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

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.

doi:10.1186/s40168-018-0421-8

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

Journal Article · 28 February 2018 · Microbiome

DOI: https://doi.org/10.1186/s40168-018-0421-8 · OSTI ID:1432519

Naas, A. E. ^[1]; Solden, L. M. ^[2]; Norbeck, A. D. ^[3]; Brewer, H. ^[3]; Hagen, L. H. ^[1]; Heggenes, I. M. ^[1]; McHardy, A. C. ^[4]; Mackie, R. I. ^[5]; Paša-Tolić, L. ^[3]; Arntzen, M. Ø. ^[1]; Eijsink, V. G. H. ^[1]; Koropatkin, N. M. ^[6]; Hess, M. ^[7]; Wrighton, K. C. ^[2]; Pope, P. B. ^[1]

Norwegian Univ. of Life Sciences (NMBU), As (Norway). Faculty of Chemistry, Biotechnology and Food Science
The Ohio State Univ., Columbus, OH (United States). Dept of Microbiology
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Helmholtz Centre for Infection Research, Braunschweig (Germany). Computational Biology of Infection Research
Univ. of Illinois, Urbana-Champaign, IL (United States). Inst. for Genomic Biology and Dept. of Animal Sciences
Univ. of Michigan, Ann Arbor, MI (United States). Medical School, Dept. of Microbiology and Immunology
Univ. of California, Davis, CA (United States). Dept. of Animal Science

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 in this paper, we combine meta-omics and enzymology to identify and describe a novel Bacteroidetes family (“Candidatus MH11”) composed entirely of uncultivated strains that are predominant in ruminants and only distantly related to previously characterized taxa. Results: The first metabolic reconstruction of Ca. MH11-affiliated genome bins, with a particular focus on the provisionally named “Candidatus Paraporphyromonas 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 IX 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 Ca. P. 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 Ca. P. 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 Ca. P. polyenzymogene genotypes and other Ca. MH11 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 Gram-negative 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.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Organization:: European Research Council (ERC); Research Council of Norway; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-06CH11357; AC05-76RL01830

OSTI ID:: 1432519

Report Number(s):: PNNL-SA--129531; PII: 421

Journal Information:: Microbiome, Journal Name: Microbiome Journal Issue: 1 Vol. 6; ISSN 2049-2618

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Flavobacterium johnsoniae PorV Is Required for Secretion of a Subset of Proteins Targeted to the Type IX Secretion System Kharade, Sampada S.; McBride, Mark J. Journal of Bacteriology, Vol. 197, Issue 1 https://doi.org/10.1128/JB.02085-14	journal	October 2014
Cellulosomal Scaffoldin-Like Proteins from Ruminococcus flavefaciens Ding, S. -Y.; Rincon, M. T.; Lamed, R. Journal of Bacteriology, Vol. 183, Issue 6 https://doi.org/10.1128/JB.183.6.1945-1953.2001	journal	March 2001
Do Rumen Bacteroidetes Utilize an Alternative Mechanism for Cellulose Degradation? Naas, A. E.; Mackenzie, A. K.; Mravec, J. mBio, Vol. 5, Issue 4 https://doi.org/10.1128/mBio.01401-14	journal	August 2014
Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5) Aspeborg, Henrik; Coutinho, Pedro M.; Wang, Yang BMC Evolutionary Biology, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2148-12-186	journal	January 2012
How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis Jäger, Gernot; Girfoglio, Michele; Dollo, Florian Biotechnology for Biofuels, Vol. 4, Issue 1 https://doi.org/10.1186/1754-6834-4-33	journal	January 2011
Novel enzymes for the degradation of cellulose Horn, Svein; Vaaje-Kolstad, Gustav; Westereng, Bjørge Biotechnology for Biofuels, Vol. 5, Issue 1, Article No. 45 https://doi.org/10.1186/1754-6834-5-45	journal	January 2012
De novo prediction of the genomic components and capabilities for microbial plant biomass degradation from (meta-)genomes Weimann, Aaron; Trukhina, Yulia; Pope, Phillip B. Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-24	journal	January 2013
Inference of phenotype-defining functional modules of protein families for microbial plant biomass degraders Konietzny, Sebastian GA; Pope, Phillip B.; Weimann, Aaron Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/s13068-014-0124-8	journal	September 2014
Natural diversity of cellulases, xylanases, and chitinases in bacteria Talamantes, Darrian; Biabini, Nazmehr; Dang, Hoang Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0538-6	journal	June 2016
A polysaccharide utilization locus from Flavobacterium johnsoniae enables conversion of recalcitrant chitin Larsbrink, Johan; Zhu, Yongtao; Kharade, Sampada S. Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0674-z	journal	November 2016
Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals Ormerod, Kate L.; Wood, David L. A.; Lachner, Nancy Microbiome, Vol. 4, Issue 1 https://doi.org/10.1186/s40168-016-0181-2	journal	July 2016
Metagenomic Insights into the Carbohydrate-Active Enzymes Carried by the Microorganisms Adhering to Solid Digesta in the Rumen of Cows Wang, Lingling; Hatem, Ayat; Catalyurek, Umit V. PLoS ONE, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pone.0078507	journal	November 2013
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“Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system

