[en] Soil represents a complex and dynamic ecosystem, hosting a myriad of microorganisms that coexist and play vital roles in nutrient cycling and organic matter transformation. Among these microorganisms, bacteria and fungi are key members of the microbial community, profoundly influencing the fate of nitrogen, sulfur, and carbon in terrestrial environments. Understanding the intricacies of soil ecosystems and the biological processes orchestrated by microbial communities necessitates a deep dive into their composition and metabolic activities. The advent of next-generation sequencing and ‘omics’ techniques, such as metagenomics and metaproteomics, has revolutionized our understanding of microbial ecology and the functional dynamics of soil microbial communities. Metagenomics enables the identification of microbial community composition in soil, while metaproteomics sheds light on the current biological functions performed by these communities. However, metaproteomics presents several challenges, both technical and computational. Factors such as the presence of humic acids and variations in extraction methods can influence protein yield, while the absence of high-resolution mass spectrometry and comprehensive protein databases limits the depth of protein identification. Notwithstanding these limitations, metaproteomics remains a potent tool for unraveling the intricate biological processes and functions of soil microbial communities. In this review, we delve into the methodologies and challenges of metaproteomics in soil research, covering aspects such as protein extraction, identification, and bioinformatics analysis. Furthermore, we explore the applications of metaproteomics in soil bioremediation, highlighting its potential in addressing environmental challenges.
Pan, Haixia ; Université de Mons - UMONS > Faculté des Sciences > Service de Protéomie et Microbiologie ; Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education), School of Chemical Engineering, Ocean and Life Sciences, Dalian University of Technology (Panjin Campus), Panjin, China
Wattiez, Ruddy ; Université de Mons - UMONS > Faculté des Sciences > Service de Protéomie et Microbiologie
Gillan, David ; Université de Mons - UMONS > Faculté des Sciences > Service de Protéomie et Microbiologie
Language :
English
Title :
Soil Metaproteomics for Microbial Community Profiling: Methodologies and Challenges
Joint Funds of the Natural Science Foundation of Liaoning Province of China
Funding text :
The authors are highly grateful to the authorities of the respective departments for support in doing this work, Proteomics and Microbiology Laboratory, University of Mons, Dalian University of Technology and the financial support from China Scholarship Council (201706060216) and the Joint Funds of the Natural Science Foundation of Liaoning Province of China (No.2023-BSBA-024).Funding was provided by Joint Funds of the Natural Science Foundation of Liaoning Province of China (Grant No. 2023-BSBA-024).
T.V. Abiraami S. Singh L. Nain Soil metaproteomics as a tool for monitoring functional microbial communities: promises and challenges Rev Environ Sci Bio/Technol 2020 19 1 73 102 1:CAS:528:DC%2BC1MXisVSntrbE 10.1007/s11157-019-09519-8
S. Mocali A. Benedetti Exploring research frontiers in microbiology: the challenge of metagenomics in soil microbiology Res Microbiol 2010 161 6 497 505 10.1016/j.resmic.2010.04.010 20452420
