Functional metagenomics unveils a multifunctional glycosyl hydrolase from the family 43 catalysing the breakdown of plant polymers in the calf rumen.

2.50
HDL Handle:
http://hdl.handle.net/10033/246443
Title:
Functional metagenomics unveils a multifunctional glycosyl hydrolase from the family 43 catalysing the breakdown of plant polymers in the calf rumen.
Authors:
Ferrer, Manuel; Ghazi, Azam; Beloqui, Ana; Vieites, José María; López-Cortés, Nieves; Marín-Navarro, Julia; Nechitaylo, Taras Y; Guazzaroni, María-Eugenia; Polaina, Julio; Waliczek, Agnes; Chernikova, Tatyana N; Reva, Oleg N; Golyshina, Olga V; Golyshin, Peter N
Abstract:
Microbial communities from cow rumen are known for their ability to degrade diverse plant polymers at high rates. In this work, we identified 15 hydrolases through an activity-centred metagenome analysis of a fibre-adherent microbial community from dairy cow rumen. Among them, 7 glycosyl hydrolases (GHs) and 1 feruloyl esterase were successfully cloned, expressed, purified and characterised. The most striking result was a protein of GH family 43 (GHF43), hereinafter designated as R_09-02, which had characteristics very distinct from the other proteins in this family with mono-functional β-xylosidase, α-xylanase, α-L-arabinase and α-L-arabinofuranosidase activities. R_09-02 is the first multifunctional enzyme to exhibit β-1,4 xylosidase, α-1,5 arabinofur(pyr)anosidase, β-1,4 lactase, α-1,6 raffinase, α-1,6 stachyase, β-galactosidase and α-1,4 glucosidase activities. The R_09-02 protein appears to originate from the chromosome of a member of Clostridia, a class of phylum Firmicutes, members of which are highly abundant in ruminal environment. The evolution of R_09-02 is suggested to be driven from the xylose- and arabinose-specific activities, typical for GHF43 members, toward a broader specificity to the glucose- and galactose-containing components of lignocellulose. The apparent capability of enzymes from the GHF43 family to utilise xylose-, arabinose-, glucose- and galactose-containing oligosaccharides has thus far been neglected by, or could not be predicted from, genome and metagenome sequencing data analyses. Taking into account the abundance of GHF43-encoding gene sequences in the rumen (up to 7% of all GH-genes) and the multifunctional phenotype herein described, our findings suggest that the ecological role of this GH family in the digestion of ligno-cellulosic matter should be significantly reconsidered.
Affiliation:
CSIC, Institute of Catalysis, Madrid, Spain. mferrer@icp.csic.es
Citation:
Functional metagenomics unveils a multifunctional glycosyl hydrolase from the family 43 catalysing the breakdown of plant polymers in the calf rumen. 2012, 7 (6):e38134 PLoS ONE
Journal:
PloS one
Issue Date:
2012
URI:
http://hdl.handle.net/10033/246443
DOI:
10.1371/journal.pone.0038134
PubMed ID:
22761666
Type:
Article
Language:
en
ISSN:
1932-6203
Appears in Collections:
Publications of RG Environmental Microbiology (UMW)

Full metadata record

DC FieldValueLanguage
dc.contributor.authorFerrer, Manuelen_GB
dc.contributor.authorGhazi, Azamen_GB
dc.contributor.authorBeloqui, Anaen_GB
dc.contributor.authorVieites, José Maríaen_GB
dc.contributor.authorLópez-Cortés, Nievesen_GB
dc.contributor.authorMarín-Navarro, Juliaen_GB
dc.contributor.authorNechitaylo, Taras Yen_GB
dc.contributor.authorGuazzaroni, María-Eugeniaen_GB
dc.contributor.authorPolaina, Julioen_GB
dc.contributor.authorWaliczek, Agnesen_GB
dc.contributor.authorChernikova, Tatyana Nen_GB
dc.contributor.authorReva, Oleg Nen_GB
dc.contributor.authorGolyshina, Olga Ven_GB
dc.contributor.authorGolyshin, Peter Nen_GB
dc.date.accessioned2012-10-01T14:15:48Z-
dc.date.available2012-10-01T14:15:48Z-
dc.date.issued2012-
dc.identifier.citationFunctional metagenomics unveils a multifunctional glycosyl hydrolase from the family 43 catalysing the breakdown of plant polymers in the calf rumen. 2012, 7 (6):e38134 PLoS ONEen_GB
dc.identifier.issn1932-6203-
dc.identifier.pmid22761666-
dc.identifier.doi10.1371/journal.pone.0038134-
dc.identifier.urihttp://hdl.handle.net/10033/246443-
dc.description.abstractMicrobial communities from cow rumen are known for their ability to degrade diverse plant polymers at high rates. In this work, we identified 15 hydrolases through an activity-centred metagenome analysis of a fibre-adherent microbial community from dairy cow rumen. Among them, 7 glycosyl hydrolases (GHs) and 1 feruloyl esterase were successfully cloned, expressed, purified and characterised. The most striking result was a protein of GH family 43 (GHF43), hereinafter designated as R_09-02, which had characteristics very distinct from the other proteins in this family with mono-functional β-xylosidase, α-xylanase, α-L-arabinase and α-L-arabinofuranosidase activities. R_09-02 is the first multifunctional enzyme to exhibit β-1,4 xylosidase, α-1,5 arabinofur(pyr)anosidase, β-1,4 lactase, α-1,6 raffinase, α-1,6 stachyase, β-galactosidase and α-1,4 glucosidase activities. The R_09-02 protein appears to originate from the chromosome of a member of Clostridia, a class of phylum Firmicutes, members of which are highly abundant in ruminal environment. The evolution of R_09-02 is suggested to be driven from the xylose- and arabinose-specific activities, typical for GHF43 members, toward a broader specificity to the glucose- and galactose-containing components of lignocellulose. The apparent capability of enzymes from the GHF43 family to utilise xylose-, arabinose-, glucose- and galactose-containing oligosaccharides has thus far been neglected by, or could not be predicted from, genome and metagenome sequencing data analyses. Taking into account the abundance of GHF43-encoding gene sequences in the rumen (up to 7% of all GH-genes) and the multifunctional phenotype herein described, our findings suggest that the ecological role of this GH family in the digestion of ligno-cellulosic matter should be significantly reconsidered.en_GB
dc.language.isoenen
dc.rightsArchived with thanks to PloS oneen_GB
dc.titleFunctional metagenomics unveils a multifunctional glycosyl hydrolase from the family 43 catalysing the breakdown of plant polymers in the calf rumen.en
dc.typeArticleen
dc.contributor.departmentCSIC, Institute of Catalysis, Madrid, Spain. mferrer@icp.csic.esen_GB
dc.identifier.journalPloS oneen_GB

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