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Cited by 39Microbial Community Ecology and PhysiologyEvolution and Genetic DynamicsGenomics and Phylogenetic Studies

Community diversity and habitat structure shape the repertoire of extracellular proteins in bacteria

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Garcia-Garcera, Marc, Rocha, Eduardo P. C.·2020·Nature Communications
DOI 10.1038/s41467-020-14572-xPMC PMC7005277
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Abstract

We test the hypothesis that the frequency and cost of extracellular proteins produced by bacteria, which often depend on cooperative processes, vary with habitat structure and community diversity. The integration of the environmental distribution of bacteria (using 16S datasets) and their genomes shows that bacteria living in more structured habitats encode more extracellular proteins. In contrast, the effect of community diversity depends on protein function: it’s positive for proteins implicated in antagonistic interactions and negative for those involved in nutrient acquisition. Extracellular proteins are costly and endure stronger selective pressure for low cost and for low diffusivity in less structured habitats and in more diverse communities. Finally, Bacteria found in multiple types of habitats, including host-associated generalists, encode more extracellular proteins than niche-restricted bacteria. These results show that ecological variables, notably habitat structure and community diversity, shape the evolution of the repertoires of genes encoding extracellular proteins and thus affect the ability of bacteria to manipulate their environment.

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  • Comparative genomic analyses usually test for correlations between traits.

    “Comparative genomic analyses usually test for correlations between traits.”

    From A phylogenetic approach to comparative genomics (2025) · cites this paper as [82]

    The Methods (Statistical analyses; page not provided) describe correlation tests, and the Results (High habitat structure favors extracellular proteins; page not provided) report a correlation between protein-gene frequency and habitat structure. This supports the paper as an example of a genomic analysis testing an association, but it does not establish that comparative genomic analyses usually do so. (LLM, conf=0.82)

