens; citation_author=FE Rey, JJ Faith, J Bain, MJ Muehlbauer, RD Stevens, CB Newgard, JI Gordon; citation_volume=285; citation_publication_date=2010; citation_pages=22082-22090; citation_doi=10.1074/jbc.M110.117713; citation_id=CR50
citation_journal_title=Biochim Biophys Acta; citation_title=Acetogenesis and the Wood-Ljungdahl pathway of CO(2) fixation; citation_author=SW Ragsdale, E Pierce; citation_volume=1784; citation_publication_date=2008; citation_pages=1873-1898; citation_doi=10.1016/j.bbapap.2008.08.012; citation_id=CR51
citation_journal_title=Appl Environ Microbiol; citation_title=Molecular ecological analysis of the succession and diversity of sulfate-reducing bacteria in the mouse gastrointestinal tract; citation_author=B Deplancke, KR Hristova, HA Oakley, VJ McCracken, R Aminov, RI Mackie, HR Gaskins; citation_volume=66; citation_publication_date=2000; citation_pages=2166-2174; citation_doi=10.1128/AEM.66.5.2166-2174.2000; citation_id=CR52
citation_journal_title=Adv Appl Microbiol; citation_title=Biochemistry, physiology and biotechnology of sulfate-reducing bacteria; citation_author=LL Barton, GD Fauque; citation_volume=68; citation_publication_date=2009; citation_pages=41-98; citation_doi=10.1016/S0065-2164(09)01202-7; citation_id=CR53
citation_journal_title=Nat Rev Microbiol; citation_title=The ecology and biotechnology of sulphate-reducing bacteria; citation_author=G Muyzer, AJ Stams; citation_volume=6; citation_publication_date=2008; citation_pages=441-454; citation_id=CR54
citation_journal_title=Front Physiol; citation_title=Microbial pathways in colonic sulfur metabolism and links with health and disease; citation_author=F Carbonero, AC Benefiel, AH Alizadeh-Ghamsari, HR Gaskins; citation_volume=3; citation_publication_date=2012; citation_pages=448; citation_doi=10.3389/fphys.2012.00448; citation_id=CR55
citation_journal_title=Curr Microbiol; citation_title=Nutritional aspects of dissimilatory sulfate reduction in the human large intestine; citation_author=CL Willis, JH Cummings, G Neale, GR Gibson; citation_volume=35; citation_publication_date=1997; citation_pages=294-298; citation_doi=10.1007/s002849900257; citation_id=CR56
citation_journal_title=ISME J; citation_title=High-fat diet alters gut microbiota physiology in mice; citation_author=H Daniel, A Moghaddas Gholami, D Berry, C Desmarchelier, H Hahne, G Loh, S Mondot, P Lepage, M Rothballer, A Walker, C Böhm, M Wenning, M Wagner, M Blaut, P Schmitt-Kopplin, B Kuster, D Haller, T Clavel; citation_volume=8; citation_publication_date=2014; citation_pages=295-308; citation_doi=10.1038/ismej.2013.155; citation_id=CR57
citation_journal_title=PLoS Biol; citation_title=Effects of diet on resource utilization by a model human gut microbiota containing Bacteroides cellulosilyticusWH2, a symbiont with an extensive glycobiome; citation_author=NP McNulty, M Wu, AR Erickson, C Pan, BK Erickson, EC Martens, NA Pudlo, BD Muegge, B Henrissat, RL Hettich, JI Gordon; citation_volume=11; citation_publication_date=2013; citation_pages=e1001637; citation_doi=10.1371/journal.pbio.1001637; citation_id=CR58
citation_journal_title=Proteomics; citation_title=Bioinformatic progress and applications in metaproteogenomics for bridging the gap between genomic sequences and metabolic functions in microbial communities; citation_author=J Seifert, FA Herbst, P Halkjaer Nielsen, FJ Planes, N Jehmlich, M Ferrer, M von Bergen; citation_volume=13; citation_publication_date=2013; citation_pages=2786-2804; citation_id=CR59
