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

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Ferrer, Manuel
Ghazi, Azam
Beloqui, Ana
Vieites, Jose Marıa
Lopez-Cortes, Nieves
Marın-Navarro, Julia
Nechitaylo, Taras Y.
Guazzaroni, Marıa-Eugenia
Polaina, Julio
Waliczek, Agnes

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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 bxylosidase, a-xylanase, a-L-arabinase and a-L-arabinofuranosidase activities. R_09-02 is the first multifunctional enzyme to exhibit b-1,4 xylosidase, a-1,5 arabinofur(pyr)anosidase, b-1,4 lactase, a-1,6 raffinase, a-1,6 stachyase, b-galactosidase and a- 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.

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Calf rumen, Breakdown of plant polymers

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Citation

Ferrer M, Ghazi A, Beloqui A, Vieites JM, Lopez-Cortes N, et al. (2012) Functional Metagenomics Unveils a Multifunctional Glycosyl Hydrolase from the Family 43 Catalysing the Breakdown of Plant Polymers in the Calf Rumen. PLoS ONE 7(6): e38134. DOI: 10.1371/journal.pone.0038134.