F. Bastida N. Jehmlich K. Lima B.E.L. Morris H.H. Richnow T. Hernández M. Bergen C. García The ecological and physiological responses of the microbial community from a semiarid soil to hydrocarbon contamination and its bioremediation using compost amendment J Proteomics 2016 135 162 169 1:CAS:528:DC%2BC2MXht1OqtbzK 10.1016/j.jprot.2015.07.023 26225916
F. Bastida J.L. Moreno C. Nicolas T. Hernandez C. Garcia Soil metaproteomics: a review of an emerging environmental science: significance, methodology and perspectives Eur J Soil Sci 2009 60 6 845 859 1:CAS:528:DC%2BD1MXhs1Sju77J 10.1111/j.1365-2389.2009.01184.x
F. Salvato R.L. Hettich M. Kleiner Five key aspects of metaproteomics as a tool to understand functional interactions in host associated microbiomes PLoS Pathog 2021 10.1371/journal.ppat.1009245 33630960 7906368
M.C. Lau R.L. Harris Y. Oh M.J. Yi A. Behmard T.C. Onstott Taxonomic and functional compositions impacted by the quality of metatranscriptomic assemblies Front Microbiol 2018 9 1235 10.3389/fmicb.2018.01235 29973918 6019464
D. Becher J. Bernhardt S. Fuchs K. Riedel Metaproteomics to unravel major microbial players in leaf litter and soil environments: challenges and perspectives Proteomics 2013 13 18–19 2895 2909 1:CAS:528:DC%2BC3sXhsFOgtLnN 10.1002/pmic.201300095 23894095
D.C. Gillan S. Roosa B. Kunath G. Billon R. Wattiez The long-term adaptation of bacterial communities in metal-contaminated sediments: a metaproteogenomic study Environ Microbiol 2015 17 6 1991 2005 1:CAS:528:DC%2BC2MXhtVWgs7zK 10.1111/1462-2920.12627 25244307
H. Schiebenhoefer K. Schallert B.Y. Renard K. Trappe E. Schmid D. Benndorf K. Riedel T. Muth S. Fuchs A complete and flexible workflow for metaproteomics data analysis based on MetaProteomeAnalyzer and Prophane Nat Protoc 2020 15 10 3212 3239 1:CAS:528:DC%2BB3cXhvFegu7%2FF 10.1038/s41596-020-0368-7 32859984
M. Mattarozzi M. Manfredi B. Montanini F. Gosetti A.M. Sanangelantoni E. Marengo M. Careci G. Visioli A metaproteomic approach dissecting major bacterial functions in the rhizosphere of plants living in serpentine soil Anal Bioanal Chem 2017 409 2327 2339 1:CAS:528:DC%2BC2sXpslGisw%3D%3D 10.1007/s00216-016-0175-8 28083663
D.C. Gillan H. Pan A. Roulez R. Wattiez The metaphenome of a calaminiferous soil Microbe 2023 1 10.1016/j.microb.2023.100002
R. Starke N. Jehmlich F. Bastida Using proteins to study how microbes contribute to soil ecosystem services: the current state and future perspectives of soil metaproteomics J Proteomics 2019 198 50 58 1:CAS:528:DC%2BC1cXit1ehtrbP 10.1016/j.jprot.2018.11.011 30445181
M. Tartaglia F. Bastida R. Sciarrillo C. Guarino Soil metaproteomics for the study of the relationships between microorganisms and plants: a review of extraction protocols and ecological insights Int J Mol Sci 2020 21 22 8455 1:CAS:528:DC%2BB3cXisFygsr7P 10.3390/ijms21228455 33187080 7697097
E.B. Taylor M.A. Williams Microbial protein in soil: influence of extraction method and C amendment on extraction and recovery Microb Ecol 2010 59 390 399 1:CAS:528:DC%2BC3cXjtFWlsbc%3D 10.1007/s00248-009-9593-x 19844650
O.A. Ogunseitan Direct extraction of proteins from environmental samples J Microbiol Methods 1993 17 4 273 281 1:CAS:528:DyaK3sXltlCrt7s%3D 10.1016/0167-7012(93)90056-N
D. Benndorf G.U. Balcke H. Harms M. Von Bergen Functional metaproteome analysis of protein extracts from contaminated soil and groundwater ISME J 2007 1 3 224 234 1:CAS:528:DC%2BD2sXht1KhtL%2FM 10.1038/ismej.2007.39 18043633
