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Understanding the Evolution of Interspecies Interactions in Microbial 2 Communities 3 bioRxiv preprint doi: https://doi.org/10.1101/770156; this version posted September 16, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Article title: Understanding the evolution of interspecies interactions in microbial 2 communities 3 4 Authors: Florien A. Gorter1,2, Michael Manhart1,2,3, and Martin Ackermann1,2 5 6 Author affiliations: 7 1 Institute of Biogeochemistry and Pollutant Dynamics, Department of Environmental 8 Systems Science, ETH Zürich, Zürich, Switzerland 9 2 Department of Environmental Microbiology, Swiss Federal Institute of Aquatic Science and 10 Technology (Eawag), Dübendorf, Switzerland 11 3 Institute of Integrative Biology, ETH Zürich, Zürich, Switzerland 12 13 Email: [email protected] (corresponding author), [email protected], 14 [email protected] 15 16 Keywords: microbial communities, evolution, interspecific interactions, experimental 17 evolution, mathematical modelling, spatial structure, mutualism 18 bioRxiv preprint doi: https://doi.org/10.1101/770156; this version posted September 16, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 19 Abstract 20 21 Microbial communities are complex multi-species assemblages that are characterized by a 22 multitude of interspecies interactions, which can range from mutualism to competition. The 23 overall sign and strength of interspecies interactions have important consequences for 24 emergent community-level properties such as productivity and stability. It is not well 25 understood whether and how interspecies interactions change over evolutionary timescales. 26 Here, we review the empirical evidence that evolution is an important driver of microbial 27 community properties and dynamics on timescales that have traditionally been regarded as 28 purely ecological. Next, we briefly discuss different modelling approaches to study evolution 29 of communities, emphasizing the similarities and differences between evolutionary and 30 ecological perspectives. We then propose a simple conceptual model for the evolution of 31 communities. Specifically, we propose that the evolution of interspecies interactions depends 32 crucially on the spatial structure of the environment. We predict that in well-mixed 33 environments, traits will be selected exclusively for their direct fitness effects, while in 34 spatially structured environments, traits may also be selected for their indirect fitness effects. 35 Selection of indirectly beneficial traits should result in an increase in interaction strength over 36 time, while selection of directly beneficial traits should not have such a systematic effect. We 37 tested our intuitions using a simple quantitative model and found support for our hypotheses. 38 The next step will be to test these hypotheses experimentally and provide input for a more 39 refined version of the model in turn, thus closing the scientific cycle of models and 40 experiments. 41 bioRxiv preprint doi: https://doi.org/10.1101/770156; this version posted September 16, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 42 Introduction 43 44 Microorganisms play key roles in biogeochemical cycling, industry, and health and disease of 45 humans, animals, and plants[1–5]. For example, the roughly 1030 microbial cells on our 46 planet contain ten times more nitrogen than all plants combined and are responsible for half 47 of the global production of O2[6]. Almost all of these microorganisms reside in communities, 48 which are assemblages of multiple interacting species. Despite their importance, we currently 49 know little about how microbial communities form and function. However, such knowledge 50 is crucial if we want to fundamentally understand their properties and dynamics, as well as 51 control the processes that they mediate[7,8]. 52 53 Microbial communities, like all complex systems, are more than the sum of their parts: they 54 are characterized by a multitude of often complex interactions between their constituent 55 members (Figure 1). At any given time, microbes may compete for shared resources such as 56 metabolites and space, inhibit each other via the secretion of antibiotics and other toxic 57 compounds, and even kill each other upon direct cell-cell contact[9,10]. Yet, not all is bleak 58 in the microbial world: some organisms may—accidentally or actively—excrete enzymes or 59 molecules that others can use, and even commit suicide for others [11–13]. The overall sign 60 and strength of an interaction between two organisms is the net result of all such processes 61 and can be characterised as anything from competition to parasitism and mutualism[14,15]. 62 63 Interspecific interactions have a crucial role to play in microbial communities. That is, what 64 makes a community a community—rather than a random set of species—is precisely these 65 interactions, because they give rise to properties at the level of the community that we cannot 66 understand by considering each species in isolation. For example, it may not be possible to 67 predict from growing each species by itself what the joint reproductive output of a collective 68 will be, or how robust such a collective will be to external biotic and abiotic perturbations. 69 Microbial communities can also perform chemical transformations that would be impossible 70 for one individual species to achieve[16], and some communities even display complex 71 behaviours such as collective motion and electrochemical signalling, which have traditionally 72 been associated with higher organisms[17,18]. 73 74 Over the past decades, an impressive amount of thought and effort has been dedicated 75 towards obtaining an ever-more detailed and realistic picture of a wide range of different bioRxiv preprint doi: https://doi.org/10.1101/770156; this version posted September 16, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 76 77 Figure 1. Microbial communities are characterized by a multitude of often complex interactions between 78 their members. For example, three bacterial species commonly found in yoghurt cultures engage in both 79 positive and negative interactions, which are mediated by metabolic compounds and toxins[19,20]. 80 81 microbial systems. The advance of omics technologies has led to an incredible leap forward 82 in terms of available data that can be integrated to extract and analyse patterns that inform us 83 about the lives of microbes in their natural surroundings. However, if we want to arrive at a 84 more fundamental understanding of the current and future properties of microbial 85 communities, we will have to uncover general principles of how such communities will 86 typically change over time. 87 88 Since interactions are often mediated by whole suites of different chemicals, interactions may 89 significantly change in strength and even sign over ecological timescales. For example, 90 bacteria may alter the pH of their environment during growth, which may then change the 91 sign of their interactions with other species from positive to negative, or vice versa[21]. 92 Extrapolating such findings to more general principles of community dynamics is 93 challenging. Nonetheless, an increasing number of studies finds that ecological community 94 dynamics are remarkably repeatable across experimental and biological replicates, and may 95 be understood from a combination of metabolic properties of the environment and species 96 functional traits[22–24]. Less is known about how communities change over evolutionary 97 timescales, even if such changes have potentially much more far-reaching consequences bioRxiv preprint doi: https://doi.org/10.1101/770156; this version posted September 16, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 98 because they are essentially irreversible (i.e. they are the result of mutations, so the 99 community will not change back to its original state unless these mutations are reverted, or 100 species acquires additional ones). Given that interactions are the defining feature of a 101 community, we propose that what is most important in this respect, is how interspecific 102 interactions change. 103 104 Here, we review the empirical evidence that evolution is an important driver of microbial 105 community properties and dynamics on timescales that have traditionally been regarded as 106 purely ecological. Next, we briefly discuss different modelling approaches to this problem, 107 emphasizing the similarities and differences between evolutionary and ecological 108 perspectives. We then propose a simple conceptual model for the evolution of communities, 109 which we explore using simulations. Finally, we discuss experimental approaches that may 110 help to test our framework and thus improve our understanding of this fascinating process. 111 112 113 Evolution of microbial communities: empirical approaches 114 115 The question of how microbial communities evolve has been addressed empirically by 116 authors from several different fields. One approach that has
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