Mechanism for microbial population collapse in a fluctuating resource environment

Abstract

Managing trade‐offs through gene regulation is believed to confer resilience to a microbial community in a fluctuating resource environment. To investigate this hypothesis, we imposed a fluctuating environment that required the sulfate‐reducer Desulfovibrio vulgaris to undergo repeated ecologically relevant shifts between retaining metabolic independence (active capacity for sulfate respiration) and becoming metabolically specialized to a mutualistic association with the hydrogen‐consuming Methanococcus maripaludis. Strikingly, the microbial community became progressively less proficient at restoring the environmentally relevant physiological state after each perturbation and most cultures collapsed within 3–7 shifts. Counterintuitively, the collapse phenomenon was prevented by a single regulatory mutation. We have characterized the mechanism for collapse by conducting RNA‐seq analysis, proteomics, microcalorimetry, and single‐cell transcriptome analysis. We demonstrate that the collapse was caused by conditional gene regulation, which drove precipitous decline in intracellular abundance of essential transcripts and proteins, imposing greater energetic burden of regulation to restore function in a fluctuating environment.

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

“…In light of these observations, in a previous study we investigated whether conditional regulation contributes to robustness of a model microbial population growing under variable conditions in contrast to the stable conditions noted above. One of the DvH regulatory genes that accumulated mutations during evolution in syntrophy (DVU0744 – a sigma‐54 family transcription factor), was identified as a potential novel transcriptional regulator of SR using a network model of gene expression under a range of conditions and a DVU0744 transposon insertion mutant was generated (Turkarslan et al ., ). The growth rate of the DVU0744::Tn5 mutant was reduced relative to wild type under conditions of excess sulfate.…”

“…We found that all replicates of the wild type DvH co‐culture were unable to persist with repeated transfer between these growth states, some collapsing after as few as 3 SR/ST transitions. Remarkably, all replicates of a co‐culture with DvH DVU0744::Tn5 persisted across the same transitions without collapse (Turkarslan et al ., ). A series of additional measurements were used to explore the mechanism underlying this collapse in wild type and persistence in the mutant.…”

“…Global proteomics and initial analysis of single cell gene expression reflected model predictions, displaying decreased, or ‘diluted’, protein and transcript abundance in wild type cells after repeated transitions. In addition, the amount of heat production measured through microcalorimetry was much higher for wild type than the mutant, suggesting that conditional regulation imposed a greater energetic burden on cells during a fluctuating resource environment, leading to depletion in abundance of condition‐specific transcripts and proteins and collapse (Turkarslan et al ., ).…”

“…The purpose of the present study was to further investigate whether collapse of the wild type DvH population during repetitive resource fluctuations was a consequence of altered population structure with regard to heterogeneity in gene expression between single cells, beyond simply diluted transcript abundance noted in Turkarslan et al . (). Technological advances have made it possible to examine gene expression in microorganisms at the single cell level and have uncovered stochastic processes, heterogeneity among single cells and relationships between mRNA and protein abundance (Blake et al ., ; Cai et al ., ; Taniguchi et al ., ).…”

Evolution on the bright side of life: microorganisms and the evolution of mutualism

“…In the first 300 generations of evolution of the syntrophy I study, changes in both Desulfovibrio vulgaris and Methanococcus maripaludis contributed to substantial increases in the number of cells produced from a fixed amount of a single limiting resource and resulted in substantial increases in growth of the community . By 1000 generations, the communities grew about three times faster than the ancestor, a change that was correlated in D. vulgaris with loss of its ability to respire sulfate, a trait that has a substantial impact on survival outside syntrophy and may impede performance in syntrophy …”