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  1. [1]Dalbey RE Kuhn A Protein traffic in Gram-negative bacteria–how exported and secreted proteins find their way FEMS Microbiol. Rev. 2012 36 1023 1045 10.1111/j.1574-6976.2012.00327.x 22250915 · DOI
  2. [2]Lee VT Schneewind O Protein secretion and the pathogenesis of bacterial infections Genes Dev. 2001 15 1725 1752 10.1101/gad.896801 11459823 · DOI
  3. [3]Ma W Guttman DS Evolution of prokaryotic and eukaryotic virulence effectors Curr. Opin. Plant Biol. 2008 11 412 419 10.1016/j.pbi.2008.05.001 18585954 · DOI
  4. [4]Hicks SW Galán JE Exploitation of eukaryotic subcellular targeting mechanisms by bacterial effectors Nat. Rev. Microbiol. 2013 11 316 326 10.1038/nrmicro3009 23588250 PMC3859125 · DOI
  5. [5]Bassler BL Losick R Bacterially speaking Cell 2006 125 237 246 10.1016/j.cell.2006.04.001 16630813 · DOI
  6. [6]Freudl R Leaving home ain’t easy: protein export systems in Gram-positive bacteria Res. Microbiol. 2013 164 664 674 10.1016/j.resmic.2013.03.014 23541477 · DOI
  7. [7]Costa TRD Secretion systems in Gram-negative bacteria: structural and mechanistic insights Nat. Rev. Microbiol. 2015 13 343 359 10.1038/nrmicro3456 25978706 · DOI · Paper page
  8. [8]Allison SD Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments Ecol. Lett. 2005 8 626 635 10.1111/j.1461-0248.2005.00756.x · DOI
  9. [9]Özkaya Ö Balbontín R Gordo I Xavier KB Cheating on cheaters stabilizes cooperation in Pseudomonas aeruginosa Curr. Biol. 2018 28 2070 2080 10.1016/j.cub.2018.04.093 30008329 · DOI
  10. [10]Jousset A Ecological and evolutive implications of bacterial defences against predators Environ. Microbiol. 2012 14 1830 1843 10.1111/j.1462-2920.2011.02627.x 22040156 · DOI
  11. [11]Bonhoeffer S Nowak MA Intra-host versus inter-host selection: viral strategies of immune function impairment Proc. Natl Acad. Sci. USA 1994 91 8062 8066 10.1073/pnas.91.17.8062 8058757 PMC44545 · DOI
  12. [12]Smith J The social evolution of bacterial pathogenesis Proc. Biol. Sci. 2001 268 61 69 10.1098/rspb.2000.1330 12123299 PMC1087601 · DOI
  13. [13]Nogueira T Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence Curr. Biol. 2009 19 1683 1691 10.1016/j.cub.2009.08.056 19800234 PMC2773837 · DOI
  14. [14]West SA Griffin AS Gardner A Diggle SP Social evolution theory for microorganisms Nat. Rev. Microbiol. 2006 4 597 607 10.1038/nrmicro1461 16845430 · DOI
  15. [15]Rankin DJ Bargum K Kokko H The tragedy of the commons in evolutionary biology Trends Ecol. Evol. 2007 22 643 651 10.1016/j.tree.2007.07.009 17981363 · DOI
  16. [16]Nogueira T Touchon M Rocha EPC Rapid evolution of the sequences and gene repertoires of secreted proteins in bacteria PLoS ONE 2012 7 e49403 10.1371/journal.pone.0049403 23189144 PMC3506625 · DOI
  17. [17]Rankin DJ Rocha EPC Brown SP What traits are carried on mobile genetic elements, and why? Heredity 2011 106 1 10 10.1038/hdy.2010.24 20332804 PMC3183850 · DOI
  18. [18]Mc Ginty SÉ Rankin DJ Brown SP Horizontal gene transfer and the evolution of bacterial cooperation Evolution 2011 65 21 32 10.1111/j.1558-5646.2010.01121.x 20825481 PMC3038327 · DOI
  19. [19]Dimitriu T Genetic information transfer promotes cooperation in bacteria Proc. Natl Acad. Sci. USA 2014 111 11103 11108 10.1073/pnas.1406840111 25024219 PMC4121819 · DOI
  20. [20]Lopez Pascua L Higher resources decrease fluctuating selection during host-parasite coevolution Ecol. Lett. 2014 17 1380 1388 10.1111/ele.12337 25167763 PMC4257576 · DOI
  21. [21]Hiltunen T Ayan GB Becks L Environmental fluctuations restrict eco-evolutionary dynamics in predator-prey system Proc. Biol. Sci. 2015 282 20150013 20150013 10.1098/rspb.2015.0013 25994670 PMC4455795 · DOI
