Rare Microbial Taxa Emerge When Communities Collide: Freshwater and Marine Microbiome Responses to Experimental Seawater Intrusion

Abstract

Whole microbial communities regularly merge with one another, often in tandem with their environments, in a process called community coalescence. Such events allow us to address a central question in ecology – what processes shape community assembly. We used a reciprocal transplant and mixing experiment to directly and independently unravel the effects of environmental filtering and biotic interactions on microbiome success when freshwater and marine communities coalesce. The brackish treatment and community mixing resulted in strong convergence of microbiome structure and function toward the marine. Brackish exposure imposed a 96% taxa loss from freshwater and 66% loss from marine microbiomes, which was somewhat counterbalanced by the emergence of tolerant rare taxa. Community mixing further resulted in 29% and 49% loss from biotic interactions between freshwater and marine microbiomes, offset somewhat by mutualistically-assisted rare microbial taxa. Our study emphasizes the importance of the rare biosphere as a critical component of community resilience.

Community coalescence: an eco-evolutionary perspective

“…The simplest coalescence outcomes would be one community asymmetrically dominating if a large proportion of its constituent species' populations are better adapted to the abiotic environment, and hence monopolize resources faster than the ecologically equivalent populations within other communities [13,26]. Recent theory has shown that more diverse communities are more likely to asymmetrically dominate because they have a higher chance of containing better adapted populations (selection effects) [42]; a result consistent with previous empirical work [17,43]. However, this simple prediction does not take into account structural differences between communities' species interaction networks.…”

“…First, the 'resident advantage' outlined in §2 as the experimental studies aforementioned in this section coalesced communities into a common garden environment [7,15,54]. When coalescence occurs as invasion, the nonresident community is likely to be less successful as the niches present are occupied and potentially different from that which species are adapted [17,25,26]. Experimentally, local adaptation to the environment gave resident bacterioplankton communities a competitive advantage, and naive communities a disadvantage, in coalescence [55,56].…”

Effects of diversity and coalescence of species assemblages on ecosystem function at the margins of an environmental shift

“…3), it is unlikely that the increase in observed bacterial richness is due to mixing of species pools via the mixed treatments. Instead it is likely that rare taxa, which we didn't detect at the beginning, become dominant in intermediate salinities (Rocca et al, 2019) and that there was higher immigration from natural sources to freshwater treatments than other treatments. We do, in fact, expect passive dispersal via wind (Nemergut et al, 2013).…”

Gene Transmission in the One Health Microbiosphere and the Channels of Antimicrobial Resistance

“…Reduction in alpha diversity could be expected to reduce the possibility of asymmetric dispersion of a variety of rare organisms in neighboring habitats (reduction in beta diversity). However, the collision of microbiotas creates new configurations in which rare taxa could emerge (Rocca et al, 2018(Rocca et al, , 2019. The application of zeta diversity metrics (measuring the degree of overlap in the type of taxa present between a set microbiotas) will be most useful to illustrate the spatial structure of multispecies distributions in various environments, and therefore the dimensions of microbiome merging (Hui and McGeoch, 2014).…”

“…The dynamics of microbiome merging are insufficiently understood (Roughgarden et al, 2018). New observations, suggesting the modular structure of microbiota (Earle et al, 2015;Tropini et al, 2017), indicate the possibility of a "recombinational merging" within and between microbiomes, eventually resulting in emerging taxa and emerging communities (Rocca et al, 2018(Rocca et al, , 2019. In the soil, specific microbial aggregate communities can be considered "microbial villages, " periodically connected through wetting events, where soil moisture is increased as a result of rainfall infiltration, allowing for the transfer of bacterial organisms and genetic material (Wilpiszeski et al, 2019).…”