S. Chen M.C. Rillig W. Wang Improving soil protein extraction for metaproteome analysis and glomalin-related soil protein detection Proteomics 2009 9 21 4970 4973 1:CAS:528:DC%2BD1MXhtleqtbnF 10.1002/pmic.200900251 19743425
K.M. Keiblinger I.C. Wilhartitz T. Schneider B. Roschitzki E. Schmid L. Eberl K. Riedel S. Zechmeister-Boltenstern Soil metaproteomics-comparative evaluation of protein extraction protocols Soil Biol Biochem 2012 54 14 24 1:CAS:528:DC%2BC38XhtVSlsLfE 10.1016/j.soilbio.2012.05.014 23125465 3413887
C. Qian R.L. Hettich Optimized extraction method to remove humic acid interferences from soil samples prior to microbial proteome measurements J Proteome Res 2017 16 7 2537 2546 1:CAS:528:DC%2BC2sXotlSrsbs%3D 10.1021/acs.jproteome.7b00103 28537741
A. Murase M. Yoneda R. Ueno K. Yonebayashi Isolation of extracellular protein from greenhouse soil Soil Biol Biochem 2003 35 5 733 736 1:CAS:528:DC%2BD3sXjt1GqsLc%3D 10.1016/S0038-0717(03)00087-7
I. Singleton G. Merrington S. Colvan J.S. Delahunty The potential of soil protein-based methods to indicate metal contamination Appl Soil Ecol 2003 23 1 25 32 10.1016/S0929-1393(03)00004-0
L.M. Greenfield P.W. Hill E. Paterson et al. Methodological bias associated with soluble protein recovery from soil Sci Rep 2018 8 11186 1:CAS:528:DC%2BC1MXovV2l 10.1038/s41598-018-29559-4 30046143 6060134
A.M. Herruzo-Ruiz C.A. Fuentes-Almagro J.M. Jiménez-Pastor V.M. Pérez-Rosa J. Blasco C. Michán J. Alhama Meta-omic evaluation of bacterial microbial community structure and activity for the environmental assessment of soils: overcoming protein extraction pitfalls Environ Microbiol 2021 23 8 4706 4725 1:CAS:528:DC%2BB3MXitVeqtLvI 10.1111/1462-2920.15673 34258847
C.E. Thorn C. Bergesch A. Joyce G. Sambrano K. McDonnell F. Brennan R. Heyer D. Benndorf F. Abram A robust, cost-effective method for DNA, RNA and protein co-extraction from soil, other complex microbiomes and pure cultures Mol Ecol Resources 2019 19 2 439 455 1:CAS:528:DC%2BC1MXjslKrtLw%3D 10.1111/1755-0998.12979
H.B. Wang Z.X. Zhang H. Li H.B. He C.X. Fang A.J. Zhang Q.S. Li R.S. Chen X.K. Guo H.F. Lin L.K. Wu S. Lin T. Chen R.Y. Lin X.X. Peng W.X. Lin Characterization of metaproteomics in crop rhizospheric soil J Proteome Res 2011 10 3 932 940 1:CAS:528:DC%2BC3MXmslCnsw%3D%3D 10.1021/pr100981r 21142081
H.B. Wang C.L. Zhu Y.H. Wang Q.X. Zhang P. Wang D. Li X.L. Jia J.H. Ye H.B. He Protein extraction and database construction in tea rhizosphere soil Acta Physiol Plant 2020 42 1 9 1:CAS:528:DC%2BB3cXitVGqtrbP 10.1007/s11738-020-03146-5
K. Chourey J. Jansson N. VerBerkmoes M. Shah K.L. Chavarria L.M. Tom E.L. Brodie R.L. Hettich Direct cellular lysis/protein extraction protocol for soil metaproteomics J Proteome Res 2010 9 12 6615 6622 1:CAS:528:DC%2BC3cXhsVaju7bE 10.1021/pr100787q 20954746
F. Bastida T. Hernández C. García Metaproteomics of soils from semiarid environment: functional and phylogenetic information obtained with different protein extraction methods J Proteomics 2014 101 31 42 1:CAS:528:DC%2BC2cXks1ajsrk%3D 10.1016/j.jprot.2014.02.006 24530626
F. Bastida N. Selevsek I.F. Torres T. Hernández C. García Soil restoration with organic amendments: linking cellular functionality and ecosystem processes Sci Rep 2015 5 1 15550 1:CAS:528:DC%2BC2MXhslens73K 10.1038/srep15550 26503516 4621494
B.W. Pirok D.R. Stoll P.J. Schoenmakers Recent developments in two-dimensional liquid chromatography: fundamental improvements for practical applications Anal Chem 2018 91 1 240 263 1:CAS:528:DC%2BC1cXitVKiu7%2FJ 10.1021/acs.analchem.8b04841 30380827 6322149
