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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 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 couldmore » 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.« less

Authors:
 [1];  [2];  [3];  [3];  [1];  [1];  [4];  [5];  [3];  [1];  [1];  [6];  [7];  [2];  [1]
+ Show Author Affiliations
  1. Norwegian Univ. of Life Sciences (NMBU), As (Norway). Faculty of Chemistry, Biotechnology and Food Science
  2. The Ohio State Univ., Columbus, OH (United States). Dept of Microbiology
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
  4. Helmholtz Centre for Infection Research, Braunschweig (Germany). Computational Biology of Infection Research
  5. Univ. of Illinois, Urbana-Champaign, IL (United States). Inst. for Genomic Biology and Dept. of Animal Sciences
  6. Univ. of Michigan, Ann Arbor, MI (United States). Medical School, Dept. of Microbiology and Immunology
  7. Univ. of California, Davis, CA (United States). Dept. of Animal Science
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL); Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
Research Council of Norway; European Research Council (ERC); USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1432519
Alternate Identifier(s):
OSTI ID: 1499741
Report Number(s):
PNNL-SA-129531
Journal ID: ISSN 2049-2618; PII: 421
Grant/Contract Number:  
AC05-76RL01830; AC02-06CH11357; 336355-MicroDE
Resource Type:
Accepted Manuscript
Journal Name:
Microbiome
Additional Journal Information:
Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 2049-2618
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Type IX secretion system; Carbohydrate-active enzymes; Cellulases; Bacteroidetes

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.
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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. https://doi.org/10.1186/s40168-018-0421-8
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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. https://doi.org/10.1186/s40168-018-0421-8. https://www.osti.gov/servlets/purl/1432519.
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@article{osti_1432519,
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 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.},
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}
}
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https://doi.org/10.1186/s40168-018-0421-8
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Outer membrane proteins related to SusC and SusD are not required for Cytophaga hutchinsonii cellulose utilization
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Analysis of the bovine rumen microbiome reveals a diversity of Sus-like polysaccharide utilization loci from the bacterial phylum Bacteroidetes
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Chemical profiles of switchgrass
journal, May 2010

Flavobacterium gliding motility and the type IX secretion system
journal, December 2015

Unique aspects of the grass cell wall
journal, June 2008

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Metabolic networks for nitrogen utilization in Prevotella ruminicola 23
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Structural Features of a Bacteroidetes-Affiliated Cellulase Linked with a Polysaccharide Utilization Locus
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Identification of protein secretion systems in bacterial genomes
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The outer-membrane export signal of Porphyromonas gingivalis type IX secretion system (T9SS) is a conserved C-terminal β-sandwich domain
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A protein secretion system linked to bacteroidete gliding motility and pathogenesis
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Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores
journal, July 2010

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  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 33
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Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation
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PRED-TMBB2: improved topology prediction and detection of beta-barrel outer membrane proteins
journal, September 2016

HMMER web server: interactive sequence similarity searching
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IMG/M 4 version of the integrated metagenome comparative analysis system
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KEGG as a reference resource for gene and protein annotation
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Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen
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Isolation of Succinivibrionaceae Implicated in Low Methane Emissions from Tammar Wallabies
journal, June 2011

Revealing Nature's Cellulase Diversity The Digestion Mechanism of Caldicellulosiruptor bescii CelA
journal, December 2013

Flavobacterium johnsoniae Chitinase ChiA Is Required for Chitin Utilization and Is Secreted by the Type IX Secretion System
journal, December 2013

  • Kharade, S. S.; McBride, M. J.
  • Journal of Bacteriology, Vol. 196, Issue 5
  • DOI: 10.1128/jb.01170-13

Flavobacterium johnsoniae PorV Is Required for Secretion of a Subset of Proteins Targeted to the Type IX Secretion System
journal, October 2014

  • Kharade, Sampada S.; McBride, Mark J.
  • Journal of Bacteriology, Vol. 197, Issue 1
  • DOI: 10.1128/jb.02085-14

Cellulosomal Scaffoldin-Like Proteins from Ruminococcus flavefaciens
journal, March 2001

Do Rumen Bacteroidetes Utilize an Alternative Mechanism for Cellulose Degradation?
journal, August 2014

How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis
journal, January 2011

  • Jäger, Gernot; Girfoglio, Michele; Dollo, Florian
  • Biotechnology for Biofuels, Vol. 4, Issue 1
  • DOI: 10.1186/1754-6834-4-33

Natural diversity of cellulases, xylanases, and chitinases in bacteria
journal, June 2016

  • Talamantes, Darrian; Biabini, Nazmehr; Dang, Hoang
  • Biotechnology for Biofuels, Vol. 9, Issue 1
  • DOI: 10.1186/s13068-016-0538-6

A polysaccharide utilization locus from Flavobacterium johnsoniae enables conversion of recalcitrant chitin
journal, November 2016

  • Larsbrink, Johan; Zhu, Yongtao; Kharade, Sampada S.
  • Biotechnology for Biofuels, Vol. 9, Issue 1
  • DOI: 10.1186/s13068-016-0674-z

Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5)
text, January 2012

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