  22. [22]Gonzalez D Sabnis A Foster KR Mavridou DAI Costs and benefits of provocation in bacterial warfare PNAS 2018 115 7593 7598 10.1073/pnas.1801028115 29967163 PMC6055196 · DOI
  23. [23]Bourke AFG Hamilton’s rule and the causes of social evolution Philos. Trans. R. Soc. B 2014 369 20130362 20130362 10.1098/rstb.2013.0362 PMC3982664 24686934 · DOI
  24. [24]Wakano JY Nowak MA Hauert C Spatial dynamics of ecological public goods PNAS 2009 106 7910 7914 10.1073/pnas.0812644106 19416839 PMC2683138 · DOI
  25. [27]Morris, J. J., Lenski, R. E. & Zinser, E. R. The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. MBio 3, e00036–12 (2012). PMC3315703 22448042
  26. [28]Butaitė E Baumgartner M Wyder S Kümmerli R Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities Nat. Commun. 2017 8 414 10.1038/s41467-017-00509-4 28871205 PMC5583256 · DOI
  27. [29]Yu NY PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes Bioinformatics 2010 26 1608 1615 10.1093/bioinformatics/btq249 20472543 PMC2887053 · DOI
  28. [30]Kümmerli R Schiessl KT Waldvogel T McNeill K Ackermann M Habitat structure and the evolution of diffusible siderophores in bacteria Ecol. Lett. 2014 17 1536 1544 10.1111/ele.12371 25250530 · DOI
  29. [32]Allocati N Masulli M Di Ilio C De Laurenzi V Die for the community: an overview of programmed cell death in bacteria Cell Death Dis. 2015 6 e1609 e1609 10.1038/cddis.2014.570 25611384 PMC4669768 · DOI
  30. [33]Foerstner KU Mering von C Hooper SD Bork P Environments shape the nucleotide composition of genomes EMBO Rep. 2005 6 1208 1213 10.1038/sj.embor.7400538 16200051 PMC1369203 · DOI
  31. [34]Seligmann H Cost-minimization of amino acid usage J. Mol. Evol. 2003 56 151 161 10.1007/s00239-002-2388-z 12574861 · DOI
  32. [35]Burns JH Strauss SY More closely related species are more ecologically similar in an experimental test Proc. Natl Acad. Sci. USA 2011 108 5302 5307 10.1073/pnas.1013003108 21402914 PMC3069184 · DOI
  33. [36]Garcia-Garcerà M Touchon M Brisse S Rocha EPC Metagenomic assessment of the interplay between the environment and the genetic diversification of Acinetobacter Environ. Microbiol. 2017 19 5010 5024 10.1111/1462-2920.13949 28967182 PMC5767740 · DOI
  34. [37]Petchey OL Gaston KJ Functional diversity: back to basics and looking forward Ecol. Lett. 2006 9 741 758 10.1111/j.1461-0248.2006.00924.x 16706917 · DOI
  35. [38]Dandekar AA Chugani S Greenberg EP Bacterial quorum sensing and metabolic incentives to cooperate Science 2012 338 264 266 10.1126/science.1227289 23066081 PMC3587168 · DOI
  36. [39]West SA Pen I Griffin AS Cooperation and competition between relatives Science 2002 296 72 75 10.1126/science.1065507 11935015 · DOI
  37. [40]Cianfanelli FR Monlezun L Coulthurst SJ Aim, load, fire: the type VI secretion system, a bacterial nanoweapon Trends Microbiol. 2016 24 51 62 10.1016/j.tim.2015.10.005 26549582 · DOI
  38. [41]Smith DR Chapman MR Economical evolution: microbes reduce the synthetic cost of extracellular proteins MBio 2010 1 e00131–10 e00131–18 10.1128/mBio.00131-10 20824102 PMC2932507 · DOI
  39. [42]Hamilton WD The genetical theory of kin selection J. Theor. Biol. 1964 7 1 52 10.1016/0022-5193(64)90038-4 5875341 · DOI · Paper page
  40. [43]Ubeda C Djukovic A Isaac S Roles of the intestinal microbiota in pathogen protection Clin. Transl. Immunol. 2017 6 e128 10.1038/cti.2017.2 PMC5311919 28243438 · DOI
  41. [44]Kerr B Riley MA Feldman MW Bohannan BJM Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors Nature 2002 418 171 174 10.1038/nature00823 12110887 · DOI
