Abstract
Microbes form multispecies communities that play essential roles in our environment and health. Not surprisingly, there is an increasing need for understanding if certain invader species will modify a given microbial community, producing either a desired or undesired change in the observed collection of resident species. However, the complex interactions that species can establish between each other and the diverse external factors underlying their dynamics have made constructing such understanding context-specific. Here we integrate tractable theoretical systems with tractable experimental systems to find general conditions under which non-resident species can change the collection of resident communities—game-changing species. We show that non-resident colonizers are more likely to be game-changers than transients, whereas game-changers are more likely to suppress than to promote resident species. Importantly, we find general heuristic rules for game-changers under controlled environments by integrating mutual invasibility theory with in vitro experimental systems, and general heuristic rules under changing environments by integrating structuralist theory with in vivo experimental systems. Despite the strong context-dependency of microbial communities, our work shows that under an appropriate integration of tractable theoretical and experimental systems, it is possible to unveil regularities that can then be potentially extended to understand the behavior of complex natural communities.
Highlights
Microbes form multispecies communities that play essential roles in maintaining our environment and health, from regulating natural resources and balancing climatic factors, to stimulating our immune system and protecting us from pathogens.[1,2,3,4]. These microbial communities can be modified by nonresident microbes, producing desired or undesired changes in the observed collection of resident species,[4,5] For example, in the human gut microbiota, non-resident species can modify the resident community leading to changes associated with chronic gastrointestinal diseases,[6] or they can produce changes that cure their hosts of recurrent infections,[7,8] via interventions like probiotic cocktails or microbiota transplants, there is a growing interest in regulating microbial communities by promoting or avoiding the introduction of colonizing and transient non-resident species.[9,10,11,12]
While tractable theoretical systems have a long tradition in microbial ecology,[26,27,28] it remains unclear which of these theoretical and experimental systems can be integrated to answer how and when it is expected that a non-resident species modify a given resident community
As an alternative potential generalization, we introduce a second heuristic rule based on structuralist theory,[32,40,41] Across many areas of biology, the structuralist view has provided a systematic and probabilistic platform for understanding the diversity that we observe in nature,[31,42,43] In ecology, structuralist theory assumes that the probability of observing a community is based on the match between the internal constraints established by species interactions within a community and the changing external conditions.[32,44,45]
Summary
Explaining and predicting if a non-resident species will modify or not a given microbial community has become a contextspecific problem.[13,14,15,16,17] These challenges originate from the intricate interactions that species can establish between each other,[18,19,20] together with the diverse external conditions underlying the dynamics of microbial communities.[21,22,23,24] Importantly, synthetic (microbial) ecology has emerged as a promising framework to formalize model systems and address the challenges above by either systematically modifying the collection of species, altering abiotic conditions, or using genome-based technologies.[25,26,27] In particular, it has been suggested that the appropriate integration of tractable mathematical and experimental systems can provide a general system-level causative knowledge about the dynamics of entire microbial communities (not just single species—the realm of synthetic biology).[26,27] That is, tractable theoretical models can allow us to understand the possible solutions of a system and build predictions that can be corroborated and replicated using tractable experimental systems. While tractable theoretical systems have a long tradition in microbial ecology,[26,27,28] it remains unclear which of these theoretical and experimental systems can be integrated to answer how and when it is expected that a non-resident species modify a given resident community
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