1887

Abstract

Bacteria cooperate by working collaboratively to defend their colonies, share nutrients, and resist antibiotics. Nevertheless, our understanding of these remarkable behaviours primarily comes from studying a few well-characterized species. Consequently, there is a significant gap in our understanding of microbial social traits, particularly in natural environments. To address this gap, we can use bioinformatic tools to identify genes that control cooperative or otherwise social traits. Existing tools address this challenge through two approaches. One approach is to identify genes that encode extracellular proteins, which can provide benefits to neighbouring cells. An alternative approach is to predict gene function using annotation tools. However, these tools have several limitations. Not all extracellular proteins are cooperative, and not all cooperative behaviours are controlled by extracellular proteins. Furthermore, existing functional annotation methods frequently miss known cooperative genes. We introduce SOCfinder as a new tool to find bacterial genes that control cooperative or otherwise social traits. SOCfinder combines information from several methods, considering if a gene is likely to [ 1 ] code for an extracellular protein [ 2 ], have a cooperative functional annotation, or [ 3 ] be part of the biosynthesis of a cooperative secondary metabolite. We use data on two extensively-studied species ( and ) to show that SOCfinder is better at finding known cooperative genes than existing tools. We also use theory from population genetics to identify a signature of kin selection in SOCfinder cooperative genes, which is lacking in genes identified by existing tools. SOCfinder opens up a number of exciting directions for future research, and is available to download from https://github.com/lauriebelch/SOCfinder.

Funding
This study was supported by the:
  • BBSRC
    • Principle Award Recipient: ZoharKatz
  • European Research Council (Award 834164)
    • Principle Award Recipient: StuartA West
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2023-12-20
2024-12-05
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References

  1. West SA, Griffin AS, Gardner A, Diggle SP. Social evolution theory for microorganisms. Nat Rev Microbiol 2006; 4:597–607 [View Article] [PubMed]
    [Google Scholar]
  2. Strassmann JE, Gilbert OM, Queller DC. Kin discrimination and cooperation in microbes. Annu Rev Microbiol 2011; 65:349–367 [View Article] [PubMed]
    [Google Scholar]
  3. Ghoul M, Andersen SB, West SA. Sociomics: using omic approaches to understand social evolution. Trends Genet 2017; 33:408–419 [View Article] [PubMed]
    [Google Scholar]
  4. Mitri S, Foster KR. The genotypic view of social interactions in microbial communities. Annu Rev Genet 2013; 47:247–273 [View Article] [PubMed]
    [Google Scholar]
  5. West SA, Cooper GA, Ghoul MB, Griffin AS. Ten recent insights for our understanding of cooperation. Nat Ecol Evol 2021; 5:419–430 [View Article] [PubMed]
    [Google Scholar]
  6. Kümmerli R, Santorelli LA, Granato ET, Dumas Z, Dobay A et al. Co-evolutionary dynamics between public good producers and cheats in the bacterium Pseudomonas aeruginosa. J Evol Biol 2015; 28:2264–2274 [View Article] [PubMed]
    [Google Scholar]
  7. Griffin AS, West SA, Buckling A. Cooperation and competition in pathogenic bacteria. Nature 2004; 430:1024–1027 [View Article] [PubMed]
