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Microbial Interactions

Microbes live all around us, and in us, and are central to health and wellbeing. A lot of what microbes do they do in dense groups where social interaction is rife. Sometimes they help each other by secreting signals and growth-promoting enzymes. Sometimes they harm each other with powerful toxins and molecular spearguns. Why then do some microbes cooperate with one another while others engage in mutual destruction? Cooperation within a microbial community can bring with it both virulent disease and antibiotic resistance. Moreover, we now realise that our health rests upon cooperation with vast numbers of symbiotic microbes that we carry on and inside us: the mammalian microbiome. Understanding what causes microbes to cooperate, therefore, is important for both medicine and biology.

When will cooperation evolve within a species of microbe?

We study microbes by applying the theory that was first developed to predict the balance between cooperation and conflict in humans and other animals, including game theory, kin selection theory and multilevel selection theory. This work has helped to identify a number of key processes that affect the balance between cooperation and competition in microbes.

1. Emergent genetic structure. Microbes undergo genetic bottlenecks as they divide on a surface, which leads to regions of genetically-identical cells that share a common evolutionary interest. We have shown how this process can lead to cooperation using an individual-based model and followed the effects of bottlenecks on genetic diversity in colonies of real bacteria, showing that spatial structure is important for traits such as cooperative mechanisms of antibiotic resistance.

Xavier, J.B., and Foster, K.R. 2007 Cooperation and conflict in microbial biofilms. Proceedings of the National Academy of Sciences, 104: 876-881; Foster, K. R. and Xavier, J. B. 2007 Cooperation: Bridging ecology and sociobiology. Current Biology, 17: R319-R321; Nadell CD, Xavier J, Levin SA, & Foster, KR 2008 The evolution of quorum sensing in bacterial biofilms. PLoS Biology, 6: e14, Nadell CD, Xavier J, & Foster, KR 2009 The sociobiology of biofilms. FEMS microbiology reviews, 33: 206-224; Nadell CD, Foster KR, Xavier J. 2010 Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Computational Biology, 6: e1000716; Korolev KS, Xavier JB, Nelson DR, Foster KR 2011. A quantitative test of population genetics using spatio-genetic patterns in bacterial colonies. American Naturalist, 178: 538-552.; Kim W, Racimo F, Schluter J, Levy SB, Foster KR. 2014. Importance of Positioning for Microbial Evolution. Proceedings of the National Academy of Sciences, 111, E1639–E1647; Schluter S, Schoech A, Foster KR, Mitri S. 2016. The evolution of quorum sensing as a mechanism to infer kinship. PLoS Computational Biology, 12: e1004848; Nadell CD, Drescher K, Foster KR. 2016 Spatial structure, cooperation, and competition in biofilms, Nature Reviews Microbiology, 14: 589-600; Frost I, Smith W, Mitri S, San Millan A, Davit Y, Osborne JM, Pitt-Francis JM, Maclean C, Foster KR. 2018. Cooperation, competition and antibiotic resistance in bacterial colonies.  ISME journal, 12: 1582–1593.

2. Incomplete cell separation. Another way to form groups of genetically identical cells is to not divide properly. We have shown that the budding yeast Saccharomyces cerevisiae does this and that this can help cells to use cooperative enzymes. Is this the reason why multicellularity first evolved?

Koschwanez J, Foster KR, Murray AJ. 2011. Sucrose utilization in budding yeast as a model for the origin of undifferentiated multicellularity. Plos Biology, 9(8): e1001122; Koschwanez J, Foster KR, Murray AJ. 2013. Improved use of a public good selects for the evolution of undifferentiated multicellularity. eLife, 2:e00367.

3. Genetic recognition. Cells can directly recognise other cooperating cells and preferentially interact with them, which prevents non-cooperators from benefiting from the investments of cooperators. We have shown that cells of the budding yeast Saccharomyces cerevisiae are capable of this impressive form of discrimination by virtue of a single gene FLO1. This produces a sticky protein that allows cells to find other cells making the protein by the simple virtue that they are more likely to stick to each other.

Smukalla S, Caldara M, Pochet N, Beauvais A, Guadagnini S, Yan C, Vinces MD, Jansen A, Christine Prevost M, Latge J, Fink GR, Foster KR, Verstrepen KJ 2008. FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell, 135: 727-737

4. Metabolic prudence. if cells only produce cooperative traits when it is cheap to do so, then they can be prosocial at little or no cost to themselves. We have found that Pseudomonas aeruginosa does just this, secreting carbon-rich rhamnolipids that help other cells when there is excess carbon in the environment.

