1932

Abstract

Mutually beneficial interspecific interactions are abundant throughout the natural world, including between microbes. Mutualisms between microbes are critical for everything from human health to global nutrient cycling. Studying model microbial mutualisms in the laboratory enables highly controlled experiments for developing and testing evolutionary and ecological hypotheses. In this review, we begin by describing the tools available for studying model microbial mutualisms. We then outline recent insights that laboratory systems have shed on the evolutionary origins, evolutionary dynamics, and ecological features of microbial mutualism. We touch on gaps in our current understanding of microbial mutualisms, note connections to mutualism in nonmicrobial systems, and call attention to open questions ripe for future study.

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2021-11-03
2024-03-28
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Literature Cited

  1. Adamowicz EM, Flynn J, Hunter RC, Harcombe WR 2018. Cross-feeding modulates antibiotic tolerance in bacterial communities. ISME J 12:112723–35
    [Google Scholar]
  2. Adamowicz EM, Harcombe WR. 2020. Weakest-link dynamics predict apparent antibiotic interactions in a model cross-feeding community. Antimicrob. Agents Chemother. 64:11e00465-20
    [Google Scholar]
  3. Adamowicz EM, Muza M, Chacón JM, Harcombe WR. 2020. Cross-feeding modulates the rate and mechanism of antibiotic resistance evolution in a model microbial community of Escherichia coli and Salmonella enterica. PLOS Pathog 16:7e1008700
    [Google Scholar]
  4. Afkhami ME, Rudgers JA, Stachowicz JJ. 2014. Multiple mutualist effects: conflict and synergy in multispecies mutualisms. Ecology 95:4833–44
    [Google Scholar]
  5. Allee WC. 1927. Animal aggregations. Q. Rev. Biol. 2:3367–98
    [Google Scholar]
  6. Allison DG, Matthews MJ 1992. Effect of polysaccharide interactions on antibiotic susceptibility of Pseudomonas aeruginosa. J. Appl. Bacteriol. 73:6484–88
    [Google Scholar]
  7. Amor DR, Montañez R, Duran-Nebreda S, Solé R. 2017. Spatial dynamics of synthetic microbial mutualists and their parasites. PLOS Comput. Biol. 13:8e1005689
    [Google Scholar]
  8. Basan M, Hui S, Okano H, Zhang Z, Shen Y et al. 2015. Overflow metabolism in Escherichia coli results from efficient proteome allocation. Nature 528:758099–104
    [Google Scholar]
  9. Bergstrom CT, Lachmann M. 2003. The Red King effect: when the slowest runner wins the coevolutionary race. PNAS 100:2593–98
    [Google Scholar]
  10. Bertaux F, Sosa-Carillo S, Fraisse A, Aditya C, Furstenheim M, Batt G 2021. Enhancing bioreactor arrays for automated measurements and reactive control with ReacSight. bioRxiv 2020.12.27.424467. https://doi.org/10.1101/2020.12.27.424467
    [Crossref]
  11. Bertness MD, Callaway R. 1994. Positive interactions in communities. Trends Ecol. Evol. 9:5191–93
    [Google Scholar]
  12. Blount ZD, Lenski RE, Losos JB. 2018. Contingency and determinism in evolution: replaying life's tape. Science 362:6415eaam5979
    [Google Scholar]
  13. Bronstein JL 2015. Mutualism Oxford, UK: Oxford Univ. Press
  14. Bryant MP, Wolin EA, Wolin MJ, Wolfe RS. 1967. Methanobacillus omelianskii, a symbiotic association of two species of bacteria. Arch. Mikrobiol. 59:120–31
    [Google Scholar]
  15. Bull JJ, Harcombe WR. 2009. Population dynamics constrain the cooperative evolution of cross-feeding. PLOS ONE 4:1e4115
    [Google Scholar]
  16. Burke MK, Liti G, Long AD 2014. Standing genetic variation drives repeatable experimental evolution in outcrossing populations of Saccharomyces cerevisiae. Mol. Biol. Evol. 31:123228–39