    [Google Scholar]
  8. Harrison F, Buckling A. Siderophore production and biofilm formation as linked social traits. ISME J 2009; 3:632–634 [View Article] [PubMed]
    [Google Scholar]
  9. Kümmerli R, Ross-Gillespie A. Explaining the sociobiology of pyoverdin producing Pseudomonas: a comment on Zhang and Rainey (2013). Evolution 2014; 68:3337–3343 [View Article] [PubMed]
    [Google Scholar]
  10. O’Brien S, Hodgson DJ, Buckling A. Social evolution of toxic metal bioremediation in Pseudomonas aeruginosa. Proc Biol Sci 2014; 281:20140858 [View Article] [PubMed]
    [Google Scholar]
  11. Kümmerli R, Griffin AS, West SA, Buckling A, Harrison F. Viscous medium promotes cooperation in the pathogenic bacterium Pseudomonas aeruginosa. Proc R Soc B Biol Sci 2009; 276:3531–3538 [View Article] [PubMed]
    [Google Scholar]
  12. Dragoš A, Kiesewalter H, Martin M, Hsu C-Y, Hartmann R et al. Division of labor during biofilm matrix production. Curr Biol 2018; 28:1903–1913 [View Article] [PubMed]
    [Google Scholar]
  13. Chai Y, Chu F, Kolter R, Losick R. Bistability and biofilm formation in Bacillus subtilis. Mol Microbiol 2008; 67:254–263 [View Article] [PubMed]
    [Google Scholar]
  14. O’Brien S, Luján AM, Paterson S, Cant MA, Buckling A. Adaptation to public goods cheats in Pseudomonas aeruginosa. Proc R Soc B Biol Sci 2017; 284:20171089 [View Article] [PubMed]
    [Google Scholar]
  15. Andersen SB, Marvig RL, Molin S, Krogh Johansen H, Griffin AS. Long-term social dynamics drive loss of function in pathogenic bacteria. Proc Natl Acad Sci U S A 2015; 112:10756–10761 [View Article] [PubMed]
    [Google Scholar]
  16. Cordero OX, Ventouras L-A, DeLong EF, Polz MF. Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations. Proc Natl Acad Sci U S A 2012; 109:20059–20064 [View Article] [PubMed]
    [Google Scholar]
  17. Sathe S, Mathew A, Agnoli K, Eberl L, Kümmerli R. Genetic architecture constrains exploitation of siderophore cooperation in the bacterium Burkholderia cenocepacia. Evol Lett 2019; 3:610–622 [View Article] [PubMed]
    [Google Scholar]
  18. Chen R, Déziel E, Groleau M-C, Schaefer AL, Greenberg EP. Social cheating in a Pseudomonas aeruginosa quorum-sensing variant. Proc Natl Acad Sci U S A 2019; 116:7021–7026 [View Article] [PubMed]
    [Google Scholar]
  19. van Gestel J, Weissing FJ, Kuipers OP, Kovács AT. Density of founder cells affects spatial pattern formation and cooperation in Bacillus subtilis biofilms. ISME J 2014; 8:2069–2079 [View Article] [PubMed]
    [Google Scholar]
  20. Yu NY, Wagner JR, Laird MR, Melli G, Rey S et al. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 2010; 26:1608–1615 [View Article] [PubMed]
    [Google Scholar]
  21. Törönen P, Holm L. PANNZER-a practical tool for protein function prediction. Protein Sci 2022; 31:118–128 [View Article] [PubMed]
    [Google Scholar]
  22. Taglialegna A, Lasa I, Valle J. Amyloid structures as biofilm matrix scaffolds. J Bacteriol 2016; 198:2579–2588 [View Article] [PubMed]
    [Google Scholar]
  23. Bruce JB, West SA, Griffin AS. Functional amyloids promote retention of public goods in bacteria. Proc R Soc B Biol Sci 2019; 286:20190709 [View Article] [PubMed]
    [Google Scholar]
  24. Ringel MT, Brüser T. The biosynthesis of pyoverdines. Microb Cell 2018; 5:424–437 [View Article] [PubMed]
    [Google Scholar]
