Robustness of a model microbial community emerges from population structure among single cells of a clonal population

Abstract

Microbial populations can withstand, overcome and persist in the face of environmental fluctuation. Previously, we demonstrated how conditional gene regulation in a fluctuating environment drives dilution of condition-specific transcripts, causing a population of Desulfovibrio vulgaris Hildenborough (DvH) to collapse after repeatedly transitioning from sulfate respiration to syntrophic conditions with the methanogen Methanococcus maripaludis. Failure of the DvH to successfully transition contributed to the collapse of this model community. We investigated the mechanistic basis for loss of robustness by examining whether conditional gene regulation altered heterogeneity in gene expression across individual DvH cells. We discovered that robustness of a microbial population across environmental transitions was attributable to the retention of cells in two states that exhibited different condition-specific gene expression patterns. In our experiments, a population with disrupted conditional regulation successfully alternated between cell states. Meanwhile, a population with intact conditional regulation successfully switched between cell states initially, but collapsed after repeated transitions, possibly due to the high energy requirements of regulation. These results demonstrate that the survival of this entire model microbial community is dependent on the regulatory system's influence on the distribution of distinct cell states among individual cells within a clonal population.

AnEscherichia colinitrogen starvation response is important for mutualistic coexistence withRhodopseudomonas palustris

“…One important resilience factor is the activation of regulatory networks that allow for microbes to quickly respond to environmental perturbations. Whereas flexible gene expression is useful for an individual microbe’s survival, excessive flexibility can sometimes lead to community collapse between mutualists in a fluctuating environment (30, 31). In the coculture of D. vulgaris and M. maripaludis , alternating between coculture and monoculture conditions, which require different metabolic lifestyles, resulted in community collapse (30, 31).…”

“…Surprisingly, community collapse could be avoided by mutations that disrupted the D. vulgaris regulatory response needed to adapt cells for optimal growth rates in monoculture (30). Disruption of this regulatory response resulted in a heterogeneous D. vulgaris population, ensuring that a subpopulation would be primed for immediate mutualistic growth upon transition between growth conditions (31). In our system, the E. coli nitrogen starvation regulatory network was specifically activated by coculturing with R. palustris and was important for coculture stability.…”

Systems biology approaches towards predictive microbial ecology

“…There have been multiple efforts to build such synthetic communities with simple interactions that result in predictive dynamical behaviour ranging from predation, to competition and cooperation (Grosskopf & Soyer, ). Uncovering the mechanistic underpinnings of resilience of microbial communities (Turkarslan et al, ; Thompson et al, ; Valenzuela et al, ) will facilitate more accurate prediction of their response and adaptability to novel environments (López García de Lomana et al, ). In the future, we foresee these models as useful tools to perturb microbial communities in the field such that metabolic sources and sinks are manipulated.…”

Synergistic epistasis enhances cooperativity of mutualistic interspecies interactions

“…Mm (87 from EPD-03, and 72 from EPD-09) to reconstruct lineages of both organisms within each 32 EPD (( Thompson et al, 2017) and Methods, Supplementary Table S2) of EPDs, single cell sequencing, and sequencing of clonal isolates, we reconstructed the lineage 14…”