title: Anaerobic choline metabolism in microcompartments promotes growth and swarming of Proteus mirabilis.
abstract: Gammaproteobacteria are important gut microbes but only persist at low levels in the healthy gut. The ecology of Gammaproteobacteria in the gut environment is poorly understood. Here, we demonstrate that choline is an important growth substrate for representatives of Gammaproteobacteria. Using Proteus mirabilis as a model, we investigate the role of choline metabolism and demonstrate that the cutC gene, encoding a choline-trimethylamine lyase, is essential for choline degradation to trimethylamine by targeted mutagenesis of cutC and subsequent complementation experiments. Proteus mirabilis can rapidly utilize choline to enhance growth rate and cell yield in broth culture. Importantly, choline also enhances swarming-associated colony expansion of P. mirabilis under 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 for P. mirabilis and contributes to better understand the ecology of this bacterium in health and disease.
authors.affiliation: School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK.
authors.forename: Eleanor
authors.initials: E
authors.lastname: Jameson
authors.affiliation: School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK.
authors.forename: Tiantian
authors.initials: T
authors.lastname: Fu
authors.affiliation: School of Biosciences, University of Kent, Canterbury, Kent, CT2 7NJ, UK.
authors.forename: Ian R
authors.initials: IR
authors.lastname: Brown
authors.affiliation: College of Life and Environmental Sciences, University of Exeter, Exeter, EX4 4QD, UK.
authors.forename: Konrad
authors.initials: K
authors.lastname: Paszkiewicz
authors.affiliation: School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK.
authors.forename: Kevin J
authors.initials: KJ
authors.lastname: Purdy
authors.affiliation: School of Biosciences, University of Kent, Canterbury, Kent, CT2 7NJ, UK. S.Frank@kent.ac.uk.
authors.forename: Stefanie
authors.initials: S
authors.lastname: Frank
authors.affiliation: School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK. Y.chen.25@warwick.ac.uk.
authors.forename: Yin
authors.initials: Y
authors.lastname: Chen
mesh_terms: D000693:Anaerobiosis; D002794:Choline / Q000378:metabolism*; D008190:Lyases / Q000235:genetics; D016296:Mutagenesis; D011513:Proteus mirabilis / Q000235:genetics / Q000254:growth & development / Q000378:metabolism* / Q000648:ultrastructure
chemical_list: D008190:Lyases; D002794:Choline