Journal Article · 2018 · Microbiome · OSTI ID:1439008

Naas, A. E.; Solden, L. M.; Norbeck, A. D.; +12 more

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

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Bacteroidetes
Carbohydrate-active enzymes
Cellulases
Type IX secretion system

Additional file 7: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/M9.FIGSHARE.5937997 The current record is supplemented by this dataset	dataset	March 2018
Additional file 10: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937715 The current record is supplemented by this preprint	preprint	March 2018
Additional file 10: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937715.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 11: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937745 The current record is supplemented by this figure	figure	March 2018
Additional file 11: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937745.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 12: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937769 The current record is supplemented by this dataset	dataset	January 2018
Additional file 12: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937769.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 13: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937784 The current record is supplemented by this figure	figure	March 2018
Additional file 13: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937784.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 14: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937796 The current record is supplemented by this dataset	dataset	March 2018
Additional file 14: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937796.v1 The current record is supplemented by this figure	figure	March 2018
Additional file 15: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937820 The current record is supplemented by this dataset	dataset	March 2018
Additional file 15: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937820.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 16: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937838 The current record is supplemented by this dataset	dataset	March 2018
Additional file 16: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937838.v1 The current record is supplemented by this figure	figure	March 2018
Additional file 17: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937856 The current record is supplemented by this dataset	dataset	March 2018
Additional file 17: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937856.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 18: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937874 The current record is supplemented by this figure	figure	March 2018
Additional file 18: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937874.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 1: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937889 The current record is supplemented by this figure	figure	March 2018
Additional file 1: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937889.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 2: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937910 The current record is supplemented by this dataset	dataset	March 2018
Additional file 2: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937910.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 3: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937925 The current record is supplemented by this dataset	dataset	January 2018
Additional file 3: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937925.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 4: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937940 The current record is supplemented by this figure	figure	March 2018
Additional file 4: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937940.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 5: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937955 The current record is supplemented by this dataset	dataset	March 2018
Additional file 5: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937955.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 6: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937979 The current record is supplemented by this dataset	dataset	March 2018
Additional file 6: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937979.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 7: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5937997.v1 The current record is supplemented by this		March 2018
Additional file 8: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5938015 The current record is supplemented by this figure	figure	March 2018
Additional file 8: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5938015.v1 The current record is supplemented by this dataset	dataset	March 2018
Additional file 9: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5938030 The current record is supplemented by this figure	figure	March 2018
Additional file 9: of “Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.5938030.v1 The current record is supplemented by this figure	figure	March 2018
“Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system [Supplemental Data] Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.c.4019146 The current record is supplemented by this collection	collection	March 2018
“Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system Naas, A.; Solden, L.; Norbeck, A. https://doi.org/10.6084/m9.figshare.c.4019146.v1 The current record is supplemented by this dataset	dataset	March 2018

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

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