in

Mutualism-enhancing mutations dominate early adaptation in a two-species microbial community

  • Agostini, S. et al. Ocean acidification drives community shifts towards simplified non-calcified habitats in a subtropical–temperate transition zone. Sci. Rep. 8, 11354 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Walther, G.-R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Gilbert, B. & Levine, J. M. Ecological drift and the distribution of species diversity. Proc. Biol. Sci. 284, 20170507 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • White, E. P. et al. A comparison of the species–time relationship across ecosystems and taxonomic groups. Oikos 112, 185–195 (2006).

    Article 

    Google Scholar 

  • Sax, D. F. & Gaines, S. D. Species invasions and extinction: the future of native biodiversity on islands. Proc. Natl Acad. Sci. USA 105, 11490–11497 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Thompson, J. N. Rapid evolution as an ecological process. Trends Ecol. Evol. 13, 329–332 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Post, D. M. & Palkovacs, E. P. Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play. Philos. Trans. R. Soc. Lond. B 364, 1629–1640 (2009).

    Article 

    Google Scholar 

  • Reznick, D. N. & Travis, J. Experimental studies of evolution and eco-evo dynamics in guppies (Poecilia reticulata). Annu. Rev. Ecol. Evol. Syst. https://doi.org/10.1146/annurev-ecolsys-110218-024926 (2019).

  • Hendry, A. P. Eco-evolutionary Dynamics (Princeton Univ. Press, 2020).

  • Schoener, T. W. The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science 331, 426–429 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Yoshida, T., Jones, L. E., Ellner, S. P., Fussmann, G. F. & Hairston, N. G. Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424, 303–306 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hansen, S. K., Rainey, P. B., Haagensen, J. A. J. & Molin, S. Evolution of species interactions in a biofilm community. Nature 445, 533–536 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hillesland, K. L. & Stahl, D. A. Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc. Natl Acad. Sci. USA 107, 2124–2129 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Turcotte, M. M., Reznick, D. N. & Hare, J. D. The impact of rapid evolution on population dynamics in the wild: experimental test of eco-evolutionary dynamics. Ecol. Lett. 14, 1084–1092 (2011).

    Article 
    PubMed 

    Google Scholar 

  • Lawrence, D. et al. Species interactions alter evolutionary responses to a novel environment. PLoS Biol. 10, e1001330 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Celiker, H. & Gore, J. Clustering in community structure across replicate ecosystems following a long-term bacterial evolution experiment. Nat. Commun. 5, 4643 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Andrade-Domínguez, A. et al. Eco-evolutionary feedbacks drive species interactions. ISME J. 8, 1041–1054 (2014).

    Article 
    PubMed 

    Google Scholar 

  • Reznick, D. Hard and soft selection revisited: how evolution by natural selection works in the real world. J. Hered. 107, 3–14 (2016).

    Article 
    PubMed 

    Google Scholar 

  • Matthews, B., Aebischer, T., Sullam, K. E., Lundsgaard-Hansen, B. & Seehausen, O. Experimental evidence of an eco-evolutionary feedback during adaptive divergence. Curr. Biol. 26, 483–489 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Harcombe, W. R., Chacón, J. M., Adamowicz, E. M., Chubiz, L. M. & Marx, C. J. Evolution of bidirectional costly mutualism from byproduct consumption. Proc. Natl Acad. Sci. USA 115, 12000–12004 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Preussger, D., Giri, S., Muhsal, L. K., Oña, L. & Kost, C. Reciprocal fitness feedbacks promote the evolution of mutualistic cooperation. Curr. Biol. https://doi.org/10.1016/j.cub.2020.06.100 (2020).

  • Adamowicz, E. M., Muza, M., Chacón, J. M. & Harcombe, W. R. 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, e1008700 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Rodríguez-Verdugo, A. & Ackermann, M. Rapid evolution destabilizes species interactions in a fluctuating environment. ISME J. 15, 450–460 (2021).

    Article 
    PubMed 

    Google Scholar 

  • Barber, J. N. et al. The evolution of coexistence from competition in experimental co-cultures of Escherichia coli and Saccharomyces cerevisiae. ISME J. 15, 746–761 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hart, S. F. M., Chen, C.-C. & Shou, W. Pleiotropic mutations can rapidly evolve to directly benefit self and cooperative partner despite unfavorable conditions. eLife 10, e57838 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kokko, H. et al. Can evolution supply what ecology demands? Trends Ecol. Evol. 32, 187–197 (2017).

    Article 
    PubMed 

    Google Scholar 

  • Nuismer, S. Introduction to Coevolutionary Theory (Macmillan Learning, 2017).

