Simulations reveal challenges to artificial community selection and possible strategies for success

Xie, Li; Yuan, Alex E.; Shou, Wenying

doi:10.1371/journal.pbio.3000295

Cited by 66 publications

(143 citation statements)

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“…Experimental and theoretical studies demonstrate that artificial selection on microbial communities results in rapid functional improvement (Swenson et al, 2000a,b;Goodnight, 2000;Wade, 2016;Xie et al, 2019). This is not unexpected given that experimental manipulations ensure that communities engage directly in the process of evolution by (artificial) selection as units in their own right.…”

Section: Discussionmentioning

confidence: 99%

“…In nature, communities rarely ever qualify as units of selection in the traditional sense (Lewontin, 1970;Godfrey-Smith, 2009), because communities in nature rarely manifest heritable variance in fitness. In the laboratory however, experimenters can exogenously impose (scaffold) Darwinian-like properties on communities such that they have no choice, but to become units of selection (Wilson and Sober, 1989;Xie et al, 2019;Black et al, 2019). This typically involves placement of communities in some kind of container (pot, test-tube, flask, droplet, etc.)…”

Section: Discussionmentioning

confidence: 99%

“…Phoretic insect communities are an apparent case in point. In the laboratory, however, the experimenter can readily construct conditions that ensure communities (or any collective of cells) are units of selection in their own right (Johnson and Boerlijst, 2002;Day et al, 2011;Xie and Shou, 2018;Xie et al, 2019). A critical requirement is a birth-death process operating over a time scale longer than the doubling time of individual cells (Hammerschmidt et al, 2014;Rainey et al, 2017;Black et al, 2019).…”

Section: November 7 2019mentioning

confidence: 99%

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Eco-evolutionary dynamics of nested Darwinian populations and the emergence of community-level heredity

Doulcier

Lambert

Monte

et al. 2019

Preprint

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Interactions among microbial cells can generate new chemistries and functions, but exploitation requires establishment of communities that reliably recapitulate communitylevel phenotypes. Using mechanistic mathematical models, we show how simple manipulations to population structure can exogenously impose Darwinian-like properties on communities. Such imposition causes communities to participate directly in the process of evolution by natural selection and drives the evolution of cell-level interactions to the point where, despite underlying stochasticity, derived communities give rise to offspring communities that faithfully re-establish parental phenotype. The mechanism (developmental correction) is akin to a developmental process that arises from density dependent interactions among cells. Knowledge of ecological factors affecting evolution of developmental correction has implications for understanding the evolutionary origin of egalitarian transitions in individuality, symbioses, and for top-down engineering of microbial communities.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: November 7 2019mentioning

confidence: 99%

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Eco-evolutionary dynamics of nested Darwinian populations and the emergence of community-level heredity

Doulcier

Lambert

Monte

et al. 2019

Preprint

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“…Given that this approach does not usually assess genetic changes in each 146 of the constituent species, it is conceivable that the observed changes are mainly due to 147 ecological sorting rather than evolutionary adaptation [41,42]. However, the duration of these 148 experiments is sufficient for evolution to occur, and it has in fact been argued that continued 149 species coexistence and within-species evolution are crucial for maximally-effective 150 community selection [43]. One important advantage of this approach over methods that are 151 centred on focal species is that it explicitly tracks the dynamics of the entire community.…”

mentioning

confidence: 99%

“…One intriguing question that has received an increasing amount of interest over the past few 529 years is whether microbial communities may be regarded as coherent units, on which 530 selection can act directly [126,127]. If this were the case, we might be able to select for 531 certain desired community-level properties, such as efficiency in producing a specific 532 compound [43]. While this idea has a strong intuitive appeal, experimental results have been 533 mixed [128].…”

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confidence: 99%

Understanding the evolution of interspecies interactions in microbial communities

Gorter

Manhart

Ackermann

2019

Preprint

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20Microbial communities are complex multi-species assemblages that are characterized by a 21 multitude of interspecies interactions, which can range from mutualism to competition. The 22The next step will be to test these hypotheses experimentally and provide input for a more 38 refined version of the model in turn, thus closing the scientific cycle of models and 39 experiments. 40 control the processes that they mediate [7,8]. 51 52 Microbial communities, like all complex systems, are more than the sum of their parts: they 53 are characterized by a multitude of often complex interactions between their constituent 54 members (Figure 1). At any given time, microbes may compete for shared resources such as 55 metabolites and space, inhibit each other via the secretion of antibiotics and other toxic 56 compounds, and even kill each other upon direct cell-cell contact[9,10]. Yet, not all is bleak 57in the microbial world: some organisms may-accidentally or actively-excrete enzymes or 58 molecules that others can use, and even commit suicide for others [11][12][13]. The overall sign 59 and strength of an interaction between two organisms is the net result of all such processes 60 and can be characterised as anything from competition to parasitism and mutualism [14,15]. 61 62Interspecific interactions have a crucial role to play in microbial communities. That is, what 63 makes a community a community-rather than a random set of species-is precisely these 64 interactions, because they give rise to properties at the level of the community that we cannot 65 understand by considering each species in isolation. For example, it may not be possible to 66 predict from growing each species by itself what the joint reproductive output of a collective 67 will be, or how robust such a collective will be to external biotic and abiotic perturbations. 68Microbial communities can also perform chemical transformations that would be impossible 69 for one individual species to achieve[16], and some communities even display complex 70 behaviours such as collective motion and electrochemical signalling, which have traditionally 71 been associated with higher organisms [17,18]. 72 73Over the past decades, an impressive amount of thought and effort has been dedicated 74 towards obtaining an ever-more detailed and realistic picture of a wide range of different 75

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Guided by the principles of microbiome engineering: Accomplishments and perspectives for environmental use

Fang

Huang

et al. 2022

mLife

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Although the accomplishments of microbiome engineering highlight its significance for the targeted manipulation of microbial communities, knowledge and technical gaps still limit the applications of microbiome engineering in biotechnology, especially for environmental use. Addressing the environmental challenges of refractory pollutants and fluctuating environmental conditions requires an adequate understanding of the theoretical achievements and practical applications of microbiome engineering. Here, we review recent cutting-edge studies on microbiome engineering strategies and their classical applications in bioremediation. Moreover, a framework is summarized for combining both top-down and bottom-up approaches in microbiome engineering toward improved applications. A strategy to engineer microbiomes for environmental use, which avoids the build-up of toxic intermediates that pose a risk to human health, is suggested. We anticipate that the highlighted framework and strategy will be beneficial for engineering microbiomes to address difficult environmental challenges such as degrading multiple refractory pollutants and sustain the performance of engineered microbiomes in situ with indigenous microorganisms under fluctuating conditions.

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Simulations reveal challenges to artificial community selection and possible strategies for success

Cited by 66 publications

References 123 publications

Eco-evolutionary dynamics of nested Darwinian populations and the emergence of community-level heredity

Eco-evolutionary dynamics of nested Darwinian populations and the emergence of community-level heredity

Understanding the evolution of interspecies interactions in microbial communities

Guided by the principles of microbiome engineering: Accomplishments and perspectives for environmental use

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