    [Google Scholar]
  17. Chacón JM, Möbius W, Harcombe WR 2018. The spatial and metabolic basis of colony size variation. ISME J 12:3669–80
    [Google Scholar]
  18. Chacón JM, Shaw AK, Harcombe WR. 2020. Increasing growth rate slows adaptation when genotypes compete for diffusing resources. PLOS Comput. Biol. 16:1e1007585
    [Google Scholar]
  19. Chamberlain SA, Bronstein JL, Rudgers JA. 2014. How context dependent are species interactions?. Ecol. Lett. 17:7881–90
    [Google Scholar]
  20. Chomicki G, Kiers ET, Renner SS. 2020. The evolution of mutualistic dependence. Annu. Rev. Ecol. Evol. Syst. 51:409–32
    [Google Scholar]
  21. Chubiz LM, Granger BR, Segrè D, Harcombe WR. 2015. Species interactions differ in their genetic robustness. Front. Microbiol. 6:271
    [Google Scholar]
  22. Connor RC. 1986. Pseudo-reciprocity: investing in mutualism. Anim. Behav. 34:51562–66
    [Google Scholar]
  23. Coyte KZ, Tabuteau H, Gaffney EA, Foster KR, Durham WM. 2017. Microbial competition in porous environments can select against rapid biofilm growth. PNAS 114:2E161–70
    [Google Scholar]
  24. Dal Co A, van Vliet S, Kiviet DJ, Schlegel S, Ackermann M 2020. Short-range interactions govern the dynamics and functions of microbial communities. Nat. Ecol. Evol. 4:3366–75
    [Google Scholar]
  25. Dallinger WH. 1887. The president's address. J. R. Microsc. Soc. 7:2185–99
    [Google Scholar]
  26. Douglas SM, Chubiz LM, Harcombe WR, Ytreberg FM, Marx CJ. 2016. Parallel mutations result in a wide range of cooperation and community consequences in a two-species bacterial consortium. . PLOS ONE 11:9e0161837
    [Google Scholar]
  27. D'Souza G, Shitut S, Preussger D, Yousif G, Waschina S, Kost C 2018. Ecology and evolution of metabolic cross-feeding interactions in bacteria. Nat. Prod. Rep. 35:5455–88
    [Google Scholar]
  28. D'Souza G, Waschina S, Pande S, Bohl K, Kaleta C, Kost C 2014. Less is more: selective advantages can explain the prevalent loss of biosynthetic genes in bacteria. Evolution 68:92559–70
    [Google Scholar]
  29. Duarte NC, Becker SA, Jamshidi N, Thiele I, Mo ML et al. 2007. Global reconstruction of the human metabolic network based on genomic and bibliomic data. PNAS 104:61777–82
    [Google Scholar]
  30. Ebert D, Fields PD. 2020. Host-parasite co-evolution and its genomic signature. Nat. Rev. Genet. 21:12754–68
    [Google Scholar]
  31. Elena SF, Lenski RE 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. . Nat. Rev. Genet. 4:6457–69
    [Google Scholar]
  32. Estrela S, Libby E, Van Cleve J, Débarre F, Deforet M et al. 2019. Environmentally mediated social dilemmas. Trends Ecol. Evol. 34:16–18
    [Google Scholar]
  33. Estrela S, Morris JJ, Kerr B 2016. Private benefits and metabolic conflicts shape the emergence of microbial interdependencies. Environ. Microbiol. 18:51415–27
    [Google Scholar]
  34. Eyre-Walker A, Keightley PD 2007. The distribution of fitness effects of new mutations. Nat. Rev. Genet. 8:8610–18
    [Google Scholar]
  35. Fazzino L, Anisman J, Chacón JM, Heineman RH, Harcombe WR. 2020. Lytic bacteriophage have diverse indirect effects in a synthetic cross-feeding community. ISME J 14:1123–34
    [Google Scholar]
  36. Flynn JM, Cameron LC, Wiggen TD, Dunitz JM, Harcombe WR, Hunter RC. 2020. Disruption of cross-feeding inhibits pathogen growth in the sputa of patients with cystic fibrosis. mSphere 5:2e00343-20
    [Google Scholar]
  37. Flynn JM, Niccum D, Dunitz JM, Hunter RC. 2016. Evidence and role for bacterial mucin degradation in cystic fibrosis airway disease. PLOS Pathog 12:8e1005846
