Metagenomic Analysis of the Gut Microbiome of the Common Black Slug Arion ater in Search of Novel Lignocellulose Degrading Enzymes

Some eukaryotes are able to gain access to well-protected carbon sources in plant biomass by exploiting microorganisms in the environment or harbored in their digestive system. One is the land pulmonate Arion ater, which takes advantage of a gut microbial consortium that can break down the widely av...

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Main Authors: Ryan Joynson, Leighton Pritchard, Ekenakema Osemwekha, Natalie Ferry
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.02181/full
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spelling doaj-d77c4d89302e4b1193895641b96434332020-11-24T22:55:54ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-11-01810.3389/fmicb.2017.02181290624Metagenomic Analysis of the Gut Microbiome of the Common Black Slug Arion ater in Search of Novel Lignocellulose Degrading EnzymesRyan Joynson0Ryan Joynson1Leighton Pritchard2Ekenakema Osemwekha3Natalie Ferry4School of Environment and Life Science, University of Salford, Greater Manchester, United KingdomEarlham Institute, Norwich, United KingdomInformation and Computational Sciences, James Hutton Institute, Dundee, United KingdomSchool of Environment and Life Science, University of Salford, Greater Manchester, United KingdomSchool of Environment and Life Science, University of Salford, Greater Manchester, United KingdomSome eukaryotes are able to gain access to well-protected carbon sources in plant biomass by exploiting microorganisms in the environment or harbored in their digestive system. One is the land pulmonate Arion ater, which takes advantage of a gut microbial consortium that can break down the widely available, but difficult to digest, carbohydrate polymers in lignocellulose, enabling them to digest a broad range of fresh and partially degraded plant material efficiently. This ability is considered one of the major factors that have enabled A. ater to become one of the most widespread plant pest species in Western Europe and North America. Using metagenomic techniques we have characterized the bacterial diversity and functional capability of the gut microbiome of this notorious agricultural pest. Analysis of gut metagenomic community sequences identified abundant populations of known lignocellulose-degrading bacteria, along with well-characterized bacterial plant pathogens. This also revealed a repertoire of more than 3,383 carbohydrate active enzymes (CAZymes) including multiple enzymes associated with lignin degradation, demonstrating a microbial consortium capable of degradation of all components of lignocellulose. This would allow A. ater to make extensive use of plant biomass as a source of nutrients through exploitation of the enzymatic capabilities of the gut microbial consortia. From this metagenome assembly we also demonstrate the successful amplification of multiple predicted gene sequences from metagenomic DNA subjected to whole genome amplification and expression of functional proteins, facilitating the low cost acquisition and biochemical testing of the many thousands of novel genes identified in metagenomics studies. These findings demonstrate the importance of studying Gastropod microbial communities. Firstly, with respect to understanding links between feeding and evolutionary success and, secondly, as sources of novel enzymes with biotechnological potential, such as, CAZYmes that could be used in the production of biofuel.http://journal.frontiersin.org/article/10.3389/fmicb.2017.02181/fullCAZymeslignocelluloseArion aterbiofuelshotgun metagenomicswhole genome amplification
collection DOAJ
language English
format Article
sources DOAJ
author Ryan Joynson
Ryan Joynson
Leighton Pritchard
Ekenakema Osemwekha
Natalie Ferry
spellingShingle Ryan Joynson
Ryan Joynson
Leighton Pritchard
Ekenakema Osemwekha
Natalie Ferry
Metagenomic Analysis of the Gut Microbiome of the Common Black Slug Arion ater in Search of Novel Lignocellulose Degrading Enzymes
Frontiers in Microbiology
CAZymes
lignocellulose
Arion ater
biofuel
shotgun metagenomics
whole genome amplification
author_facet Ryan Joynson
Ryan Joynson
Leighton Pritchard
Ekenakema Osemwekha
Natalie Ferry
author_sort Ryan Joynson
title Metagenomic Analysis of the Gut Microbiome of the Common Black Slug Arion ater in Search of Novel Lignocellulose Degrading Enzymes
title_short Metagenomic Analysis of the Gut Microbiome of the Common Black Slug Arion ater in Search of Novel Lignocellulose Degrading Enzymes
title_full Metagenomic Analysis of the Gut Microbiome of the Common Black Slug Arion ater in Search of Novel Lignocellulose Degrading Enzymes
title_fullStr Metagenomic Analysis of the Gut Microbiome of the Common Black Slug Arion ater in Search of Novel Lignocellulose Degrading Enzymes
title_full_unstemmed Metagenomic Analysis of the Gut Microbiome of the Common Black Slug Arion ater in Search of Novel Lignocellulose Degrading Enzymes
title_sort metagenomic analysis of the gut microbiome of the common black slug arion ater in search of novel lignocellulose degrading enzymes
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2017-11-01
description Some eukaryotes are able to gain access to well-protected carbon sources in plant biomass by exploiting microorganisms in the environment or harbored in their digestive system. One is the land pulmonate Arion ater, which takes advantage of a gut microbial consortium that can break down the widely available, but difficult to digest, carbohydrate polymers in lignocellulose, enabling them to digest a broad range of fresh and partially degraded plant material efficiently. This ability is considered one of the major factors that have enabled A. ater to become one of the most widespread plant pest species in Western Europe and North America. Using metagenomic techniques we have characterized the bacterial diversity and functional capability of the gut microbiome of this notorious agricultural pest. Analysis of gut metagenomic community sequences identified abundant populations of known lignocellulose-degrading bacteria, along with well-characterized bacterial plant pathogens. This also revealed a repertoire of more than 3,383 carbohydrate active enzymes (CAZymes) including multiple enzymes associated with lignin degradation, demonstrating a microbial consortium capable of degradation of all components of lignocellulose. This would allow A. ater to make extensive use of plant biomass as a source of nutrients through exploitation of the enzymatic capabilities of the gut microbial consortia. From this metagenome assembly we also demonstrate the successful amplification of multiple predicted gene sequences from metagenomic DNA subjected to whole genome amplification and expression of functional proteins, facilitating the low cost acquisition and biochemical testing of the many thousands of novel genes identified in metagenomics studies. These findings demonstrate the importance of studying Gastropod microbial communities. Firstly, with respect to understanding links between feeding and evolutionary success and, secondly, as sources of novel enzymes with biotechnological potential, such as, CAZYmes that could be used in the production of biofuel.
topic CAZymes
lignocellulose
Arion ater
biofuel
shotgun metagenomics
whole genome amplification
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.02181/full
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