Anaerobic choline metabolism in microcompartments promotes growth and swarming ofProteus mirabilis

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Abstract

Gammaproteobacteriaare important gut microbes but only persist at low levels in the healthy gut. The ecology ofGammaproteobacteriain the gut environment is poorly understood. Here, we demonstrate that choline is an important growth substrate for representatives ofGammaproteobacteria. UsingProteus mirabilisas a model, we investigate the role of choline metabolism and demonstrate that thecutCgene, encoding a choline-trimethylamine lyase, is essential for choline degradation to trimethylamine by targeted mutagenesis ofcutCand subsequent complementation experiments.Proteus mirabiliscan rapidly utilize choline to enhance growth rate and cell yield in broth culture. Importantly, choline also enhances swarming-associated colony expansion ofP. mirabilisunder anaerobic conditions on a solid surface. Comparative transcriptomics demonstrated that choline not only induces choline-trimethylamine lyase but also genes encoding shell proteins for the formation of bacterial microcompartments. Subsequent analyses by transmission electron microscopy confirmed the presence of such novel microcompartments in cells cultivated in liquid broth and hyper-flagellated swarmer cells from solid medium. Together, our study reveals choline metabolism as an adaptation strategy forP. mirabilisand contributes to better understand the ecology of this bacterium in health and disease.

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