  25. Sandoz KM, Mitzimberg SM, Schuster M. Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci U S A 2007; 104:15876–15881 [View Article] [PubMed]
    [Google Scholar]
  26. Simonet C, McNally L. Kin selection explains the evolution of cooperation in the gut microbiota. Proc Natl Acad Sci U S A 2021; 118:e2016046118 [View Article] [PubMed]
    [Google Scholar]
  27. Nogueira T, Touchon M, Rocha EPC. Rapid evolution of the sequences and gene repertoires of secreted proteins in bacteria. PLoS One 2012; 7:1–10 [View Article] [PubMed]
    [Google Scholar]
  28. Nogueira T, Rankin DJ, Touchon M, Taddei F, Brown SP et al. Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence. Curr Biol 2009; 19:1683–1691 [View Article] [PubMed]
    [Google Scholar]
  29. Garcia-Garcera M, Rocha EPC. Community diversity and habitat structure shape the repertoire of extracellular proteins in bacteria. Nat Commun 2020; 11:1–11 [View Article] [PubMed]
    [Google Scholar]
  30. Hao C, Dewar AE, West SA, Ghoul M. Gene transferability and sociality do not correlate with gene connectivity. Proc R Soc B Biol Sci 2022; 289:20221819 [View Article] [PubMed]
    [Google Scholar]
  31. Dewar AE, Thomas JL, Scott TW, Wild G, Griffin AS et al. Plasmids do not consistently stabilize cooperation across bacteria but may promote broad pathogen host-range. Nat Ecol Evol 2021; 5:1624–1636 [View Article] [PubMed]
    [Google Scholar]
  32. Belcher LJ, Dewar AE, Ghoul M, West SA. Kin selection for cooperation in natural bacterial populations. Proc Natl Acad Sci U S A 2022; 119:e2119070119 [View Article] [PubMed]
    [Google Scholar]
  33. Belcher LJ, Dewar AE, Hao C, Ghoul M, West SA. Signatures of kin selection in a natural population of the bacteria Bacillus subtilis. Evol Lett 2023; 7:1–21 [View Article] [PubMed]
    [Google Scholar]
  34. Tai J-S, Mukherjee S, Nero T, Olson R, Tithof J et al. Social evolution of shared biofilm matrix components. Proc Natl Acad Sci U S A 2022; 119:e2123469119 [View Article] [PubMed]
    [Google Scholar]
  35. Pollak S, Omer-Bendori S, Even-Tov E, Lipsman V, Bareia T et al. Facultative cheating supports the coexistence of diverse quorum-sensing alleles. Proc Natl Acad Sci U S A 2016; 113:2152–2157 [View Article] [PubMed]
    [Google Scholar]
  36. West SA, Griffin AS, Gardner A. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol 2007; 20:415–432 [View Article] [PubMed]
    [Google Scholar]
  37. West SA, Griffin AS, Gardner A. Evolutionary explanations for cooperation. Curr Biol 2007; 17:R661–R672 [View Article] [PubMed]
    [Google Scholar]
  38. Ghoul M, Griffin AS, West SA. Toward an evolutionary definition of cheating. Evolution 2014; 68:318–331 [View Article] [PubMed]
    [Google Scholar]
  39. Hamilton WD. The genetical evolution of social behaviour. II. J Theor Biol 1964; 7:17–52 [View Article] [PubMed]
    [Google Scholar]
  40. Oster GF, Wilson E. Caste and Ecology in the Social Insects Princeton University Press; 1978
    [Google Scholar]
  41. Wilkinson GS. Reciprocal food sharing in the vampire bat. Nature 1984; 308:181–184 [View Article]
    [Google Scholar]
  42. Clutton-Brock TH, Brotherton PN, Russell AF, O’Riain MJ, Gaynor D et al. Cooperation, control, and concession in meerkat groups. Science 2001; 291:478–481 [View Article] [PubMed]
    [Google Scholar]
  43. West SA, Buckling A. Cooperation, virulence and siderophore production in bacterial parasites. Proc R Soc B Biol Sci 2003; 270:37–44 [View Article] [PubMed]
