The role of competition versus cooperation in microbial community coalescence

Abstract

New microbial communities often arise through the mixing of two or more separately assembled parent communities, a phenomenon that has been termed “community coalescence”. Understanding how the interaction structures of complex parent communities determine the outcomes of coalescence events is an important challenge. While recent work has begun to elucidate the role of competition in coalescence, that of cooperation, a key interaction type commonly seen in microbial communities, is still largely unknown. Here, using a general consumer-resource model, we study the combined effects of competitive and cooperative interactions on the outcomes of coalescence events. To do so, we simulate coalescence events between pairs of communities with different degrees of competition for shared carbon resources and cooperation through cross-feeding on leaked metabolic by-products (facilitation). We also study how structural and functional properties of post-coalescence communities evolve when they are subjected to repeated coalescence events. We find that in coalescence events, the less competitive and more cooperative parent communities contribute a higher proportion of species to the new community because of their superior ability to deplete resources and resist invasions. Consequently, when a community is subjected to repeated coalescence events, it gradually evolves towards being less competitive and more cooperative, as well as more speciose, robust and efficient in resource use. Encounters between microbial communities are becoming increasingly frequent as a result of anthropogenic environmental change, and there is great interest in how the coalescence of microbial communities affects environmental and human health. Our study provides new insights into the mechanisms behind microbial community coalescence, and a framework to predict outcomes based on the interaction structures of parent communities.

Top-down and bottom-up cohesiveness in microbial community coalescence

“…Keeping track of every nutrient secreted by every species in coculture and by which species they are uptaken is still a low-throughput process that is both labor intensive and expensive, but recent progress in metabolomic tools promise to help us test this hypothesis in future work. Our findings, together with previous results in different systems ( 22 ) as well as theoretical predictions ( 11 , 18 – 21 ), suggest that collective interactions of microbes with one another and with the environment should be generically expected to produce ecological coselection during community coalescence.…”

“…1 A ) and used them to inoculate eight identical habitats containing minimal media with either glutamine or citrate as the only supplied carbon source. We chose these two carbon sources because they are metabolized through different pathways in bacteria ( 31 , 32 ), and we hypothesize that communities assembled in either resource will be supported by cross-feeding networks of distinct sets of metabolites ( 27 , 28 ), thus leading to potentially variable degrees of community cohesiveness and coalescence outcomes ( 14 , 18 , 19 , 21 ). After inoculation, all communities were serially passaged for 12 transfers (84 generations), with an incubation time of 48 h and a dilution factor of 1:100.…”

“…However, and despite its clear potential importance, the role of coalescence in microbiome assembly is only beginning to be addressed and little is known about the mechanisms that govern it and its potential implications or applications ( 15 – 17 ). Early mathematical models of community–community invasions ( 11 ) as well as more recent work ( 18 – 21 ) suggest that high-order invasion effects are common during community coalescence. Communities that have a previous history of coexistence may exhibit an emergent “cohesiveness” that produces correlated invasional outcomes among species from the same community ( 12 , 22 ).…”

“…Which of these potential scenarios are typically found in nature? Previous theoretical and computational studies suggest that the answer is determined by the type and strength of the interactions of the community members with one another and with the environment ( 18 , 20 , 21 ), but addressing this question has been experimentally challenging ( 22 , 23 ).…”

Oral and Stool Microbiome Coalescence and Its Association With Antibiotic Exposure in Acute Leukemia Patients

“…Although the oral and gut microbiomes of an individual typically maintain unique compositions, there are several bacterial species that can colonize both the human mouth and intestines ( Segata et al., 2012 ; Seedorf et al., 2014 ; Schmidt et al., 2019 ). Recently, the novel theory of the process of microbial “community coalescence” has been proposed, which is defined as a new microbial community arising from the admixture of two or more separate communities ( Rillig et al., 2015 ; Lechon-Alonso et al., 2021 ). Although this terminology has been primarily applied to describe ecological community interchange in an environmental context (i.e.…”