citation_journal_title=PLoS One; citation_title=Evaluating the impact of different sequence databases on metaproteome analysis: insights from a lab-assembled microbial mixture; citation_author=A Tanca, A Palomba, M Deligios, T Cubeddu, C Fraumene, G Biosa, D Pagnozzi, MF Addis, S Uzzau; citation_volume=8; citation_publication_date=2013; citation_pages=e82981; citation_doi=10.1371/journal.pone.0082981; citation_id=CR60
citation_journal_title=PLoS One; citation_title=Strategies for metagenomic-guided whole-community proteomics of complex microbial environments; citation_author=BL Cantarel, AR Erickson, NC VerBerkmoes, BK Erickson, PA Carey, C Pan, M Shah, EF Mongodin, JK Jansson, CM Fraser-Liggett, RL Hettich; citation_volume=6; citation_publication_date=2011; citation_pages=e27173; citation_doi=10.1371/journal.pone.0027173; citation_id=CR61
citation_journal_title=Appl Environ Microbiol; citation_title=Abundant and diverse fungal microbiota in the murine intestine; citation_author=AJ Scupham, LL Presley, B Wei, E Bent, N Griffith, M McPherson, F Zhu, O Oluwadara, N Rao, J Braun, J Borneman; citation_volume=72; citation_publication_date=2006; citation_pages=793-801; citation_doi=10.1128/AEM.72.1.793-801.2006; citation_id=CR62
citation_journal_title=PLoS One; citation_title=Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents; citation_author=C Hoffmann, S Dollive, S Grunberg, J Chen, H Li, GD Wu, JD Lewis, FD Bushman; citation_volume=8; citation_publication_date=2013; citation_pages=e66019; citation_doi=10.1371/journal.pone.0066019; citation_id=CR63
citation_journal_title=Appl Environ Microbiol; citation_title=Effective recovery of bacterial DNA and percent-guanine-plus-cytosine-based analysis of community structure in the gastrointestinal tract of broiler chickens; citation_author=JH Apajalahti, LK Sarkilahti, BR Maki, JP Heikkinen, PH Nurminen, WE Holben; citation_volume=64; citation_publication_date=1998; citation_pages=4084-4088; citation_id=CR64
citation_journal_title=BMC Bioinformatics; citation_title=The M5nr: a novel non-redundant database containing protein sequences and annotations from multiple sources and associated tools; citation_author=A Wilke, T Harrison, J Wilkening, D Field, EM Glass, N Kyrpides, K Mavrommatis, F Meyer; citation_volume=13; citation_publication_date=2012; citation_pages=141; citation_doi=10.1186/1471-2105-13-141; citation_id=CR65
citation_journal_title=Proteomics; citation_title=Comparison of detergent-based sample preparation workflows for LTQ-Orbitrap analysis of the Escherichia coliproteome; citation_author=A Tanca, G Biosa, D Pagnozzi, MF Addis, S Uzzau; citation_volume=13; citation_publication_date=2013; citation_pages=2597-2607; citation_doi=10.1002/pmic.201200478; citation_id=CR66
citation_journal_title=Mol Cell Proteomics; citation_title=Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap; citation_author=JV Olsen, LM de Godoy, G Li, B Macek, P Mortensen, R Pesch, A Makarov, O Lange, S Horning, M Mann; citation_volume=4; citation_publication_date=2005; citation_pages=2010-2021; citation_doi=10.1074/mcp.T500030-MCP200; citation_id=CR67
citation_journal_title=J Proteome Res; citation_title=Unipept: tryptic peptide-based biodiversity analysis of metaproteome samples; citation_author=B Mesuere, B Devreese, G Debyser, M Aerts, P Vandamme, P Dawyndt; citation_volume=11; citation_publication_date=2012; citation_pages=5773-5780; citation_id=CR68