β-glucan is a major growth substrate for human gut bacteria related to Coprococcus eutactus

Anna M Alessi; Victoria Gray; Freda M Farquharson; Adriana  Flores-López; Sophie Shaw; David Stead; Udo Wegmann; Claire  Shearman; Mike  Gasson; Elaina SR Collie-Duguid; Harry J Flint; Petra Louis

doi:10.1111/1462-2920.14977

β-glucan is a major growth substrate for human gut bacteria related to Coprococcus eutactus

Anna M Alessi, Victoria Gray, Freda M Farquharson, Adriana Flores-López, Sophie Shaw, David Stead, Udo Wegmann, Claire Shearman, Mike Gasson, Elaina SR Collie-Duguid, Harry J Flint, Petra Louis^* (Corresponding Author)

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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Abstract

A clone encoding carboxymethylcellulase activity was isolated during functional screening of a human gut metagenomic library using Lactococcus lactis MG1363 as heterologous host. The insert carried a glycoside hydrolase family 9 (GH9) catalytic domain with sequence similarity to a gene from Coprococcus eutactus ART55/1. Genome surveys indicated a limited distribution of GH9 domains among dominant human colonic anaerobes. Genomes of C. eutactus‐related strains harboured two GH9‐encoding and four GH5‐encoding genes, but the strains did not appear to degrade cellulose. Instead, they grew well on β‐glucans and one of the strains also grew on galactomannan, galactan, glucomannan and starch. Coprococcus comes and Coprococcus catus strains did not harbour GH9 genes and were not able to grow on β‐glucans. Gene expression and proteomic analysis of C. eutactus ART55/1 grown on cellobiose, β‐glucan and lichenan revealed similar changes in expression in comparison to glucose. On β‐glucan and lichenan only, one of the four GH5 genes was strongly upregulated. Growth on glucomannan led to a transcriptional response of many genes, in particular a strong upregulation of glycoside hydrolases involved in mannan degradation. Thus, β‐glucans are a major growth substrate for species related to C. eutactus, with glucomannan and galactans alternative substrates for some strains.

Original language	English
Pages (from-to)	2150-2164
Number of pages	15
Journal	Environmental Microbiology
Volume	22
Issue number	6
Early online date	20 Mar 2020
DOIs	https://doi.org/10.1111/1462-2920.14977
Publication status	Published - 1 Jun 2020

Bibliographical note

Open Access via the Jisc Wiley Deal
Funding Information:
University of Aberdeen Rowett Institute
Institute of Food Research
Scottish Government Rural and Environment Science and Analytical Services Division

Acknowledgements
Freda M. Farquharson, Harry J. Flint and Petra Louis received financial support from the Scottish Government Rural and Environment Science and Analytical Services Division (RESAS). Anna M. Alessi received a PhD scholarship jointly funded by the Institute of Food Research (Norwich, UK, now Quadram Institute) and the Rowett Institute (University of Aberdeen, Aberdeen, UK). The authors wish to thank Gill Campbell and Pauline Young for their assistance with colony picking and screening metagenomic libraries, Brennan Martin at the Centre for Genome Enabled Biology and Medicine, University of Aberdeen, for performing the RNA sequencing, Evelyn Argo and Craig Pattinson for advice on sample preparation for proteomics work, Bekhal Kareem Sharif and Manon Le Merrer for help with growth experiments, Sylvia Duncan for the gift of acid‐swollen cellulose and for providing strains C. comes A2‐232 and SL7/1, Pat Bain for help with figure formats and Mike Peck and Bruce Pearson at the Institute for Food Research Norwich for helpful discussions.

Keywords

BUTYRATE-PRODUCING BACTERIA
RUMINOCOCCUS-CHAMPANELLENSIS
CELLULOSE DEGRADATION
ENDOGLUCANASE
MICROBIOTA
METAGENOMICS
PHYLOGENIES
PROPIONATE
SECRETION
GENOMICS

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10.1111/1462-2920.14977Licence: CC BY

Alessi_etal_EM_BGlucan_VOR
© 2020 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 License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. https://creativecommons.org/licenses/by/4.0/
Final published version, 2.09 MBLicence: CC BY

