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.人们认为，通过基因调控协调代谢权衡，可维持波动资源环境中微生物群落的抗逆性。为验证该假说，我们构建了波动环境体系，使硫酸盐还原广适性普通脱硫弧菌（Desulfovibrio vulgaris）需协调两类生态相关的反复环境转变间的代谢权衡：一是维持代谢独立性（具备活跃的硫酸盐呼吸能力），二是转向代谢特化，与耗氢马氏甲烷球菌（Methanococcus maripaludis）形成互利共生关系。令人意外的是，每次环境扰动后，该微生物群落恢复符合环境需求的生理状态的能力逐渐下降。多数共培养体系在3-7次环境转变后崩溃，仅少数延迟崩溃。我们证实，群落崩溃源于条件性基因调控：该调控机制导致关键转录本与蛋白质的胞内丰度急剧下降，使得在波动环境中恢复功能所需的调控能量负担显著增加。仅需一次调控基因突变即可挽救该微生物群落的崩溃，该突变或可作为后续在可变资源环境中发生适应性进化的基础。我们以两种组合开展厌氧重复共培养：分别为马氏甲烷球菌（Methanococcus maripaludis）野生型与普通脱硫弧菌（Desulfovibrio vulgaris）野生型，以及马氏甲烷球菌野生型与普通脱硫弧菌DVU0744::Tn5突变株。在菌体生长至对数早期时，将共培养样本在互营生长与硫酸盐呼吸生长两种条件之间切换。