Cargando…

The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist

Fibrobacter succinogenes is an important member of the rumen microbial community that converts plant biomass into nutrients usable by its host. This bacterium, which is also one of only two cultivated species in its phylum, is an efficient and prolific degrader of cellulose. Specifically, it has a p...

Descripción completa

Detalles Bibliográficos
Autores principales: Suen, Garret, Weimer, Paul J., Stevenson, David M., Aylward, Frank O., Boyum, Julie, Deneke, Jan, Drinkwater, Colleen, Ivanova, Natalia N., Mikhailova, Natalia, Chertkov, Olga, Goodwin, Lynne A., Currie, Cameron R., Mead, David, Brumm, Phillip J.
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3079729/
https://www.ncbi.nlm.nih.gov/pubmed/21526192
http://dx.doi.org/10.1371/journal.pone.0018814
_version_ 1782202056085340160
author Suen, Garret
Weimer, Paul J.
Stevenson, David M.
Aylward, Frank O.
Boyum, Julie
Deneke, Jan
Drinkwater, Colleen
Ivanova, Natalia N.
Mikhailova, Natalia
Chertkov, Olga
Goodwin, Lynne A.
Currie, Cameron R.
Mead, David
Brumm, Phillip J.
author_facet Suen, Garret
Weimer, Paul J.
Stevenson, David M.
Aylward, Frank O.
Boyum, Julie
Deneke, Jan
Drinkwater, Colleen
Ivanova, Natalia N.
Mikhailova, Natalia
Chertkov, Olga
Goodwin, Lynne A.
Currie, Cameron R.
Mead, David
Brumm, Phillip J.
author_sort Suen, Garret
collection PubMed
description Fibrobacter succinogenes is an important member of the rumen microbial community that converts plant biomass into nutrients usable by its host. This bacterium, which is also one of only two cultivated species in its phylum, is an efficient and prolific degrader of cellulose. Specifically, it has a particularly high activity against crystalline cellulose that requires close physical contact with this substrate. However, unlike other known cellulolytic microbes, it does not degrade cellulose using a cellulosome or by producing high extracellular titers of cellulase enzymes. To better understand the biology of F. succinogenes, we sequenced the genome of the type strain S85 to completion. A total of 3,085 open reading frames were predicted from its 3.84 Mbp genome. Analysis of sequences predicted to encode for carbohydrate-degrading enzymes revealed an unusually high number of genes that were classified into 49 different families of glycoside hydrolases, carbohydrate binding modules (CBMs), carbohydrate esterases, and polysaccharide lyases. Of the 31 identified cellulases, none contain CBMs in families 1, 2, and 3, typically associated with crystalline cellulose degradation. Polysaccharide hydrolysis and utilization assays showed that F. succinogenes was able to hydrolyze a number of polysaccharides, but could only utilize the hydrolytic products of cellulose. This suggests that F. succinogenes uses its array of hemicellulose-degrading enzymes to remove hemicelluloses to gain access to cellulose. This is reflected in its genome, as F. succinogenes lacks many of the genes necessary to transport and metabolize the hydrolytic products of non-cellulose polysaccharides. The F. succinogenes genome reveals a bacterium that specializes in cellulose as its sole energy source, and provides insight into a novel strategy for cellulose degradation.
format Text
id pubmed-3079729
institution National Center for Biotechnology Information
language English
publishDate 2011
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-30797292011-04-27 The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist Suen, Garret Weimer, Paul J. Stevenson, David M. Aylward, Frank O. Boyum, Julie Deneke, Jan Drinkwater, Colleen Ivanova, Natalia N. Mikhailova, Natalia Chertkov, Olga Goodwin, Lynne A. Currie, Cameron R. Mead, David Brumm, Phillip J. PLoS One Research Article Fibrobacter succinogenes is an important member of the rumen microbial community that converts plant biomass into nutrients usable by its host. This bacterium, which is also one of only two cultivated species in its phylum, is an efficient and prolific degrader of cellulose. Specifically, it has a particularly high activity against crystalline cellulose that requires close physical contact with this substrate. However, unlike other known cellulolytic microbes, it does not degrade cellulose using a cellulosome or by producing high extracellular titers of cellulase enzymes. To better understand the biology of F. succinogenes, we sequenced the genome of the type strain S85 to completion. A total of 3,085 open reading frames were predicted from its 3.84 Mbp genome. Analysis of sequences predicted to encode for carbohydrate-degrading enzymes revealed an unusually high number of genes that were classified into 49 different families of glycoside hydrolases, carbohydrate binding modules (CBMs), carbohydrate esterases, and polysaccharide lyases. Of the 31 identified cellulases, none contain CBMs in families 1, 2, and 3, typically associated with crystalline cellulose degradation. Polysaccharide hydrolysis and utilization assays showed that F. succinogenes was able to hydrolyze a number of polysaccharides, but could only utilize the hydrolytic products of cellulose. This suggests that F. succinogenes uses its array of hemicellulose-degrading enzymes to remove hemicelluloses to gain access to cellulose. This is reflected in its genome, as F. succinogenes lacks many of the genes necessary to transport and metabolize the hydrolytic products of non-cellulose polysaccharides. The F. succinogenes genome reveals a bacterium that specializes in cellulose as its sole energy source, and provides insight into a novel strategy for cellulose degradation. Public Library of Science 2011-04-19 /pmc/articles/PMC3079729/ /pubmed/21526192 http://dx.doi.org/10.1371/journal.pone.0018814 Text en This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. https://creativecommons.org/publicdomain/zero/1.0/ This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
spellingShingle Research Article
Suen, Garret
Weimer, Paul J.
Stevenson, David M.
Aylward, Frank O.
Boyum, Julie
Deneke, Jan
Drinkwater, Colleen
Ivanova, Natalia N.
Mikhailova, Natalia
Chertkov, Olga
Goodwin, Lynne A.
Currie, Cameron R.
Mead, David
Brumm, Phillip J.
The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist
title The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist
title_full The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist
title_fullStr The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist
title_full_unstemmed The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist
title_short The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist
title_sort complete genome sequence of fibrobacter succinogenes s85 reveals a cellulolytic and metabolic specialist
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3079729/
https://www.ncbi.nlm.nih.gov/pubmed/21526192
http://dx.doi.org/10.1371/journal.pone.0018814
work_keys_str_mv AT suengarret thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT weimerpaulj thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT stevensondavidm thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT aylwardfranko thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT boyumjulie thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT denekejan thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT drinkwatercolleen thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT ivanovanatalian thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT mikhailovanatalia thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT chertkovolga thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT goodwinlynnea thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT curriecameronr thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT meaddavid thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT brummphillipj thecompletegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT suengarret completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT weimerpaulj completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT stevensondavidm completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT aylwardfranko completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT boyumjulie completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT denekejan completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT drinkwatercolleen completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT ivanovanatalian completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT mikhailovanatalia completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT chertkovolga completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT goodwinlynnea completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT curriecameronr completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT meaddavid completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist
AT brummphillipj completegenomesequenceoffibrobactersuccinogeness85revealsacellulolyticandmetabolicspecialist