S. Qiu W.Z. Yang X.J. Shi C.L. Yao M. Yang X. Liu B.H. Jiang W.Y. Wu D.A. Guo A green protocol for efficient discovery of novel natural compounds: characterization of new ginsenosides from the stems and leaves of Panax ginseng as a case study Anal Chim Acta 2015 893 65 76 1:CAS:528:DC%2BC2MXhsVOnurrI 10.1016/j.aca.2015.08.048 26398424
P. Scherp G. Ku L. Coleman I. Kheterpal J. Gimble B. Bunnell Gel-based and gel-free proteomic technologies Adipose-derived stem cells. Methods in molecular biology 2011 Totowa Humana Press 10.1007/978-1-61737-960-4_13
D.N. Perkins D.J. Pappin D.M. Creasy J.S. Cottrell Probability-based protein identification by searching sequence databases using mass spectrometry data Electrophor Int J 1999 20 18 3551 3567 1:CAS:528:DC%2BD3cXhtF2ntw%3D%3D 10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2 10.1002/(SICI)1522-2683(19991201)20:183.0.CO;2-2
P. James Proteome research: mass spectrometry 2000 Berlin Springer 10.1007/978-3-642-56895-4_7
R. Craig R.C. Beavis TANDEM: matching proteins with tandem mass spectra Bioinformatics 2004 20 9 1466 1467 1:CAS:528:DC%2BD2cXkvVSrtLs%3D 10.1093/bioinformatics/bth092 14976030
L.Y. Geer S.P. Markey J.A. Kowalak L. Wagner M. Xu D.M. Maynard X.Y. Yang W.Y. Shi S.H. Bryant Open mass spectrometry search algorithm J Proteome Res 2004 3 5 958 964 1:CAS:528:DC%2BD2cXltl2lur8%3D 10.1021/pr0499491 15473683
Y.E. Chen X. Ge K. Woyshner M. McDermott A. Manousopoulou S.B. Ficarro J.A. Marto K.X. Li L.D. Wang J.J. Li APIR: aggregating universal proteomics database search algorithms for peptide identification with FDR control bioRxiv 2021 10.1101/2021.09.08.459494 34981065 8168384
M. Vaudel J.M. Burkhart R.P. Zahedi E. Oveland F.S. Berven A. Sickmann L. Martens H. Barsnes PeptideShaker enables reanalysis of MS-derived proteomics data sets Nat Biotechnol 2015 33 1 22 24 1:CAS:528:DC%2BC2MXmtVyhsg%3D%3D 10.1038/nbt.3109 25574629
M. Vaudel H. Barsnes F.S. Berven A. Sickmann L. Martens SearchGUI: an open-source graphical user interface for simultaneous OMSSA and X!Tandem searches Proteomics 2011 11 5 996 999 1:CAS:528:DC%2BC3MXitFGku74%3D 10.1002/pmic.201000595 21337703
D. Shteynberg E.W. Deutsch H. Lam J.K. Eng Z. Sun N. Tasman L. Mendoza R.L. Moritz R. Aebersold A.I. Nesvizhskii iProphet: multi-level integrative analysis of shotgun proteomic data improves peptide and protein identification rates and error estimates Mol Cell Proteom 2011 10.1074/mcp.M111.007690
T. Kwon H. Choi C. Vogel A.I. Nesvizhskii E.M. Marcotte MSblender: a probabilistic approach for integrating peptide identifications from multiple database search engines J Proteome Res 2011 10 7 2949 2958 1:CAS:528:DC%2BC3MXlsVWjsL8%3D 10.1021/pr2002116 21488652 3128686
R.L. Tatusov M.Y. Galperin D.A. Natale E.V. Koonin The COG database: a tool for genome-scale analysis of protein functions and evolution Nucleic Acids Res 2000 28 1 33 36 1:CAS:528:DC%2BD3cXhvVGqu7w%3D 10.1093/nar/28.1.33 10592175 102395
Gene Ontology Consortium The gene ontology resource: 20 years and still going strong Nucleic Acids Res 2019 47 D1 D330 D338 1:CAS:528:DC%2BC1MXhs1GqtrvP 10.1093/nar/gky1055
J. Huerta-Cepas D. Szklarczyk K. Forslund H. Cook D. Heller M.C. Walter T. Rattei D.R. Mende S. Sunagawa M. Kuhn L.J. Jensen C. Mering P. Bork eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences Nucleic Acids Res 2016 44 D1 D286 D293 1:CAS:528:DC%2BC2sXhtV2ns77L 10.1093/nar/gkv1248 26582926
