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Title: “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system

Abstract

Background In Nature, obligate herbivorous ruminants have a close symbiotic relationship with their gastrointestinal microbiome, which proficiently deconstructs plant biomass. Despite decades of research, lignocellulose degradation in the rumen has thus far been attributed to a limited number of culturable microorganisms. Here, we combine metaomics and enzymology to identify and describe a novel Bacteroidetes family (UMH11) composed entirely of uncultivated strains that are predominant in ruminants and only distantly related to previously characterized taxa. Results The first metabolic reconstruction of UMH11-affiliated genome bins, with a particular focus on the provisionally named UParaporphyromonas polyenzymogenes, illustrated their capacity to degrade various lignocellulosic substrates via comprehensive inventories of singular and multi-modular carbohydrate active enzymes (CAZymes). Closer examination revealed an absence of archetypical polysaccharide utilization loci found in human-gut microbiota. Instead, we identified many multi-modular CAZymes putatively secreted via the Bacteroidetes-specific Type 9 secretion system (T9SS). This included cellulases with two or more catalytic domains, which are modular arrangements that are unique to Bacteroidetes species studied to date. Core metabolic proteins from UP. polyenzymogenes were detected in metaproteomic data and were enriched in rumen-incubated plant biomass, indicating that active saccharification and fermentation of complex carbohydrates could be assigned to members of this novel family.more » Biochemical analysis of selected UP. polyenzymogenes CAZymes further iterated the cellulolytic activity of this hitherto uncultured bacterium towards linear polymers, such as amorphous and crystalline cellulose as well as mixed linkage β-glucans. Conclusion We propose that UP. olyenzymogenes genotypes and other UMH11 members actively degrade plant biomass in the rumen of cows, sheep, and most likely other ruminants, utilizing singular and multi-domain catalytic CAZymes secreted through the T9SS. The discovery of a prominent role of multi-modular cellulases in the Gramnegative Bacteroidetes, together with similar findings for Gram-positive cellulosomal bacteria (Ruminococcus flavefaciens) and anaerobic fungi (Orpinomyces sp.), suggests that complex enzymes are essential and have evolved within all major cellulolytic dominions inherent to the rumen.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1439008
Report Number(s):
PNNL-SA-129531
Journal ID: ISSN 2049-2618; 47483; KP1704020
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Microbiome; Journal Volume: 6; Journal Issue: 1
Country of Publication:
United States
Language:
English
Subject:
Environmental Molecular Sciences Laboratory

Citation Formats

Naas, A. E., Solden, L. M., Norbeck, A. D., Brewer, H., Hagen, L. H., Heggenes, I. M., McHardy, A. C., Mackie, R. I., Paša-Tolić, L., Arntzen, M. Ø., Eijsink, V. G. H., Koropatkin, N. M., Hess, M., Wrighton, K. C., and Pope, P. B. “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system. United States: N. p., 2018. Web. doi:10.1186/s40168-018-0421-8.
Naas, A. E., Solden, L. M., Norbeck, A. D., Brewer, H., Hagen, L. H., Heggenes, I. M., McHardy, A. C., Mackie, R. I., Paša-Tolić, L., Arntzen, M. Ø., Eijsink, V. G. H., Koropatkin, N. M., Hess, M., Wrighton, K. C., & Pope, P. B. “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system. United States. doi:10.1186/s40168-018-0421-8.
Naas, A. E., Solden, L. M., Norbeck, A. D., Brewer, H., Hagen, L. H., Heggenes, I. M., McHardy, A. C., Mackie, R. I., Paša-Tolić, L., Arntzen, M. Ø., Eijsink, V. G. H., Koropatkin, N. M., Hess, M., Wrighton, K. C., and Pope, P. B. Thu . "“Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system". United States. doi:10.1186/s40168-018-0421-8.
@article{osti_1439008,
title = {“Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system},
author = {Naas, A. E. and Solden, L. M. and Norbeck, A. D. and Brewer, H. and Hagen, L. H. and Heggenes, I. M. and McHardy, A. C. and Mackie, R. I. and Paša-Tolić, L. and Arntzen, M. Ø. and Eijsink, V. G. H. and Koropatkin, N. M. and Hess, M. and Wrighton, K. C. and Pope, P. B.},
abstractNote = {Background In Nature, obligate herbivorous ruminants have a close symbiotic relationship with their gastrointestinal microbiome, which proficiently deconstructs plant biomass. Despite decades of research, lignocellulose degradation in the rumen has thus far been attributed to a limited number of culturable microorganisms. Here, we combine metaomics and enzymology to identify and describe a novel Bacteroidetes family (UMH11) composed entirely of uncultivated strains that are predominant in ruminants and only distantly related to previously characterized taxa. Results The first metabolic reconstruction of UMH11-affiliated genome bins, with a particular focus on the provisionally named UParaporphyromonas polyenzymogenes, illustrated their capacity to degrade various lignocellulosic substrates via comprehensive inventories of singular and multi-modular carbohydrate active enzymes (CAZymes). Closer examination revealed an absence of archetypical polysaccharide utilization loci found in human-gut microbiota. Instead, we identified many multi-modular CAZymes putatively secreted via the Bacteroidetes-specific Type 9 secretion system (T9SS). This included cellulases with two or more catalytic domains, which are modular arrangements that are unique to Bacteroidetes species studied to date. Core metabolic proteins from UP. polyenzymogenes were detected in metaproteomic data and were enriched in rumen-incubated plant biomass, indicating that active saccharification and fermentation of complex carbohydrates could be assigned to members of this novel family. Biochemical analysis of selected UP. polyenzymogenes CAZymes further iterated the cellulolytic activity of this hitherto uncultured bacterium towards linear polymers, such as amorphous and crystalline cellulose as well as mixed linkage β-glucans. Conclusion We propose that UP. olyenzymogenes genotypes and other UMH11 members actively degrade plant biomass in the rumen of cows, sheep, and most likely other ruminants, utilizing singular and multi-domain catalytic CAZymes secreted through the T9SS. The discovery of a prominent role of multi-modular cellulases in the Gramnegative Bacteroidetes, together with similar findings for Gram-positive cellulosomal bacteria (Ruminococcus flavefaciens) and anaerobic fungi (Orpinomyces sp.), suggests that complex enzymes are essential and have evolved within all major cellulolytic dominions inherent to the rumen.},
doi = {10.1186/s40168-018-0421-8},
journal = {Microbiome},
number = 1,
volume = 6,
place = {United States},
year = {Thu Mar 01 00:00:00 EST 2018},
month = {Thu Mar 01 00:00:00 EST 2018}
}