  • Stoltzfus, A. & McCandlish, D. M. Mutational biases influence parallel adaptation. Mol. Biol. Evol. 34, 2163–2172 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Payne, J. L. et al. Transition bias influences the evolution of antibiotic resistance in Mycobacterium tuberculosis. PLoS Biol. 17, e3000265 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Storz, J. F. et al. The role of mutation bias in adaptive molecular evolution: insights from convergent changes in protein function. Philos. Trans. R. Soc. Lond. B 374, 20180238 (2019).

    Article 
    CAS 

    Google Scholar 

  • Gomez, K., Bertram, J. & Masel, J. Mutation bias can shape adaptation in large asexual populations experiencing clonal interference. Proc. Biol. Sci. 287, 20201503 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Venkataram, S., Monasky, R., Sikaroodi, S. H., Kryazhimskiy, S. & Kacar, B. Evolutionary stalling and a limit on the power of natural selection to improve a cellular module. Proc. Natl Acad. Sci. USA 117, 18582–18590 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hom, E. F. Y. & Murray, A. W. Niche engineering demonstrates a latent capacity for fungal–algal mutualism. Science 345, 94–98 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wolfe, B. E. & Dutton, R. J. Fermented foods as experimentally tractable microbial ecosystems. Cell 161, 49–55 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Chacón, J. M., Hammarlund, S. P., Martinson, J. N. V., Smith, L. B. & Harcombe, W. R. The ecology and evolution of model microbial mutualisms. Annu. Rev. Ecol. Evol. Syst. 52, 363–384 (2021).

    Article 

    Google Scholar 

  • Blasche, S., Kim, Y., Oliveira, A. P. & Patil, K. R. Model microbial communities for ecosystems biology. Curr. Opin. Syst. Biol. 6, 51–57 (2017).

    Article 

    Google Scholar 

  • Levy, S. F. et al. Quantitative evolutionary dynamics using high-resolution lineage tracking. Nature 519, 181–186 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Venkataram, S. et al. Development of a comprehensive genotype-to-fitness map of adaptation-driving mutations in yeast. Cell 166, 1585–1596.e22 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jones, E. I., Bronstein, J. L. & Ferrière, R. The fundamental role of competition in the ecology and evolution of mutualisms. Ann. N. Y. Acad. Sci. 1256, 66–88 (2012).

    Article 
    PubMed 

    Google Scholar 

  • Boyer, S., Hérissant, L. & Sherlock, G. Adaptation is influenced by the complexity of environmental change during evolution in a dynamic environment. PLoS Genet. 17, e1009314 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Blundell, J. R. et al. The dynamics of adaptive genetic diversity during the early stages of clonal evolution. Nat. Ecol. Evol. 3, 293–301 (2019).

    Article 
    PubMed 

    Google Scholar 

  • Good, B. H., Rouzine, I. M., Balick, D. J., Hallatschek, O. & Desai, M. M. Distribution of fixed beneficial mutations and the rate of adaptation in asexual populations. Proc. Natl Acad. Sci. USA 109, 4950–4955 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Good, B. H., Martis, S. & Hallatschek, O. Adaptation limits ecological diversification and promotes ecological tinkering during the competition for substitutable resources. Proc. Natl Acad. Sci. USA 115, E10407–E10416 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhu, Y. O., Siegal, M. L., Hall, D. W. & Petrov, D. A. Precise estimates of mutation rate and spectrum in yeast. Proc. Natl Acad. Sci. USA 111, E2310–E2318 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dunham, M. J. et al. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 99, 16144–16149 (2002).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yona, A. H. et al. Chromosomal duplication is a transient evolutionary solution to stress. Proc. Natl Acad. Sci. USA 109, 21010–21015 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sunshine, A. B. et al. The fitness consequences of aneuploidy are driven by condition-dependent gene effects. PLoS Biol. 13, e1002155 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gerrish, P. J. & Lenski, R. E. The fate of competing beneficial mutations in an asexual population. Genetica 102-103, 127–144 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Desai, M. M. & Fisher, D. S. Beneficial mutation–selection balance and the effect of linkage on positive selection. Genetics 176, 1759–1798 (2007).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Schiffels, S., Szöllosi, G. J., Mustonen, V. & Lässig, M. Emergent neutrality in adaptive asexual evolution. Genetics 189, 1361–1375 (2011).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nguyen, Ba,A. N. et al. High-resolution lineage tracking reveals travelling wave of adaptation in laboratory yeast. Nature 575, 494–499 (2019).

    Article 

    Google Scholar 

  • Foster, K. R., Shaulsky, G., Strassmann, J. E., Queller, D. C. & Thompson, C. R. L. Pleiotropy as a mechanism to stabilize cooperation. Nature 431, 693–696 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Sachs, J. L., Mueller, U. G., Wilcox, T. P. & Bull, J. J. The evolution of cooperation. Q. Rev. Biol. 79, 135–160 (2004).

    Article 
    PubMed 

    Google Scholar 

  • Harcombe, W. Novel cooperation experimentally evolved between species. Evolution 64, 2166–2172 (2010).