    [Google Scholar]
  38. Fritts RK, Bird JT, Behringer MG, Lipzen A, Martin J et al. 2020. Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community. ISME J 14:112816–28
    [Google Scholar]
  39. Gaba S, Ebert D. 2009. Time-shift experiments as a tool to study antagonistic coevolution. Trends Ecol. Evol. 24:4226–32
    [Google Scholar]
  40. Gause GF. 1934. The Struggle for Existence Baltimore, MD: Williams & Wilkins
  41. Goldberg Y, Friedman J. 2021. Positive interactions within and between populations decrease the likelihood of evolutionary rescue. PLOS Comput. Biol. 17:2e1008732
    [Google Scholar]
  42. Goldford JE, Lu N, Baji D, Sanchez-Gorostiaga A, Segrè D et al. 2018. Emergent simplicity in microbial community assembly. Science 361:6401469–74
    [Google Scholar]
  43. Green R, Sonal, Wang L, Hart SFM, Lu W et al. 2020. Metabolic excretion associated with nutrient-growth dysregulation promotes the rapid evolution of an overt metabolic defect. PLOS Biol 18:8e3000757
    [Google Scholar]
  44. Gude S, Pherribo GJ, Taga ME. 2020. Emergence of metabolite provisioning as a by-product of evolved biological functions. mSystems 5:3e00259-20
    [Google Scholar]
  45. Hammarlund SP, Chacón JM, Harcombe WR. 2019. A shared limiting resource leads to competitive exclusion in a cross-feeding system. . Environ. Microbiol. 21:2759–71
    [Google Scholar]
  46. Hammarlund SP, Gedeon T, Carlson RP, Harcombe WR. 2021. Limitation by a shared mutualist promotes coexistence of multiple competing partners. Nat. Comm. 12:1619
    [Google Scholar]
  47. Hammarlund SP, Harcombe WR. 2019. Refining the stress gradient hypothesis in a microbial community. PNAS 116:3215760–62
    [Google Scholar]
  48. Harcombe WR. 2010. Novel cooperation experimentally evolved between species. Evolution 64:72166–72
    [Google Scholar]
  49. Harcombe WR, Betts A, Shapiro JW, Marx CJ. 2016. Adding biotic complexity alters the metabolic benefits of mutualism. Evolution 70:81871–81
    [Google Scholar]
  50. Harcombe WR, Chacón JM, Adamowicz EM, Chubiz LM, Marx CJ. 2018. Evolution of bidirectional costly mutualism from byproduct consumption. PNAS 115:4712000–4
    [Google Scholar]
  51. Harcombe WR, Riehl WJ, Dukovski I, Granger BR, Betts A et al. 2014. Metabolic resource allocation in individual microbes determines ecosystem interactions and spatial dynamics. Cell Rep 7:41104–15
    [Google Scholar]
  52. Harte J, Kinzig AP. 1993. Mutualism and competition between plants and decomposers: implications for nutrient allocation in ecosystems. Am. Nat. 141:6829–46
    [Google Scholar]
  53. Helling RB, Vargas CN, Adams J. 1987. Evolution of Escherichia coli during growth in a constant environment. Genetics 116:3349–58
    [Google Scholar]
  54. Hillesland KL, Lim S, Flowers JJ, Turkarslan S, Pinel N et al. 2014. Erosion of functional independence early in the evolution of a microbial mutualism. PNAS 111:4114822–27
    [Google Scholar]
  55. Hillesland KL, Stahl DA. 2010. Rapid evolution of stability and productivity at the origin of a microbial mutualism. PNAS 107:52124–29
    [Google Scholar]
  56. Hoek TA, Axelrod K, Biancalani T, Yurtsev EA, Liu J, Gore J. 2016. Resource availability modulates the cooperative and competitive nature of a microbial cross-feeding mutualism. PLOS Biol 14:8e1002540
    [Google Scholar]
  57. Hom EFY, Murray AW. 2014. Niche engineering demonstrates a latent capacity for fungal-algal mutualism. Science 345:619294–98
    [Google Scholar]
  58. Husser MC, Vo PQ, Sinha H, Ahmadi F, Shih SC. 2018. An automated induction microfluidics system for synthetic biology. ACS Synth. Biol. 7:3933–44