Cite this

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title = "β-glucan is a major growth substrate for human gut bacteria related to Coprococcus eutactus",

abstract = "A clone encoding carboxymethylcellulase activity was isolated during functional screening of a human gut metagenomic library using Lactococcus lactis MG1363 as heterologous host. The insert carried a glycoside hydrolase family 9 (GH9) catalytic domain with sequence similarity to a gene from Coprococcus eutactus ART55/1. Genome surveys indicated a limited distribution of GH9 domains among dominant human colonic anaerobes. Genomes of C. eutactus‐related strains harboured two GH9‐encoding and four GH5‐encoding genes, but the strains did not appear to degrade cellulose. Instead, they grew well on β‐glucans and one of the strains also grew on galactomannan, galactan, glucomannan and starch. Coprococcus comes and Coprococcus catus strains did not harbour GH9 genes and were not able to grow on β‐glucans. Gene expression and proteomic analysis of C. eutactus ART55/1 grown on cellobiose, β‐glucan and lichenan revealed similar changes in expression in comparison to glucose. On β‐glucan and lichenan only, one of the four GH5 genes was strongly upregulated. Growth on glucomannan led to a transcriptional response of many genes, in particular a strong upregulation of glycoside hydrolases involved in mannan degradation. Thus, β‐glucans are a major growth substrate for species related to C. eutactus, with glucomannan and galactans alternative substrates for some strains.",

keywords = "BUTYRATE-PRODUCING BACTERIA, RUMINOCOCCUS-CHAMPANELLENSIS, CELLULOSE DEGRADATION, ENDOGLUCANASE, MICROBIOTA, METAGENOMICS, PHYLOGENIES, PROPIONATE, SECRETION, GENOMICS",

author = "Alessi, {Anna M} and Victoria Gray and Farquharson, {Freda M} and Adriana Flores-L{\'o}pez and Sophie Shaw and David Stead and Udo Wegmann and Claire Shearman and Mike Gasson and Collie-Duguid, {Elaina SR} and Flint, {Harry J} and Petra Louis",

note = "Open Access via the Jisc Wiley Deal Funding Information: University of Aberdeen Rowett Institute Institute of Food Research Scottish Government Rural and Environment Science and Analytical Services Division Acknowledgements Freda M. Farquharson, Harry J. Flint and Petra Louis received financial support from the Scottish Government Rural and Environment Science and Analytical Services Division (RESAS). Anna M. Alessi received a PhD scholarship jointly funded by the Institute of Food Research (Norwich, UK, now Quadram Institute) and the Rowett Institute (University of Aberdeen, Aberdeen, UK). The authors wish to thank Gill Campbell and Pauline Young for their assistance with colony picking and screening metagenomic libraries, Brennan Martin at the Centre for Genome Enabled Biology and Medicine, University of Aberdeen, for performing the RNA sequencing, Evelyn Argo and Craig Pattinson for advice on sample preparation for proteomics work, Bekhal Kareem Sharif and Manon Le Merrer for help with growth experiments, Sylvia Duncan for the gift of acid‐swollen cellulose and for providing strains C. comes A2‐232 and SL7/1, Pat Bain for help with figure formats and Mike Peck and Bruce Pearson at the Institute for Food Research Norwich for helpful discussions. ",

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AU - Shaw, Sophie

AU - Stead, David

AU - Wegmann, Udo

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AU - Gasson, Mike

AU - Collie-Duguid, Elaina SR

AU - Flint, Harry J

AU - Louis, Petra

N1 - Open Access via the Jisc Wiley Deal Funding Information: University of Aberdeen Rowett Institute Institute of Food Research Scottish Government Rural and Environment Science and Analytical Services Division Acknowledgements Freda M. Farquharson, Harry J. Flint and Petra Louis received financial support from the Scottish Government Rural and Environment Science and Analytical Services Division (RESAS). Anna M. Alessi received a PhD scholarship jointly funded by the Institute of Food Research (Norwich, UK, now Quadram Institute) and the Rowett Institute (University of Aberdeen, Aberdeen, UK). The authors wish to thank Gill Campbell and Pauline Young for their assistance with colony picking and screening metagenomic libraries, Brennan Martin at the Centre for Genome Enabled Biology and Medicine, University of Aberdeen, for performing the RNA sequencing, Evelyn Argo and Craig Pattinson for advice on sample preparation for proteomics work, Bekhal Kareem Sharif and Manon Le Merrer for help with growth experiments, Sylvia Duncan for the gift of acid‐swollen cellulose and for providing strains C. comes A2‐232 and SL7/1, Pat Bain for help with figure formats and Mike Peck and Bruce Pearson at the Institute for Food Research Norwich for helpful discussions.

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KW - ENDOGLUCANASE

KW - MICROBIOTA

KW - METAGENOMICS

KW - PHYLOGENIES

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JO - Environmental Microbiology

JF - Environmental Microbiology

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ER -

β-glucan is a major growth substrate for human gut bacteria related to Coprococcus eutactus

Abstract

Bibliographical note

Keywords

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β-glucan is a major growth substrate for human gut bacteria related to Coprococcus eutactus

Abstract

Bibliographical note

Keywords

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