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Anaerobic choline metabolism in microcompartments promotes growth and swarming of P roteus mirabilis

Gammaproteobacteria are important gut microbes but only persist at low levels in the healthy gut. The ecology of G ammaproteobacteria in the gut environment is poorly understood. Here, we demonstrate that choline is an important growth substrate for representatives of G ammaproteobacteria. Using P r...

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Autores principales: Jameson, Eleanor, Fu, Tiantian, Brown, Ian R., Paszkiewicz, Konrad, Purdy, Kevin J., Frank, Stefanie, Chen, Yin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5026066/
https://www.ncbi.nlm.nih.gov/pubmed/26404097
http://dx.doi.org/10.1111/1462-2920.13059
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author Jameson, Eleanor
Fu, Tiantian
Brown, Ian R.
Paszkiewicz, Konrad
Purdy, Kevin J.
Frank, Stefanie
Chen, Yin
author_facet Jameson, Eleanor
Fu, Tiantian
Brown, Ian R.
Paszkiewicz, Konrad
Purdy, Kevin J.
Frank, Stefanie
Chen, Yin
author_sort Jameson, Eleanor
collection PubMed
description Gammaproteobacteria are important gut microbes but only persist at low levels in the healthy gut. The ecology of G ammaproteobacteria in the gut environment is poorly understood. Here, we demonstrate that choline is an important growth substrate for representatives of G ammaproteobacteria. Using P roteus mirabilis as a model, we investigate the role of choline metabolism and demonstrate that the cut C gene, encoding a choline‐trimethylamine lyase, is essential for choline degradation to trimethylamine by targeted mutagenesis of cut C and subsequent complementation experiments. P roteus 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.
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spelling pubmed-50260662016-10-03 Anaerobic choline metabolism in microcompartments promotes growth and swarming of P roteus mirabilis Jameson, Eleanor Fu, Tiantian Brown, Ian R. Paszkiewicz, Konrad Purdy, Kevin J. Frank, Stefanie Chen, Yin Environ Microbiol Research Articles Gammaproteobacteria are important gut microbes but only persist at low levels in the healthy gut. The ecology of G ammaproteobacteria in the gut environment is poorly understood. Here, we demonstrate that choline is an important growth substrate for representatives of G ammaproteobacteria. Using P roteus mirabilis as a model, we investigate the role of choline metabolism and demonstrate that the cut C gene, encoding a choline‐trimethylamine lyase, is essential for choline degradation to trimethylamine by targeted mutagenesis of cut C and subsequent complementation experiments. P roteus 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. John Wiley and Sons Inc. 2015-11-03 2016-09 /pmc/articles/PMC5026066/ /pubmed/26404097 http://dx.doi.org/10.1111/1462-2920.13059 Text en © 2015 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/3.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Jameson, Eleanor
Fu, Tiantian
Brown, Ian R.
Paszkiewicz, Konrad
Purdy, Kevin J.
Frank, Stefanie
Chen, Yin
Anaerobic choline metabolism in microcompartments promotes growth and swarming of P roteus mirabilis
title Anaerobic choline metabolism in microcompartments promotes growth and swarming of P roteus mirabilis
title_full Anaerobic choline metabolism in microcompartments promotes growth and swarming of P roteus mirabilis
title_fullStr Anaerobic choline metabolism in microcompartments promotes growth and swarming of P roteus mirabilis
title_full_unstemmed Anaerobic choline metabolism in microcompartments promotes growth and swarming of P roteus mirabilis
title_short Anaerobic choline metabolism in microcompartments promotes growth and swarming of P roteus mirabilis
title_sort anaerobic choline metabolism in microcompartments promotes growth and swarming of p roteus mirabilis
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5026066/
https://www.ncbi.nlm.nih.gov/pubmed/26404097
http://dx.doi.org/10.1111/1462-2920.13059
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