    [Google Scholar]
  59. Jessup CM, Kassen R, Forde SE, Kerr B, Buckling A et al. 2004. Big questions, small worlds: microbial model systems in ecology. Trends Ecol. Evol. 19:4189–97
    [Google Scholar]
  60. Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM 2010. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. PNAS 107:52093–98
    [Google Scholar]
  61. Kehe J, Kulesa A, Ortiz A, Ackerman CM, Thakku SG et al. 2019. Massively parallel screening of synthetic microbial communities. PNAS 116:2612804–9
    [Google Scholar]
  62. Kehe J, Ortiz A, Kulesa A, Gore J, Blainey PC, Friedman J. 2020. Positive interactions are common among culturable bacteria. bioRxiv 2020.06.24.169474. https://doi.org/10.1101/2020.06.24.169474
    [Crossref]
  63. Kim HJ, Boedicker JQ, Choi JW, Ismagilov RF. 2008. Defined spatial structure stabilizes a synthetic multispecies bacterial community. PNAS 105:4718188–93
    [Google Scholar]
  64. Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith VS. 2004. Species coextinctions and the biodiversity crisis. Science 305:56901632–34
    [Google Scholar]
  65. Kosina SM, Danielewicz MA, Mohammed M, Ray J, Suh Y et al. 2016. Exometabolomics assisted design and validation of synthetic obligate mutualism. ACS Synth. Biol. 5:7569–76
    [Google Scholar]
  66. LaSarre B, Deutschbauer AM, Love CE, McKinlay JB. 2020. Covert cross-feeding revealed by genome-wide analysis of fitness determinants in a synthetic bacterial mutualism. Appl. Environ. Microbiol. 86:13e00543-20
    [Google Scholar]
  67. LaSarre B, McCully AL, Lennon JT, McKinlay JB. 2017. Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients. ISME J 11:2337–48
    [Google Scholar]
  68. Lau JA, terHorst CP 2020. Evolutionary responses to global change in species-rich communities. Ann. N. Y. Acad. Sci. 1476:143–58
    [Google Scholar]
  69. Lawrence D, Fiegna F, Behrends V, Bundy JG, Phillimore AB et al. 2012. Species interactions alter evolutionary responses to a novel environment. PLOS Biol 10:5e1001330
    [Google Scholar]
  70. Lenski RE. 2017. What is adaptation by natural selection? Perspectives of an experimental microbiologist. PLOS Genet 13:4e1006668
    [Google Scholar]
  71. Lilja EE, Johnson DR. 2019. Substrate cross-feeding affects the speed and trajectory of molecular evolution within a synthetic microbial assemblage. BMC Evol. Biol. 19:1129
    [Google Scholar]
  72. Liu F, Mao J, Kong W, Hua Q, Feng Y et al. 2020. Interaction variability shapes succession of synthetic microbial ecosystems. Nat. Commun. 11:1309
    [Google Scholar]
  73. Liu Z, Müller J, Li T, Alvey RM, Vogl K et al. 2013. Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium “Chlorochromatium aggregatum. .” Genome Biol 14:11R127
    [Google Scholar]
  74. Lloyd CJ, King ZA, Sandberg TE, Hefner Y, Olson CA et al. 2019. The genetic basis for adaptation of model-designed syntrophic co-cultures. PLOS Comput. Biol. 15:3e1006213
    [Google Scholar]
  75. MacLean RC, Gudelj I. 2006. Resource competition and social conflict in experimental populations of yeast. Nature 441:7092498–501
    [Google Scholar]
  76. Marchal M, Goldschmidt F, Derksen-Müller SN, Panke S, Ackermann M, Johnson DR 2017. A passive mutualistic interaction promotes the evolution of spatial structure within microbial populations. . BMC Evol. Biol. 17:1106
    [Google Scholar]
  77. May RM. 1981. Theoretical Ecology: Principles and Applications Oxford, UK: Oxford Univ. Press
  78. McCully AL, LaSarre B, McKinlay JB 2017. Recipient-biased competition for an intracellularly generated cross-fed nutrient is required for coexistence of microbial mutualists. mBio 8:6e01620-17