    [Google Scholar]
  44. Schuster M, Sexton DJ, Hense BA. Why quorum sensing controls private goods. Front Microbiol 2017; 8:1–16 [View Article] [PubMed]
    [Google Scholar]
  45. Ghoul M, West SA, Johansen HK, Molin S, Harrison OB et al. Bacteriocin-mediated competition in cystic fibrosis lung infections. Proc R Soc B Biol Sci 2015; 282:20150972 [View Article] [PubMed]
    [Google Scholar]
  46. Granato ET, Meiller-Legrand TA, Foster KR, Meiller-Legrand TA, Foster KR. The evolution and ecology of bacterial warfare. Curr Biol 2019; 29:1–39 [View Article] [PubMed]
    [Google Scholar]
  47. Kessler E, Safrin M, Gustin JK, Ohman DE. Elastase and the LasA protease of Pseudomonas aeruginosa are secreted with their propeptides. J Biol Chem 1998; 273:30225–30231 [View Article] [PubMed]
    [Google Scholar]
  48. Diggle SP, Griffin AS, Campbell GS, West SA. Cooperation and conflict in quorum-sensing bacterial populations. Nature 2007; 450:411–414 [View Article] [PubMed]
    [Google Scholar]
  49. Özkaya Ö, Balbontín R, Gordo I, Xavier KB. Cheating on cheaters stabilizes cooperation in Pseudomonas aeruginosa. Curr Biol 2018; 28:2070–2080 [View Article] [PubMed]
    [Google Scholar]
  50. Jautzus T, van Gestel J, Kovács ÁT. Complex extracellular biology drives surface competition during colony expansion in Bacillus subtilis. ISME J 2022; 16:2320–2328 [View Article] [PubMed]
    [Google Scholar]
  51. Gardner A, Hardy ICW, Taylor PD, West SA. Spiteful soldiers and sex ratio conflict in polyembryonic parasitoid wasps. Am Nat 2007; 169:519–533 [View Article] [PubMed]
    [Google Scholar]
  52. McNally L, Viana M, Brown SP. Cooperative secretions facilitate host range expansion in bacteria. Nat Commun 2014; 5:4594 [View Article] [PubMed]
    [Google Scholar]
  53. Aramaki T, Blanc-Mathieu R, Endo H, Ohkubo K, Kanehisa M et al. KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics 2020; 36:2251–2252 [View Article] [PubMed]
    [Google Scholar]
  54. Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 2021; 38:5825–5829 [View Article] [PubMed]
    [Google Scholar]
  55. Velicer GJ, Vos M. Sociobiology of the Myxobacteria. Annu Rev Microbiol 2009; 63:599–623 [View Article] [PubMed]
    [Google Scholar]
  56. Vos M, Velicer GJ. Social conflict in centimeter-and global-scale populations of the bacterium Myxococcus xanthus. Curr Biol 2009; 19:1763–1767 [View Article] [PubMed]
    [Google Scholar]
  57. Kessin RH. Dictyostelium: Evolution, Cell Biology, and the Development of Multicellularity Cambridge University Press; 2001 [View Article]
    [Google Scholar]
  58. Strassmann JE, Queller DC. Evolution of cooperation and control of cheating in a social microbe. Proc Natl Acad Sci U S A 2011; 108:10855–10862 [View Article] [PubMed]
    [Google Scholar]
  59. Strassmann JE, Zhu Y, Queller DC. Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 2000; 408:965–967 [View Article] [PubMed]
    [Google Scholar]
  60. Madgwick PG, Stewart B, Belcher LJ, Thompson CRL, Wolf JB. Strategic investment explains patterns of cooperation and cheating in a microbe. Proc Natl Acad Sci U S A 2018; 115:E4823–E4832 [View Article] [PubMed]
    [Google Scholar]
  61. Belcher LJ, Madgwick PG, Kuwana S, Stewart B, Thompson CRL et al. Developmental constraints enforce altruism and avert the tragedy of the commons in a social microbe. Proc Natl Acad Sci U S A 2022; 119:e2111233119 [View Article] [PubMed]
