1887

Abstract

Ecological dependencies – where organisms rely on other organisms for survival – are a ubiquitous feature of life on earth. Multicellular hosts rely on symbionts to provide essential vitamins and amino acids. Legume plants similarly rely on nitrogen-fixing rhizobia to convert atmospheric nitrogen to ammonia. In some cases, dependencies can arise via loss-of-function mutations that allow one partner to benefit from the actions of another. It is common in microbiology to label ecological dependencies between species as cooperation – making it necessary to invoke cooperation-specific frameworks to explain the phenomenon. However, in many cases, such traits are not (at least initially) cooperative, because they are not selected for because of the benefits they confer on a partner species. In contrast, dependencies in microbial communities may originate from fitness benefits gained from genomic-streamlining (i.e. Black Queen Dynamics). Here, we outline how the Black Queen Hypothesis predicts the formation of metabolic dependencies via loss-of-function mutations in microbial communities, without needing to invoke any cooperation-specific explanations. Furthermore we outline how the Black Queen Hypothesis can act as a blueprint for true cooperation as well as discuss key outstanding questions in the field. The nature of interactions in microbial communities can predict the ability of natural communities to withstand and recover from disturbances. Hence, it is vital to gain a deeper understanding of the factors driving these dynamic interactions over evolutionary time.

Funding
This study was supported by the:
  • UK Research and Innovation (Award MR/V022482/1)
    • Principle Award Recipient: ElzeHesse
  • 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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2024-02-22
2024-12-07
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References

  1. Martens EC, Lowe EC, Chiang H, Pudlo NA, Wu M et al. Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol 2011; 9:e1001221 [View Article] [PubMed]
    [Google Scholar]
  2. Magnúsdóttir S, Ravcheev D, de Crécy-Lagard V, Thiele I. Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes. Front Genet 2015; 6:148 [View Article] [PubMed]
    [Google Scholar]
  3. LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D et al. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol 2013; 24:160–168 [View Article] [PubMed]
    [Google Scholar]
  4. Lin R, Liu W, Piao M, Zhu H. A review of the relationship between the gut microbiota and amino acid metabolism. Amino Acids 2017; 49:2083–2090 [View Article] [PubMed]
    [Google Scholar]
  5. Salem H, Kaltenpoth M. Beetle-bacterial symbioses: endless forms most functional. Annu Rev Entomol 2022; 67:201–219 [View Article] [PubMed]
    [Google Scholar]
  6. Rosenberg E, Zilber-Rosenberg I. The hologenome concept of evolution after 10 years. Microbiome 2018; 6:78 [View Article] [PubMed]
    [Google Scholar]
  7. Douglas AE, Werren JH. Holes in the hologenome: why host-microbe symbioses are not holobionts. mBio 2016; 7:e02099 [View Article] [PubMed]
    [Google Scholar]
  8. D’Souza G, Shitut S, Preussger D, Yousif G, Waschina S et al. Ecology and evolution of metabolic cross-feeding interactions in bacteria. Nat Prod Rep 2018; 35:455–488 [View Article] [PubMed]
    [Google Scholar]
  9. Wade W. Unculturable bacteria--the uncharacterized organisms that cause oral infections. J R Soc Med 2002; 95:81–83 [View Article] [PubMed]
    [Google Scholar]
  10. D’Onofrio A, Crawford JM, Stewart EJ, Witt K, Gavrish E et al. Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem Biol 2010; 17:254–264 [View Article] [PubMed]
    [Google Scholar]
  11. Kost C, Patil KR, Friedman J, Garcia SL, Ralser M. Metabolic exchanges are ubiquitous in natural microbial communities. Nat Microbiol 2023; 8:2244–2252 [View Article] [PubMed]
    [Google Scholar]
  12. Morris JJ. Black Queen evolution: the role of leakiness in structuring microbial communities. Trends Genet 2015; 31:475–482 [View Article] [PubMed]
    [Google Scholar]
  13. Morris JJ, Lenski RE, Zinser ER. The Black Queen hypothesis: evolution of dependencies through adaptive gene loss. mBio 2012; 3:e00036-12 [View Article] [PubMed]