Xavier J, Kim W, Foster KR 2011 A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa. Molecular Microbiology 79, 166-179

5. Pleiotropic constraints. If cooperative traits are genetically linked to traits that provide a benefit to the individual cells, then this will constrain mutations that produce non-cooperative phenotypes because the mutation will also remove the individual benefit. We have shown that such genes exist in the slime mould Dictyostelium discoideum.

Foster KR., Shaulsky G, Strassmann, J. E., Queller, D. C., Thompson, C. R. L. 2004. Pleiotropy as a mechanism to stabilise cooperation. Nature 431: 693-696; Foster, K.R., Parkinson, K. and Thompson, C. R. L. 2007 What can microbial genetics teach sociobiology? Trends in Genetics, 23:73-80; Foster KR. 2011 The sociobiology of molecular systems. Nature Reviews Genetics, 12: 193-203.   


When will cooperation evolve between different species of microbes?

We believe that cooperation between different microbial species is relatively rare. Our models suggest that cooperation among different species is difficult to maintain as it requires that the cells of one species can both help another, and that this help can be returned. Moreover, we have assessed the propensity for cooperation among different microbial species and it appears to be rare. However, competition between strains is common and a driver of many processes in microbial communities, both evolutionary and ecological.

Foster, K.R., Wenseleers, T. 2006. A general model for the evolution of mutualisms Journal of Evolutionary Biology, 19: 1283-1293; Mitri S, Xavier J, Foster KR 2011 Social evolution in multispecies biofilms Proceedings of the National Academy of Sciences, 108: 10839-46; Foster KR, Bell T. 2012. Competition, not cooperation, dominates interactions among culturable microbial species. Current biology 22, 1845–1850; Cornforth DM, Foster KR 2013 Competition sensing: the social side of bacterial stress responses. Nature Reviews Microbiology, 4, 285-93; Oliveira NM, Niehus R, Foster KR. 2014 The evolutionary limits to cooperation in microbial communities. Proceedings of the National Academy of Sciences, 111: 17941-17946; Oliveira NM, Martinez-Garcia E, Xavier J, Durham WM, Kolter R, Kim W, and Foster KR. 2015. Biofilm formation as a response to ecological competitionPLoS Biology, 13: e1002191; Coyte K Tabuteaue, H, Gaffney EA, Foster KR, Durham WH 2017. Microbial competition in porous environments can select against rapid biofilm growth. Proceedings of the National Academy of Sciences, 114E161–E170; Rakoff-Nahoum S, Foster KR, Comstock L. 2016. The evolution of cooperation within the gut microbiota. Nature, 533: 255–259.


When will cooperation evolve between a host and their microbiota?

Many animals, including humans, carry a vast number of microbes around with them that help with digestion and defence against pathogens. We believe that this cooperative relationship arises through a combination of microbial interactions and active host mechanisms to prevent the evolution of microbes that simply treat the host as a food source and do not provide any benefits. We are studying the mammalian microbiome using a combination of individual based modelling, network modelling, and experimentation.

Schluter J, Foster KR. 2012. The evolution of mutualism in gut microbiota via host epithelial selection. PLoS Biology, 10(11): e1001424; Schluter J, Nadell CD, Bassler BL and Foster KR. 2015 Adhesion as a weapon in microbial competition. ISME journal, 9, 139-149; Coyte KZ, Schluter J, Foster KR. 2015. The ecology of the microbiome: networks, competition, and stabilityScience, 350: 663-666; McLoughlin K, Schluter K, Rakoff-Nahoum S, Smith A, Foster KR. 2016. Host selection of microbiota via differential adhesion. Cell Host and Microbe, 19: 550–559.  Rakoff-Nahoum S, Foster KR, Comstock L. 2016. The evolution of cooperation within the gut microbiota. Nature, 533: 255–259; Foster KR, Schluter J, Coyte KZ and Rakoff-Nahoum S. 2017. The evolution of the host microbiome as an ecosystem on a leash. Nature, 548: 43-51; Johnson K, Foster KR. 2018.  Why does the microbiome affect behaviour? Nature Reviews Microbiology, online early.