    [Google Scholar]
  62. de Oliveira JL, Morales AC, Stewart B, Gruenheit N, Engelmoer J et al. Conditional expression explains molecular evolution of social genes in a microbe. Nat Commun 2019; 10:3284 [View Article] [PubMed]
    [Google Scholar]
  63. Warner MR, Mikheyev AS, Linksvayer TA. Genomic signature of kin selection in an ant with obligately sterile workers. Mol Biol Evol 2017; 34:1780–1787 [View Article] [PubMed]
    [Google Scholar]
  64. Imrit MA, Dogantzis KA, Harpur BA, Zayed A. Eusociality influences the strength of negative selection on insect genomes: negative selection in social genomes. Proc R Soc B Biol Sci 2020; 287:1–7 [View Article]
    [Google Scholar]
  65. Sharrar AM, Crits-Christoph A, Méheust R, Diamond S, Starr EP et al. Bacterial secondary metabolite biosynthetic potential in soil varies with phylum, depth, and vegetation type. mBio 2020; 11:e00416-20 [View Article] [PubMed]
    [Google Scholar]
  66. Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP et al. antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 2021; 49:W29–W35 [View Article] [PubMed]
    [Google Scholar]
  67. Wang H, Fewer DP, Holm L, Rouhiainen L, Sivonen K. Atlas of nonribosomal peptide and polyketide biosynthetic pathways reveals common occurrence of nonmodular enzymes. Proc Natl Acad Sci U S A 2014; 111:9259–9264 [View Article] [PubMed]
    [Google Scholar]
  68. Zhang S, Mukherji R, Chowdhury S, Reimer L, Stallforth P. Lipopeptide-mediated bacterial interaction enables cooperative predator defense. Proc Natl Acad Sci U S A 2021; 118:e2013759118 [View Article] [PubMed]
    [Google Scholar]
  69. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 2016; 44:D457–D462 [View Article] [PubMed]
    [Google Scholar]
  70. McNally L, Bernardy E, Thomas J, Kalziqi A, Pentz J et al. Killing by Type VI secretion drives genetic phase separation and correlates with increased cooperation. Nat Commun 2017; 8:14371 [View Article] [PubMed]
    [Google Scholar]
  71. Linksvayer TA, Wade MJ. Genes with social effects are expected to harbor more sequence variation within and between species. Evolution 2009; 63:1685–1696 [View Article] [PubMed]
    [Google Scholar]
  72. Linksvayer TA, Wade MJ. Theoretical predictions for sociogenomic data: the effects of Kin selection and sex-limited expression on the evolution of social insect genomes. Front Ecol Evol 2016; 4:1–10 [View Article]
    [Google Scholar]
  73. Van Dyken JD, Wade MJ. Detecting the molecular signature of social conflict: theory and a test with bacterial quorum sensing genes. Am Nat 2012; 179:436–450 [View Article] [PubMed]
    [Google Scholar]
  74. Van Dyken JD, Linksvayer TA, Wade MJ. Kin selection-mutation balance: a model for the origin, maintenance, and consequences of social cheating. Am Nat 2011; 177:288–300 [View Article] [PubMed]
    [Google Scholar]
  75. Hall DW, Goodisman MAD. The effects of kin selection on rates of molecular evolution in social insects. Evolution 2012; 66:2080–2093 [View Article] [PubMed]
    [Google Scholar]
  76. Schuster M, Lostroh CP, Ogi T, Greenberg EP. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 2003; 185:2066–2079 [View Article] [PubMed]
    [Google Scholar]
  77. Comella N, Grossman AD. Conservation of genes and processes controlled by the quorum response in bacteria: characterization of genes controlled by the quorum-sensing transcription factor ComA in Bacillus subtilis. Mol Microbiol 2005; 57:1159–1174 [View Article] [PubMed]