    [Google Scholar]
  79. McGlynn SE, Chadwick GL, Kempes CP, Orphan VJ. 2015. Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature 526:7574531–35
    [Google Scholar]
  80. Mee MT, Collins JJ, Church GM, Wang HH. 2014. Syntrophic exchange in synthetic microbial communities. PNAS 111:20E2149–56
    [Google Scholar]
  81. Menon R, Korolev KS. 2015. Public good diffusion limits microbial mutualism. Phys. Rev. Lett. 114:16168102
    [Google Scholar]
  82. Meredith HR, Srimani JK, Lee AJ, Lopatkin AJ, You L. 2015. Collective antibiotic tolerance: mechanisms, dynamics and intervention. Nat. Chem. Biol. 11:3182–88
    [Google Scholar]
  83. Mintz-Oron S, Meir S, Malitsky S, Ruppin E, Aharoni A, Shlomi T 2012. Reconstruction of Arabidopsis metabolic network models accounting for subcellular compartmentalization and tissue-specificity. PNAS 109:1339–44
    [Google Scholar]
  84. Mitri S, Foster K 2013. The genotypic view of social interactions in microbial communities. Annu. Rev. Genet. 47:247–73
    [Google Scholar]
  85. Momeni B, Waite AJ, Shou W. 2013. Spatial self-organization favors heterotypic cooperation over cheating. eLife 2:e00960
    [Google Scholar]
  86. Moran NA, Baumann P. 2000. Bacterial endosymbionts in animals. Curr. Opin. Microbiol. 3:3270–75
    [Google Scholar]
  87. Morris JJ, Lenski RE, Zinser ER. 2012. The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. mBio 3:2e00036-12
    [Google Scholar]
  88. Müller MJI, Neugeboren BI, Nelson DR, Murray AW 2014. Genetic drift opposes mutualism during spatial population expansion. PNAS 111:31037–42
    [Google Scholar]
  89. Naeem S, Hahn DR, Schuurman G. 2000. Producer-decomposer co-dependency influences biodiversity effects. Nature 403:6771762–64
    [Google Scholar]
  90. Niehaus L, Boland I, Liu M, Chen K, Fu D et al. 2019. Microbial coexistence through chemical-mediated interactions. Nat. Commun. 10:12052
    [Google Scholar]
  91. Oliveira NM, Niehus R, Foster KR 2014. Evolutionary limits to cooperation in microbial communities. PNAS 111:5017941–46
    [Google Scholar]
  92. Ollerton J, Winfree R, Tarrant S 2011. How many flowering plants are pollinated by animals?. Oikos 120:3321–26
    [Google Scholar]
  93. Orphan VJ. 2009. Methods for unveiling cryptic microbial partnerships in nature. Curr. Opin. Microbiol. 12:3231–37
    [Google Scholar]
  94. Pacheco AR, Moel M, Segrè D. 2019. Costless metabolic secretions as drivers of interspecies interactions in microbial ecosystems. . Nat. Commun. 10:1103
    [Google Scholar]
  95. Pande S, Kost C 2017. Bacterial unculturability and the formation of intercellular metabolic networks. Trends Microbiol 25:5349–61
    [Google Scholar]
  96. Pande S, Merker H, Bohl K, Reichelt M, Schuster S et al. 2014. Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria. ISME J 8:5953–62
    [Google Scholar]
  97. Peay KG. 2016. The mutualistic niche: mycorrhizal symbiosis and community dynamics. Annu. Rev. Ecol. Evol. Syst. 47:143–64
    [Google Scholar]
  98. Piccardi P, Vessman B, Mitri S. 2019. Toxicity drives facilitation between 4 bacterial species. PNAS 116:3215979–84
    [Google Scholar]
  99. Pospíšil J, Vítovská D, Kofroňová O, Muchová K, Šanderová H et al. 2020. Bacterial nanotubes as a manifestation of cell death. Nat. Commun. 11:14963
    [Google Scholar]
  100. Preussger D, Giri S, Muhsal LK, Oña L, Kost C. 2020. Reciprocal fitness feedbacks promote the evolution of mutualistic cooperation. Curr. Biol. 30:183580–90.e7
    [Google Scholar]
  101. Ratzke C, Gore J. 2018. Modifying and reacting to the environmental pH can drive bacterial interactions. PLOS Biol 16:3e2004248