  42. [45]Gerlach R Hensel M Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens Int. J. Med. Microbiol. 2007 297 401 415 10.1016/j.ijmm.2007.03.017 17482513 · DOI
  43. [46]Deakin WJ Broughton WJ Symbiotic use of pathogenic strategies: rhizobial protein secretion systems Nat. Rev. Microbiol. 2009 7 312 320 10.1038/nrmicro2091 19270720 · DOI
  44. [47]Granato ET Ziegenhain C Marvig RL Kümmerli R Low spatial structure and selection against secreted virulence factors attenuates pathogenicity in Pseudomonas aeruginosa ISME J. 2018 12 2907 2918 10.1038/s41396-018-0231-9 30065310 PMC6215480 · DOI
  45. [48]Allen RC McNally L Popat R Brown SP Quorum sensing protects bacterial co-operation from exploitation by cheats ISME J. 2016 10 1706 1716 10.1038/ismej.2015.232 26744811 PMC4918439 · DOI
  46. [49]Minsky A Summers RG Knowles JR Secretion of beta-lactamase into the periplasm of Escherichia coli: evidence for a distinct release step associated with a conformational change Proc. Natl Acad. Sci. USA 1986 83 4180 4184 10.1073/pnas.83.12.4180 3520569 PMC323695 · DOI
  47. [50]Kümmerli R Brown SP Molecular and regulatory properties of a public good shape the evolution of cooperation PNAS 2010 107 18921 18926 10.1073/pnas.1011154107 20944065 PMC2973908 · DOI
  48. [51]McNally L Killing by Type VI secretion drives genetic phase separation and correlates with increased cooperation Nat. Commun. 2017 8 14371 11 10.1038/ncomms14371 28165005 PMC5303878 · DOI
  49. [52]García-Bayona L Comstock LE Bacterial antagonism in host-associated microbial communities Science 2018 361 eaat2456 10.1126/science.aat2456 30237322 · DOI
  50. [53]Hibbing ME Fuqua C Parsek MR Peterson SB Bacterial competition: surviving and thriving in the microbial jungle Nat. Rev. Microbiol. 2010 8 15 25 10.1038/nrmicro2259 19946288 PMC2879262 · DOI
  51. [54]Niehus R Picot A Oliveira NM Mitri S Foster KR The evolution of siderophore production as a competitive trait Evolution 2017 71 1443 1455 10.1111/evo.13230 28323325 · DOI
  52. [55]McNally L Viana M Brown SP Cooperative secretions facilitate host range expansion in bacteria Nat. Commun. 2014 5 4594 4598 10.1038/ncomms5594 25091146 PMC4143932 · DOI
  53. [56]Nawrocki EP Eddy SR Computational identification of functional RNA homologs in metagenomic data RNA Biol. 2013 10 1170 1179 10.4161/rna.25038 23722291 PMC3849165 · DOI
  54. [57]Capella-Gutiérrez S Silla-Martínez JM Gabaldón T trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Bioinformatics 2009 25 1972 1973 10.1093/bioinformatics/btp348 19505945 PMC2712344 · DOI
  55. [58]Edgar RC Search and clustering orders of magnitude faster than BLAST Bioinformatics 2010 26 2460 2461 10.1093/bioinformatics/btq461 20709691 · DOI
  56. [59]Cole JR The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy Nucleic Acids Res. 2003 31 442 443 10.1093/nar/gkg039 12520046 PMC165486 · DOI
  57. [60]Lou Jost Entropy and diversity Oikos 2006 113 363 375 10.1111/j.2006.0030-1299.14714.x · DOI · Paper page
  58. [61]Whitman, W. B. et al. Bergey’s Manual of Systematics of Archaea and Bacteria. 1–5 (Wiley, 2015).
  59. [62]Yarza P Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences Nat. Rev. Microbiol. 2014 12 635 645 10.1038/nrmicro3330 25118885 · DOI
  60. [63]Tamames J Abellan JJ Pignatelli M Camacho A Moya A Environmental distribution of prokaryotic taxa BMC Microbiol. 2010 10 85 10.1186/1471-2180-10-85 20307274 PMC2850351 · DOI
  61. [64]Nguyen L-T Schmidt HA Haeseler von A Minh BQ IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies Mol. Biol. Evol. 2015 32 268 274 10.1093/molbev/msu300 25371430 PMC4271533 · DOI · Paper page
