Tracking transcript abundance changes of D. vulgaris co-cultures with M. maripaludis in fluctuating resource environment

Managing tradeoffs through gene regulation is believed to maintain resilience of a microbial community in a fluctuating resource environment. To investigate this hypothesis we imposed a fluctuating environment that required the sulfate-reducing generalist Desulfovibrio vulgaris to manage tradeoffs associated with 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. Most cultures collapsed within 3-7 shifts with only a few collapsing later. 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. The microbial community collapse was rescued by a single regulatory mutation that could then potentially serve as a stepping stone for further adaptive evolution in a variable resource environment. Co-culture strains of M. maripaludis wild type and either wild type or DVU0744::Tn5 mutant of D. vulgaris strains were grown anaerobically in replicates. Samples were transitioned between syntrophic and sulfate respiratory growth conditions at early log phases.