    [Google Scholar]
  14. 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]
  15. Mitri S, Xavier JB, Foster KR. Social evolution in multispecies biofilms. Proc Natl Acad Sci U S A 2011; 108 Suppl 2:10839–10846 [View Article] [PubMed]
    [Google Scholar]
  16. Oliveira NM, Niehus R, Foster KR. Evolutionary limits to cooperation in microbial communities. Proc Natl Acad Sci U S A 2014; 111:17941–17946 [View Article] [PubMed]
    [Google Scholar]
  17. 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]
  18. Dawkins R. The Selfish Gene London, England: Oxford University Press; 1976
    [Google Scholar]
  19. Waters CM, Bassler BL. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 2005; 21:319–346 [View Article] [PubMed]
    [Google Scholar]
  20. Cockburn DW, Koropatkin NM. Polysaccharide degradation by the intestinal microbiota and its influence on human health and disease. J Mol Biol 2016; 428:3230–3252 [View Article] [PubMed]
    [Google Scholar]
  21. Adak A, Khan MR. An insight into gut microbiota and its functionalities. Cell Mol Life Sci 2019; 76:473–493 [View Article] [PubMed]
    [Google Scholar]
  22. Gude S, Pherribo GJ, Taga ME. Emergence of metabolite provisioning as a by-product of evolved biological functions. mSystems 2020; 5:e00259-20 [View Article] [PubMed]
    [Google Scholar]
  23. McKinlay JB. Are bacteria leaky? Mechanisms of metabolite externalization in bacterial cross-feeding. Annu Rev Microbiol 2023; 77:277–297 [View Article] [PubMed]
    [Google Scholar]
  24. Pherribo GJ, Taga ME. Bacteriophage-mediated lysis supports robust growth of amino acid auxotrophs. ISME J 2023; 17:1785–1788 [View Article] [PubMed]
    [Google Scholar]
  25. Pande S, Kost C. Bacterial unculturability and the formation of intercellular metabolic networks. Trends Microbiol 2017; 25:349–361 [View Article] [PubMed]
    [Google Scholar]
  26. D’Souza G, Kost C. Experimental evolution of metabolic dependency in bacteria. PLoS Genet 2016; 12:e1006364 [View Article] [PubMed]
    [Google Scholar]
  27. Rhodius VA, Suh WC, Nonaka G, West J, Gross CA. Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biol 2006; 4:e2 [View Article] [PubMed]
    [Google Scholar]
  28. Waschina S, D’Souza G, Kost C, Kaleta C. Metabolic network architecture and carbon source determine metabolite production costs. FEBS J 2016; 283:2149–2163 [View Article] [PubMed]
    [Google Scholar]
  29. Lopez JG, Wingreen NS. Noisy metabolism can promote microbial cross-feeding. Elife 2022; 11:e70694 [View Article] [PubMed]
    [Google Scholar]
  30. Hesse E, O’Brien S, Luján AM, Sanders D, Bayer F et al. Stress causes interspecific facilitation within a compost community. Ecol Lett 2021; 24:2169–2177 [View Article] [PubMed]
    [Google Scholar]
  31. Piccardi P, Vessman B, Mitri S. Toxicity drives facilitation between 4 bacterial species. Proc Natl Acad Sci U S A 2019; 116:15979–15984 [View Article] [PubMed]
    [Google Scholar]
  32. Lee VT, Schneewind O. Protein secretion and the pathogenesis of bacterial infections. Genes Dev 2001; 15:1725–1752 [View Article] [PubMed]
    [Google Scholar]
  33. Ma W, Guttman DS. Evolution of prokaryotic and eukaryotic virulence effectors. Curr Opin Plant Biol 2008; 11:412–419 [View Article] [PubMed]
    [Google Scholar]
  34. Bassler BL, Losick R. Bacterially speaking. Cell 2006; 125:237–246 [View Article] [PubMed]
    [Google Scholar]
  35. McNally L, Viana M, Brown SP. Cooperative secretions facilitate host range expansion in bacteria. Nat Commun 2014; 5:4594 [View Article] [PubMed]
    [Google Scholar]
  36. Rankin DJ, Rocha EPC, Brown SP. What traits are carried on mobile genetic elements, and why?. Heredity (Edinb) 2011; 106:1–10 [View Article] [PubMed]
    [Google Scholar]
  37. Hao C, Dewar AE, West SA, Ghoul M. Gene transferability and sociality do not correlate with gene connectivity. Proc Biol Sci 2022; 289:20221819 [View Article] [PubMed]
    [Google Scholar]
  38. Garcia-Garcera M, Rocha EPC. Community diversity and habitat structure shape the repertoire of extracellular proteins in bacteria. Nat Commun 2020; 11:758 [View Article] [PubMed]
    [Google Scholar]