  62. [65]Eddy SR A probabilistic model of local sequence alignment that simplifies statistical significance estimation PLoS Comput. Biol. 2008 4 e1000069 10.1371/journal.pcbi.1000069 18516236 PMC2396288 · DOI
  63. [66]Huerta-Cepas J eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences Nucleic Acids Res. 2016 44 D286 D293 10.1093/nar/gkv1248 26582926 PMC4702882 · DOI
  64. [67]de Jong A van Hijum SAFT Bijlsma JJE Kok J Kuipers OP BAGEL: a web-based bacteriocin genome mining tool Nucleic Acids Res. 2006 34 W273 W279 10.1093/nar/gkl237 16845009 PMC1538908 · DOI
  65. [68]Hammami R Zouhir A Ben Hamida J Fliss I BACTIBASE: a new web-accessible database for bacteriocin characterization BMC Microbiol. 2007 7 89 10.1186/1471-2180-7-89 17941971 PMC2211298 · DOI
  66. [69]Ledesma-Amaro R Nicaud J-M Metabolic engineering for expanding the substrate range of Yarrowia lipolytica Trends Biotechnol. 2016 34 798 809 10.1016/j.tibtech.2016.04.010 27207225 · DOI
  67. [70]UniProt Consortium T UniProt: the universal protein knowledgebase Nucleic Acids Res. 2018 46 2699 2699 10.1093/nar/gky092 29425356 PMC5861450 · DOI
  68. [71]Katoh K Misawa K Kuma K-I Miyata T MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform Nucleic Acids Res. 2002 30 3059 3066 10.1093/nar/gkf436 12136088 PMC135756 · DOI · Paper page
  69. [72]Bard, A. J. & Faulkner, L. R. Electrochemical Methods (Wiley, Hoboken, 1980).
  70. [73]Kalwarczyk T Tabaka M Holyst R Biologistics–diffusion coefficients for complete proteome of Escherichia coli Bioinformatics 2012 28 2971 2978 10.1093/bioinformatics/bts537 22942021 PMC3496334 · DOI
  71. [74]Brune D Kim S Predicting protein diffusion coefficients Proc. Natl Acad. Sci. USA 1993 90 3835 3839 10.1073/pnas.90.9.3835 8483901 PMC46400 · DOI
  72. [75]Mastro AM Babich MA Taylor WD Keith AD Diffusion of a small molecule in the cytoplasm of mammalian cells Proc. Natl Acad. Sci. USA 1984 81 3414 3418 10.1073/pnas.81.11.3414 6328515 PMC345518 · DOI · Paper page
  73. [76]Vieira-Silva S Rocha EPC An assessment of the impacts of molecular oxygen on the evolution of proteomes Mol. Biol. Evol. 2008 25 1931 1942 10.1093/molbev/msn142 18579552 PMC2515869 · DOI
  74. [77]Akashi H Gojobori T Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis Proc. Natl Acad. Sci. USA 2002 99 3695 3700 10.1073/pnas.062526999 11904428 PMC122586 · DOI

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Authors
Garcia-Garcera, M., & Rocha, E. P. C.
Affiliations
Centre National de la Recherche Scientifique (FR)
Corresponding author
Rocha, Eduardo P. C.
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2020-02-06
Volume
11
Issue
1
Pages
758-758
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-020-14572-x
PMC
PMC7005277
OpenAlex
W3005361961
Cited by
39
References
2
Citations by year
2026: 6 · 2025: 5 · 2024: 8 · 2023: 6 · 2022: 6 · 2021: 7 · 2020: 1
FWCI
2.60
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • IRIS (submittedVersion, cc-by)
  • SERVAL (Université de Lausanne) (submittedVersion, cc-by)
Funders
  • Agence Nationale de la Recherche (ANR-16-CONV-0005)
  • FP7 Ideas: European Research Council (281605)
Topics
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
extracellular proteins, bacterial community diversity, habitat structure, antagonism, nutrient acquisition, selection pressure, host-associated bacteria, bacterial evolution, 16S rRNA
MeSH terms
Bacteria, Bacterial Proteins, Extracellular Space, Genes, Bacterial, Models, Biological, Phylogeny, RNA, Bacterial, RNA, Ribosomal, 16S, Ecosystem, Biodiversity, Microbiota

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