A Single Community Dominates Structure and Function of a Mixture of Multiple Methanogenic Communities

Abstract

The ecology of microbes frequently involves the mixing of entire communities (community coalescence), for example, flooding events, host excretion, and soil tillage [1, 2], yet the consequences of this process for community structure and function are poorly understood [3-7]. Recent theory suggests that a community, due to coevolution between constituent species, may act as a partially cohesive unit [8-11], resulting in one community dominating after community coalescence. This dominant community is predicted to be the one that uses resources most efficiently when grown in isolation [11]. We experimentally tested these predictions using methanogenic communities, for which efficient resource use, quantified by methane production, requires coevolved cross-feeding interactions between species [12]. After propagation in laboratory-scale anaerobic digesters, community composition (determined from 16S rRNA sequencing) and methane production of mixtures of communities closely resembled that of the single most productive community grown in isolation. Analysis of each community's contribution toward the final mixture suggests that certain combinations of taxa within a community might be co-selected as a result of coevolved interactions. As a corollary of these findings, we also show that methane production increased with the number of inoculated communities. These findings are relevant to the understanding of the ecological dynamics of natural microbial communities, as well as demonstrating a simple method of predictably enhancing microbial community function in biotechnology, health, and agriculture [13].

A shared coevolutionary history does not alter the outcome of coalescence in experimental populations of Pseudomonas fluorescens

“…Despite its ubiquity, research into the mechanisms that govern, and the outcome of, community coalescence and multi‐species invasions is only beginning to be addressed (Lu, Sanchez‐Gorostiaga, Tikhonov, & Sanchez, ; Rillig et al., ; Rivett et al., ; Tikhonov, ). Communities arising from coalescence can be chimeric (a combination of species from both communities; Livingston, Jiang, Fox, & Leibold, ; Rummens, De Meester, & Souffreau, ) or asymmetric (dominance of a singular community; Freilich et al., ; Gilpin, ; Guo, Harstall, Louie, Veldhuyzen Van Zanten, & Dieleman, ; Livingston et al., ; Ridaura et al., ; Rillig et al., ; Sierocinski et al., ; Vermeij, ). Understanding the ecological and evolutionary mechanisms that underpin the outcome of community coalescence is critical for environmental (LaRue, Chambers, & Emery, ), medical (He, McLean, Guo, Lux, & Shi, ; Lloyd‐Price, Abu‐Ali, & Huttenhower, ) and biotechnological (Rillig, Tsang, & Roy, ; Sierocinski et al., ) research.…”

“…Niche-packed, more functionally diverse, communities can be more resistant to invasion through having fewer vacant niches that invaders can occupy (Elton, 1958;Hodgson, Rainey, & Buckling, 2002;Levine & D'Antonio, 1999). Theory suggests that the presence of other community members, within nichepacked communities, can enhance the success of a species' population (Tikhonov, 2016): a process termed "ecological co-selection" (Lu et al, 2018;Sierocinski et al, 2017). For example, when methanogenic communities are coalesced in bioreactors, the subsequent mixture is dominated by the most productive community (Sierocinski et al, 2017).…”

“…Theory suggests that the presence of other community members, within nichepacked communities, can enhance the success of a species' population (Tikhonov, 2016): a process termed "ecological co-selection" (Lu et al, 2018;Sierocinski et al, 2017). For example, when methanogenic communities are coalesced in bioreactors, the subsequent mixture is dominated by the most productive community (Sierocinski et al, 2017). In addition, invasion experiments on natural isolates demonstrate that the presence of other community members aids recruitment of species into a coalesced community (Lu et al, 2018).…”

Soil biodiversity and soil erosion: It is time to get married

“…Consequently, erosion has a direct impact on soil population dynamics. Furthermore, loss of nutrients associated with soil runoff may also lead to population fluctuations, as it modifies the energy sources accessible to the system (Sierocinski et al, ). All these aspects come under the recently introduced concept of “community coalescence” (Rillig et al, ).…”

Next‐generation experiments linking community structure and ecosystem functioning

“…Coalescense. An alternative that does not require isolation of pure cultures is to conduct community coalescense experiments, which compare functioning of communities on their own with functioning of communities that are mixed ('coalesced') (Rillig et al, 2015;Sierocinski et al, 2017). Community coalescence alters community structure, allowing investigations of whether the coalesced community deviates from levels of functioning that are expected from the constituent communities.…”