    [Google Scholar]
  78. Molle V, Fujita M, Jensen ST, Eichenberger P, González-Pastor JE et al. The Spo0A regulon of Bacillus subtilis. Mol Microbiol 2003; 50:1683–1701 [View Article] [PubMed]
    [Google Scholar]
  79. Kobayashi K. Gradual activation of the response regulator DegU controls serial expression of genes for flagellum formation and biofilm formation in Bacillus subtilis. Mol Microbiol 2007; 66:395–409 [View Article] [PubMed]
    [Google Scholar]
  80. Chong RA, Park H, Moran NA. Genome evolution of the obligate endosymbiont Buchnera aphidicola. Mol Biol Evol 2019; 36:1481–1489 [View Article] [PubMed]
    [Google Scholar]
  81. Stelzner K, Vollmuth N, Rudel T. Intracellular lifestyle of Chlamydia trachomatis and host-pathogen interactions. Nat Rev Microbiol 2023; 21:448–462 [View Article] [PubMed]
    [Google Scholar]
  82. Hansen AK, Moran NA. Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc Natl Acad Sci U S A 2011; 108:2849–2854 [View Article] [PubMed]
    [Google Scholar]
  83. Elwell C, Mirrashidi K, Engel J. Chlamydia cell biology and pathogenesis. Nat Rev Microbiol 2016; 14:385–400 [View Article] [PubMed]
    [Google Scholar]
  84. Blackwell GA, Hunt M, Malone KM, Lima L, Horesh G et al. Exploring bacterial diversity via a curated and searchable snapshot of archived DNA sequences. PLoS Biol 2021; 19:e3001421 [View Article] [PubMed]
    [Google Scholar]
  85. Blin K, Kim HU, Medema MH, Weber T. Recent development of antiSMASH and other computational approaches to mine secondary metabolite biosynthetic gene clusters. Brief Bioinform 2018; 20:1103–1113 [View Article] [PubMed]
    [Google Scholar]
  86. Blin K, Shaw S, Augustijn HE, Reitz ZL, Biermann F et al. antiSMASH 7.0: new and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Res 2023; 51:W46–W50 [View Article] [PubMed]
    [Google Scholar]
  87. Smith EE, Sims EH, Spencer DH, Kaul R, Olson MV. Evidence for diversifying selection at the pyoverdine locus of Pseudomonas aeruginosa. J Bacteriol 2005; 187:2138–2147 [View Article] [PubMed]
    [Google Scholar]
  88. Lee W, van Baalen M, Jansen VAA. An evolutionary mechanism for diversity in siderophore-producing bacteria. Ecol Lett 2012; 15:119–125 [View Article] [PubMed]
    [Google Scholar]
  89. Ostrowski EA, Shen Y, Tian X, Sucgang R, Jiang H et al. Genomic signatures of cooperation and conflict in the social amoeba. Curr Biol 2015; 25:1661–1665 [View Article] [PubMed]
    [Google Scholar]
  90. Lima De Oliveira J. Genomic Signatures of Selection and Non-Adaptive Evolution in a Social Microbe 2019
    [Google Scholar]
  91. Brandis G, Hughes D. The selective advantage of synonymous codon usage bias in Salmonella. PLoS Genet 20161–16 [View Article] [PubMed]
    [Google Scholar]
  92. Madgwick PG, Belcher LJ, Wolf JB. Greenbeard genes: theory and reality. Trends Ecol Evol 2019; 34:1–12 [View Article] [PubMed]
    [Google Scholar]
  93. Dawkins R. The Selfish Gene Oxford University Press; 1976
    [Google Scholar]
  94. Scott TW, Grafen A, West SA. Multiple social encounters can eliminate Crozier’s paradox and stabilise genetic kin recognition. Nat Commun 2022; 13:3902 [View Article] [PubMed]
    [Google Scholar]
  95. Grafen A. Do animals really recognize kin?. Anim Behav 1990; 39:42–54 [View Article]
    [Google Scholar]
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