    PubMed 

    Google Scholar 

  • Vasi, F., Travisano, M. & Lenski, R. E. Long-term experimental evolution in Escherichia coli. II. Changes in life-history traits during adaptation to a seasonal environment. Am. Nat. 144, 432–456 (1994).

    Article 

    Google Scholar 

  • MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, 2001).

  • Reznick, D., Bryant, M. J. & Bashey, F. r– and K-selection revisited: the role of population regulation in life-history evolution. Ecology 83, 1509–1520 (2002).

    Article 

    Google Scholar 

  • Mueller, L. D. & Ayala, F. J. Trade-off between r-selection and K-selection in Drosophila populations. Proc. Natl Acad. Sci. USA 78, 1303–1305 (1981).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Novak, M., Pfeiffer, T., Lenski, R. E., Sauer, U. & Bonhoeffer, S. Experimental tests for an evolutionary trade-off between growth rate and yield in E. coli. Am. Nat. 168, 242–251 (2006).

    Article 
    PubMed 

    Google Scholar 

  • Bachmann, H. et al. Availability of public goods shapes the evolution of competing metabolic strategies. Proc. Natl Acad. Sci. USA 110, 14302–14307 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lipson, D. A. The complex relationship between microbial growth rate and yield and its implications for ecosystem processes. Front. Microbiol. 6, 615 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Orivel, J. et al. Trade-offs in an ant–plant–fungus mutualism. Proc. Biol. Sci. 284, 20161679 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Fritts, R. K. et al. Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community. ISME J. 14, 2816–2828 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wortel, M. T., Noor, E., Ferris, M., Bruggeman, F. J. & Liebermeister, W. Metabolic enzyme cost explains variable trade-offs between microbial growth rate and yield. PLoS Comput. Biol. 14, e1006010 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cheng, C. et al. Laboratory evolution reveals a two-dimensional rate-yield tradeoff in microbial metabolism. PLoS Comput. Biol. 15, e1007066 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Luckinbill, L. S. r and K selection in experimental populations of Escherichia coli. Science 202, 1201–1203 (1978).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Oxman, E., Alon, U. & Dekel, E. Defined order of evolutionary adaptations: experimental evidence. Evolution 62, 1547–1554 (2008).

    Article 
    PubMed 

    Google Scholar 

  • Jasmin, J.-N., Dillon, M. M. & Zeyl, C. The yield of experimental yeast populations declines during selection. Proc. Biol. Sci. 279, 4382–4388 (2012).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Laan, L., Koschwanez, J. H. & Murray, A. W. Evolutionary adaptation after crippling cell polarization follows reproducible trajectories. eLife 4, e09638 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Blount, Z. D., Lenski, R. E. & Losos, J. B. Contingency and determinism in evolution: replaying life’s tape. Science 362, eaam5979 (2018).

    Article 
    PubMed 

    Google Scholar 

  • Fukami, T. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu. Rev. Ecol. Evol. Syst. 46, 1–23 (2015).

    Article 

    Google Scholar 

  • Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Meyer, J. R. et al. Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 335, 428–432 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Herron, M. D. & Doebeli, M. Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biol. 11, e1001490 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hillesland, K. L. et al. Erosion of functional independence early in the evolution of a microbial mutualism. Proc. Natl Acad. Sci. USA 111, 14822–14827 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Meroz, N., Tovi, N., Sorokin, Y. & Friedman, J. Community composition of microbial microcosms follows simple assembly rules at evolutionary timescales. Nat. Commun. 12, 2891 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • MacLean, R. C. The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies. Heredity 100, 471–477 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Dunn, B. et al. Recurrent rearrangement during adaptive evolution in an interspecific yeast hybrid suggests a model for rapid introgression. PLoS Genet. 9, e1003366 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Barillot, E., Lacroix, B. & Cohen, D. Theoretical analysis of library screening using a N-dimensional pooling strategy. Nucleic Acids Res. 19, 6241–6247 (1991).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Baym, M., Shaket, L., Anzai, I. A., Adesina, O. & Barstow, B. Rapid construction of a whole-genome transposon insertion collection for Shewanella oneidensis by Knockout Sudoku. Nat. Commun. 7, 13270 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Baym, M. et al. Inexpensive multiplexed library preparation for megabase-sized genomes. PLoS ONE 10, e0128036 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Venkataram, S., Kuo, H., Hom, E., Kryazhimskiy, S. Early adaptation in a microbial community is dominated by mutualism-enhancing mutations. Dryad https://doi.org/10.6076/D14K5X (2022).


  • Source: Ecology - nature.com

    Higher-order interactions shape microbial interactions as microbial community complexity increases

    Genetic diversity and structure in wild Robusta coffee (Coffea canephora A. Froehner) populations in Yangambi (DR Congo) and their relation to forest disturbance