  39. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Annu Rev Microbiol 1995; 49:711–745 [View Article] [PubMed]
    [Google Scholar]
  40. Ryder C, Byrd M, Wozniak DJ. Role of polysaccharides in Pseudomonas aeruginosa biofilm development. Curr Opin Microbiol 2007; 10:644–648 [View Article] [PubMed]
    [Google Scholar]
  41. Popat R, Crusz SA, Messina M, Williams P, West SA et al. Quorum-sensing and cheating in bacterial biofilms. Proc Biol Sci 2012; 279:4765–4771 [View Article] [PubMed]
    [Google Scholar]
  42. Ren D, Madsen JS, Sørensen SJ, Burmølle M. High prevalence of biofilm synergy among bacterial soil isolates in cocultures indicates bacterial interspecific cooperation. ISME J 2015; 9:81–89 [View Article] [PubMed]
    [Google Scholar]
  43. Kramer J, Özkaya Ö, Kümmerli R. Bacterial siderophores in community and host interactions. Nat Rev Microbiol 2020; 18:152–163 [View Article] [PubMed]
    [Google Scholar]
  44. Amanatidou E, Matthews AC, Kuhlicke U, Neu TR, McEvoy JP et al. Biofilms facilitate cheating and social exploitation of β-lactam resistance in Escherichia coli. NPJ Biofilms Microbiomes 2019; 5:36 [View Article] [PubMed]
    [Google Scholar]
  45. Klümper U, Recker M, Zhang L, Yin X, Zhang T et al. Selection for antimicrobial resistance is reduced when embedded in a natural microbial community. ISME J 2019; 13:2927–2937 [View Article] [PubMed]
    [Google Scholar]
  46. O’Brien S, Hodgson DJ, Buckling A. Social evolution of toxic metal bioremediation in Pseudomonas aeruginosa. Proc Biol Sci 2014; 281:1787 [View Article] [PubMed]
    [Google Scholar]
  47. Velicer GJ, Plucain J. Evolution: bacterial territoriality as a byproduct of kin discriminatory warfare. Curr Biol 2016; 26:R364–6 [View Article] [PubMed]
    [Google Scholar]
  48. Smith P, Schuster M. Public goods and cheating in microbes. Curr Biol 2019; 29:R442–R447 [View Article] [PubMed]
    [Google Scholar]
  49. Hesse E, O’Brien S, Tromas N, Bayer F, Luján AM et al. Ecological selection of siderophore-producing microbial taxa in response to heavy metal contamination. Ecol Lett 2018; 21:117–127 [View Article] [PubMed]
    [Google Scholar]
  50. Morris JJ, Johnson ZI, Szul MJ, Keller M, Zinser ER. Dependence of the cyanobacterium Prochlorococcus on hydrogen peroxide scavenging microbes for growth at the ocean’s surface. PLoS One 2011; 6:e16805 [View Article] [PubMed]
    [Google Scholar]
  51. Cooksey DA. Molecular mechanisms of copper resistance and accumulation in bacteria. FEMS Microbiol Rev 1994; 14:381–386 [View Article] [PubMed]
    [Google Scholar]
  52. Cervantes C, Ji G, Ramírez JL, Silver S. Resistance to arsenic compounds in microorganisms. FEMS Microbiol Rev 1994; 15:355–367 [View Article] [PubMed]
    [Google Scholar]
  53. O’Brien S, Buckling A. The sociality of bioremediation: Hijacking the social lives of microbial populations to clean up heavy metal contamination. EMBO Rep 2015; 16:1241–1245 [View Article] [PubMed]
    [Google Scholar]
  54. Cazorla FM, Arrebola E, Sesma A, Pérez-García A, Codina JC et al. Copper resistance in Pseudomonas syringae strains isolated from mango is encoded mainly by plasmids. Phytopathology 2002; 92:909–916 [View Article] [PubMed]
    [Google Scholar]
  55. Sorg RA, Lin L, van Doorn GS, Sorg M, Olson J et al. Collective resistance in microbial communities by intracellular antibiotic deactivation. PLoS Biol 2016; 14:e2000631 [View Article] [PubMed]
    [Google Scholar]
  56. McCutcheon JP, Moran NA. Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 2011; 10:13–26 [View Article] [PubMed]
    [Google Scholar]
  57. Giovannoni SJ, Cameron Thrash J, Temperton B. Implications of streamlining theory for microbial ecology. ISME J 2014; 8:1553–1565 [View Article] [PubMed]
    [Google Scholar]
  58. Vernyik V, Karcagi I, Tímár E, Nagy I, Györkei Á et al. Exploring the fitness benefits of genome reduction in Escherichia coli by a selection-driven approach. Sci Rep 2020; 10:7345 [View Article] [PubMed]
    [Google Scholar]
  59. D’Souza G, Waschina S, Pande S, Bohl K, Kaleta C et al. Less is more: selective advantages can explain the prevalent loss of biosynthetic genes in bacteria. Evolution 2014; 68:2559–2570 [View Article] [PubMed]
    [Google Scholar]