T. Muth A. Behne R. Heyer F. Kohrs D. Benndorf M. Hoffmann M. Lehtevä U. Reichl L. Martens E. Rapp The MetaProteomeAnalyzer: a powerful open-source software suite for metaproteomics data analysis and interpretation J Proteome Res 2015 14 3 1557 1565 1:CAS:528:DC%2BC2MXit12kt7c%3D 10.1021/pr501246w 25660940
T. Schneider E. Schmid J.V. de Castro Jr M. Cardinale L. Eberl M. Grube G. Berg K. Riedel Structure and function of the symbiosis partners of the lung lichen (Lobaria pulmonaria L. Hoffm) analyzed by metaproteomics Proteomics 2011 11 13 2752 2756 1:CAS:528:DC%2BC3MXnvF2qur8%3D 10.1002/pmic.201000679 21604374
C. Blank C. Easterly B. Gruening J. Johnson C.A. Kolmeder P. Kumar D. May S. Mehta B. Mesuere Z. Brown J.E. Elias W.J. Hervey T. McGowan T. Muth B.L. Nunn J. Rudney A. Tanca T.J. Griffin P.D. Jagtap Disseminating metaproteomic informatics capabilities and knowledge using the Galaxy-P framework Proteomes 2018 6 1 7 1:CAS:528:DC%2BC1MXnt1Kgt7k%3D 10.3390/proteomes6010007 29385081 5874766
M. Porcheddu M. Abbondio L. De Diego S. Uzzau A. Tanca Meta4P: a user-friendly tool to parse label-free quantitative metaproteomic data and taxonomic/functional annotations J Proteome Res 2023 22 6 2109 2113 1:CAS:528:DC%2BB3sXoslentrs%3D 10.1021/acs.jproteome.2c00803 37116187 10243107
Q. Wu Z. Ning A. Zhang X. Zhang Z. Sun D. Figeys MetaX: a peptide centric metaproteomic data analysis platform using operational taxa-functions (OTF) bioRxiv 2024 10.1101/2024.04.19.590315 38948855 11213234
F. Bastida C. Nicolás J.L. Moreno T. Hernández C. Garcia Tracing changes in the microbial community of a hydrocarbon-polluted soil by culture-dependent proteomics Pedosphere 2010 20 4 479 485 1:CAS:528:DC%2BC3cXhtVGlsb3L 10.1016/S1002-0160(10)60037-9
U. Lechner D. Türkowsky T.T.H. Dinh H. Al-Fathi S. Schwoch S. Franke M.S. Gerlach M. Koch M. Bergen N. Jehmlich T.C.H. Dang Desulfitobacterium contributes to the microbial transformation of 2, 4, 5-T by methanogenic enrichment cultures from a Vietnamese active landfill Microb Biotechnol 2018 11 6 1137 1156 1:CAS:528:DC%2BC1cXhvF2mt7zL 10.1111/1751-7915.13301 30117290 6196390
K. Viacava J. Qiao A. Janowczyk S. Poudel N. Jacquemin K.L. Meibom H.K. Shrestha M.C. Reid R.L. Hettich R. Bernier-Latmani Meta-omics-aided isolation of an elusive anaerobic arsenic-methylating soil bacterium ISME J 2022 16 7 1740 1749 1:CAS:528:DC%2BB38XhsVOntLnK 10.1038/s41396-022-01220-z 35338334 9213503
B. Mesuere B. Devreese G. Debyser M. Aerts P. Vandamme P. Dawyndt Unipept: tryptic peptide-based biodiversity analysis of metaproteome samples J Proteome Res 2012 11 12 5773 5780 1:CAS:528:DC%2BC38Xhs1Ogu7fE 10.1021/pr300576s 23153116
B. Buchfink C. Xie D.H. Huson Fast and sensitive protein alignment using DIAMOND Nat Methods 2015 12 1 59 60 1:CAS:528:DC%2BC2cXhvFKlsrzN 10.1038/nmeth.3176 25402007
D.H. Huson A.F. Auch J. Qi S.C. Schuster MEGAN analysis of metagenomic data Genome Res 2007 17 3 377 386 1:CAS:528:DC%2BD2sXis12hsr8%3D 10.1101/gr.5969107 17255551 1800929
J. Werner A. Géron J. Kerssemakers S. Matallana-Surget mPies: a novel metaproteomics tool for the creation of relevant protein databases and automatized protein annotation Biol Direct 2019 14 1 5 1:CAS:528:DC%2BC1MXitFGqtLfF 10.1186/s13062-019-0253-x
M. Riffle D.H. May E. Timmins-Schiffman M.P. Mikan D. Jaschob W.S. Noble B.L. Nunn MetaGOmics: a web-based tool for peptide-centric functional and taxonomic analysis of metaproteomics data Proteomes 2017 6 1 2 1:CAS:528:DC%2BC1MXms12lur4%3D 10.3390/proteomes6010002 29280960 5874761