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From proteins to polysaccharides: lifestyle and genetic evolution of Coprothermobacter proteolyticus

B.J. Kunath, F. Delogu, M.Ø. Arntzen, V.G.H. Eijsink, View ORCID ProfileT.R. Hvidsten, View ORCID ProfileP.B. Pope
doi: https://doi.org/10.1101/280602
B.J. Kunath
1Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432 Ås, NORWAY
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F. Delogu
1Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432 Ås, NORWAY
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M.Ø. Arntzen
1Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432 Ås, NORWAY
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V.G.H. Eijsink
1Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432 Ås, NORWAY
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T.R. Hvidsten
1Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432 Ås, NORWAY
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  • ORCID record for T.R. Hvidsten
P.B. Pope
1Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432 Ås, NORWAY
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  • For correspondence: phil.pope@nmbu.no
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ABSTRACT

Microbial communities that degrade lignocellulosic biomass are typified by high levels of species- and strain-level complexity as well as synergistic interactions between both cellulolytic and non-cellulolytic microorganisms. Coprothermobacter proteolyticus frequently dominates thermophilic, lignocellulose-degrading communities with wide geographical distribution, which is in contrast to reports that it ferments proteinaceous substrates and is incapable of polysaccharide hydrolysis. Here we deconvolute a highly efficient cellulose-degrading consortium (SEM1b) that is co-dominated by Clostridium (Ruminiclostridium) thermocellum- and multiple heterogenic strains affiliated to C. proteolyticus. Metagenomic analysis of SEM1b recovered metagenome-assembled genomes (MAGs) for each constituent population, whilst in parallel two novel strains of C. proteolyticus were successfully isolated and sequenced. Annotation of all C. proteolyticus genotypes (two strains and one MAG) revealed their genetic acquisition of various carbohydrate-active enzymes (CAZymes), presumably derived from horizontal gene transfer (HGT) events involving C. thermocellum- or Thermotogae-affiliated populations that are historically co-located. HGT material included whole saccharolytic operons and dockerin-encoding enzymatic subunits that are synonymous with cellulosomes. Finally, temporal genome-resolved metatranscriptomic analysis of SEM1b revealed expression of C. proteolyticus CAZymes at different SEM1b life-stages as well as co-expression of CAZymes from multiple SEM1b populations, inferring deeper microbial interactions that are dedicated towards co-degradation of cellulose and hemicellulose. We show that C. proteolyticus, a ubiquitous keystone population, consists of closely related strains that have adapted via HGT to degrade both oligo- and longer polysaccharides present in decaying plants and microbial cell walls, thus explaining its dominance in thermophilic anaerobic digesters on a global scale.

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  • COMPETING INTERESTS The authors declare there are no competing financial interests in relation to the work described.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted March 12, 2018.
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From proteins to polysaccharides: lifestyle and genetic evolution of Coprothermobacter proteolyticus
B.J. Kunath, F. Delogu, M.Ø. Arntzen, V.G.H. Eijsink, T.R. Hvidsten, P.B. Pope
bioRxiv 280602; doi: https://doi.org/10.1101/280602
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From proteins to polysaccharides: lifestyle and genetic evolution of Coprothermobacter proteolyticus
B.J. Kunath, F. Delogu, M.Ø. Arntzen, V.G.H. Eijsink, T.R. Hvidsten, P.B. Pope
bioRxiv 280602; doi: https://doi.org/10.1101/280602

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