    [Google Scholar]
  102. Rietkerk M, Boerlijst MC, van Langevelde F, HilleRisLambers R, van de Koppel J et al. 2002. Self-organization of vegetation in arid ecosystems. Am. Nat. 160:4524–30
    [Google Scholar]
  103. Sachs JL, Mueller UG, Wilcox TP, Bull JJ. 2004. The evolution of cooperation. Q. Rev. Biol. 79:2135–60
    [Google Scholar]
  104. Schink B. 2002. Synergistic interactions in the microbial world. Antonie Van Leeuwenhoek 81:1257–61
    [Google Scholar]
  105. Shou W, Ram S, Vilar JMG 2007. Synthetic cooperation in engineered yeast populations. PNAS 104:61877–82
    [Google Scholar]
  106. Spribille T, Tuovinen V, Resl P, Vanderpool D, Wolinski H et al. 2016. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353:6298488–92
    [Google Scholar]
  107. Summers ZM, Fogarty HE, Leang C, Franks AE, Malvankar NS, Lovley DR. 2010. Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330:60091413–15
    [Google Scholar]
  108. Tecon R, Or D. 2017. Cooperation in carbon source degradation shapes spatial self-organization of microbial consortia on hydrated surfaces. Sci. Rep. 7:143726
    [Google Scholar]
  109. Tenaillon O, Rodríguez-Verdugo A, Gaut RL, McDonald P, Bennett AF et al. 2012. The molecular diversity of adaptive convergence. Science 335:6067457–61
    [Google Scholar]
  110. Turkarslan S, Stopnisek N, Thompson AW, Arens CE, Valenzuela JJ et al. 2021. Synergistic epistasis enhances the co-operativity of mutualistic interspecies interactions. ISME J 15:223347
    [Google Scholar]
  111. Valiente-Banuet A, Ezcurra E. 1991. Shade as a cause of the association between the cactus Neobuxbaumia tetetzo and the nurse plant Mimosa luisana in the Tehuacan Valley, Mexico. J. Ecol. 79:4961–71
    [Google Scholar]
  112. van Ham RCHJ, Kamerbeek J, Palacios C, Rausell C, Abascal F et al. 2003. Reductive genome evolution in Buchnera aphidicola. PNAS 100:2581–86
    [Google Scholar]
  113. van Tatenhove-Pel RJ, Rijavec T, Lapanje A, van Swam I, Zwering E et al. 2021. Microbial competition reduces metabolic interaction distances to the low μm-range. ISME J 15:3688–701
    [Google Scholar]
  114. Van Valen L. 1973. A new evolutionary law. Evol. Theory. 1:1–30
    [Google Scholar]
  115. Wanner G, Vogl K, Overmann J. 2008. Ultrastructural characterization of the prokaryotic symbiosis in “Chlorochromatium aggregatum. .” J. Bacteriol. 190:103721–30
    [Google Scholar]
  116. Weiblen GD, Treiber EL. 2015. Evolutionary origins and diversification of mutualism. Mutualism37–56
    [Google Scholar]
  117. West SA, Griffin AS, Gardner A, Diggle SP 2006. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4:8597–607
    [Google Scholar]
  118. Wintermute EH, Silver PA. 2010. Emergent cooperation in microbial metabolism. Mol. Syst. Biol. 6:407
    [Google Scholar]
  119. Yang DD, Alexander A, Kinnersley M, Cook E, Caudy A et al. 2020. Fitness and productivity increase with ecotypic diversity among Escherichia coli strains that coevolved in a simple, constant environment. Appl. Environ. Microbiol. 86:8e00051-20
    [Google Scholar]
  120. Yurtsev EA, Conwill A, Gore J 2016. Oscillatory dynamics in a bacterial cross-protection mutualism. PNAS 113:226236–41
    [Google Scholar]
  121. Zahran HH. 2001. Rhizobia from wild legumes: diversity, taxonomy, ecology, nitrogen fixation and biotechnology. J. Biotechnol. 91:2–3143–53
    [Google Scholar]
  122. Zelezniak A, Andrejev S, Ponomarova O, Mende DR, Bork P, Patil KR. 2015. Metabolic dependencies drive species co-occurrence in diverse microbial communities. PNAS 112:206449–54
    [Google Scholar]
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