  60. Rozen DE, Lenski RE. Long-term experimental evolution in Escherichia coli. VIII. Dynamics of a balanced polymorphism. Am Nat 2000; 155:24–35 [View Article] [PubMed]
    [Google Scholar]
  61. Adkins-Jablonsky SJ, Clark CM, Papoulis SE, Kuhl MD, Morris JJ. Market forces determine the distribution of a leaky function in a simple microbial community. Proc Natl Acad Sci U S A 2021; 118:e2109813118 [View Article] [PubMed]
    [Google Scholar]
  62. Mas A, Jamshidi S, Lagadeuc Y, Eveillard D, Vandenkoornhuyse P. Beyond the Black Queen hypothesis. ISME J 2016; 10:2085–2091 [View Article] [PubMed]
    [Google Scholar]
  63. Pastore AI, Barabás G, Bimler MD, Mayfield MM, Miller TE. The evolution of niche overlap and competitive differences. Nat Ecol Evol 2021; 5:330–337 [View Article] [PubMed]
    [Google Scholar]
  64. Griffin AS, West SA, Buckling A. Cooperation and competition in pathogenic bacteria. Nature 2004; 430:1024–1027 [View Article] [PubMed]
    [Google Scholar]
  65. Foster KR, Bell T. Competition, not cooperation, dominates interactions among culturable microbial species. Curr Biol 2012; 22:1845–1850 [View Article] [PubMed]
    [Google Scholar]
  66. Palmer JD, Foster KR. Bacterial species rarely work together. Science 2022; 376:581–582 [View Article] [PubMed]
    [Google Scholar]
  67. Kehe J, Ortiz A, Kulesa A, Gore J, Blainey PC et al. Positive interactions are common among culturable bacteria. Sci Adv 2021; 7:eabi7159 [View Article] [PubMed]
    [Google Scholar]
  68. Hammarlund SP, Harcombe WR. Refining the stress gradient hypothesis in a microbial community. Proc Natl Acad Sci U S A 2019; 116:15760–15762 [View Article] [PubMed]
    [Google Scholar]
  69. Lawrence D, Fiegna F, Behrends V, Bundy JG, Phillimore AB et al. Species interactions alter evolutionary responses to a novel environment. PLoS Biol 2012; 10:e1001330 [View Article] [PubMed]
    [Google Scholar]
  70. Coyte KZ, Schluter J, Foster KR. The ecology of the microbiome: networks, competition, and stability. Science 2015; 350:663–666 [View Article] [PubMed]
    [Google Scholar]
  71. Scheuerl T, Hopkins M, Nowell RW, Rivett DW, Barraclough TG et al. Bacterial adaptation is constrained in complex communities. Nat Commun 2020; 11:754 [View Article] [PubMed]
    [Google Scholar]
  72. Cairns J, Jokela R, Becks L, Mustonen V, Hiltunen T. Repeatable ecological dynamics govern the response of experimental communities to antibiotic pulse perturbation. Nat Ecol Evol 2020; 4:1385–1394 [View Article] [PubMed]
    [Google Scholar]
  73. Evans R, Beckerman AP, Wright RCT, McQueen-Mason S, Bruce NC et al. Eco-evolutionary dynamics set the tempo and trajectory of metabolic evolution in multispecies communities. Curr Biol 2020; 30:4984–4988 [View Article] [PubMed]
    [Google Scholar]
  74. Morris JJ, Papoulis SE, Lenski RE. Coexistence of evolving bacteria stabilized by a shared Black Queen function. Evolution 2014; 68:2960–2971 [View Article] [PubMed]
    [Google Scholar]
  75. Perlin MH, Clark DR, McKenzie C, Patel H, Jackson N et al. Protection of Salmonella by ampicillin-resistant Escherichia coli in the presence of otherwise lethal drug concentrations. Proc Biol Sci 2009; 276:3759–3768 [View Article] [PubMed]
    [Google Scholar]
  76. Frost I, Smith WPJ, Mitri S, Millan AS, Davit Y et al. Cooperation, competition and antibiotic resistance in bacterial colonies. ISME J 2018; 12:1582–1593 [View Article] [PubMed]
    [Google Scholar]
  77. Patel M, Raymond B, Bonsall MB, West SA. Crystal toxins and the volunteer’s dilemma in bacteria. J Evol Biol 2019; 32:310–319 [View Article] [PubMed]
    [Google Scholar]
  78. Brockhurst MA, Buckling A, Racey D, Gardner A. Resource supply and the evolution of public-goods cooperation in bacteria. BMC Biol 2008; 6:20 [View Article] [PubMed]
    [Google Scholar]
  79. Luo H, Csuros M, Hughes AL, Moran MA. Evolution of divergent life history strategies in marine alphaproteobacteria. mBio 2013; 4:e00373-13 [View Article] [PubMed]
    [Google Scholar]
  80. Browne HP, Forster SC, Anonye BO, Kumar N, Neville BA et al. Culturing of “unculturable” human microbiota reveals novel taxa and extensive sporulation. Nature 2016; 533:543–546 [View Article] [PubMed]
    [Google Scholar]
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