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

Grant/Contract Number:: AC05-76RL01830; AC02-06CH11357; 336355-MicroDE

OSTI ID:: 1432519

Alternate ID(s):: OSTI ID: 1499741

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

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

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 18 works

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References (99)

Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores Pope, P. B.; Denman, S. E.; Jones, M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 33 https://doi.org/10.1073/pnas.1005297107	journal	July 2010
Chemical profiles of switchgrass Hu, Zhoujian; Sykes, Robert; Davis, Mark F. Bioresource Technology, Vol. 101, Issue 9 https://doi.org/10.1016/j.biortech.2009.12.033	journal	May 2010
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
IMG/M 4 version of the integrated metagenome comparative analysis system Markowitz, Victor M.; Chen, I-Min A.; Chu, Ken Nucleic Acids Research, Vol. 42, Issue D1, p. D568-D573 https://doi.org/10.1093/nar/gkt919	journal	October 2013
Metabolic networks for nitrogen utilization in Prevotella ruminicola 23 Kim, Jong Nam; Méndez–García, Celia; Geier, Renae R. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-08463-3	journal	August 2017
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Outer membrane proteins related to SusC and SusD are not required for Cytophaga hutchinsonii cellulose utilization Zhu, Yongtao; Kwiatkowski, Kurt J.; Yang, Tengteng Applied Microbiology and Biotechnology, Vol. 99, Issue 15 https://doi.org/10.1007/s00253-015-6555-8	journal	April 2015
Periplasmic Cytophaga hutchinsonii Endoglucanases Are Required for Use of Crystalline Cellulose as the Sole Source of Carbon and Energy Zhu, Yongtao; Han, Lanlan; Hefferon, Kathleen L. Applied and Environmental Microbiology, Vol. 82, Issue 15 https://doi.org/10.1128/AEM.01298-16	journal	June 2016
Isolation of Succinivibrionaceae Implicated in Low Methane Emissions from Tammar Wallabies Pope, P. B.; Smith, W.; Denman, S. E. Science, Vol. 333, Issue 6042 https://doi.org/10.1126/science.1205760	journal	June 2011
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
Characterization of a multi-function processive endoglucanase CHU_2103 from Cytophaga hutchinsonii Zhang, Cong; Wang, Ying; Li, Zhe Applied Microbiology and Biotechnology, Vol. 98, Issue 15 https://doi.org/10.1007/s00253-014-5640-8	journal	March 2014
Structural Features of a Bacteroidetes-Affiliated Cellulase Linked with a Polysaccharide Utilization Locus Naas, A. E.; MacKenzie, A. K.; Dalhus, B. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep11666	journal	July 2015
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
Dissecting structure–function–stability relationships of a thermostable GH5-CBM3 cellulase from Bacillus subtilis 168 Santos, Camila R.; Paiva, Joice H.; Sforça, Maurício L. Biochemical Journal, Vol. 441, Issue 1 https://doi.org/10.1042/BJ20110869	journal	December 2011
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
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Evaluating Models of Cellulose Degradation by Fibrobacter succinogenes S85 Burnet, Meagan C.; Dohnalkova, Alice C.; Neumann, Anthony P. PLOS ONE, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pone.0143809	journal	December 2015
From cellulosomes to cellulosomics Bayer, Edward A.; Lamed, Raphael; White, Bryan A. The Chemical Record, Vol. 8, Issue 6, p. 364-377 https://doi.org/10.1002/tcr.20160	journal	January 2008
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
Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation Letunic, I.; Bork, P. Bioinformatics, Vol. 23, Issue 1 https://doi.org/10.1093/bioinformatics/btl529	journal	October 2006
Molecular profiling of microbial community structure and their CAZymes via metagenomics, from Tsomgo lake in the Eastern Himalayas Rai, Aditi; Bhattacharjee, Arindam Archives of Microbiology, Vol. 203, Issue 6 https://doi.org/10.1007/s00203-021-02278-7	journal	April 2021
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
PRED-TMBB2: improved topology prediction and detection of beta-barrel outer membrane proteins Tsirigos, Konstantinos D.; Elofsson, Arne; Bagos, Pantelis G. Bioinformatics, Vol. 32, Issue 17 https://doi.org/10.1093/bioinformatics/btw444	journal	September 2016
Invited review: Ruminant ecology and evolution: Perspectives useful to ruminant livestock research and production Hackmann, T. J.; Spain, J. N. Journal of Dairy Science, Vol. 93, Issue 4 https://doi.org/10.3168/jds.2009-2071	journal	April 2010
Analysis of the bovine rumen microbiome reveals a diversity of Sus-like polysaccharide utilization loci from the bacterial phylum Bacteroidetes Rosewarne, Carly P.; Pope, Phillip B.; Cheung, Jane L. Journal of Industrial Microbiology & Biotechnology, Vol. 41, Issue 3 https://doi.org/10.1007/s10295-013-1395-y	journal	January 2014
dbCAN: a web resource for automated carbohydrate-active enzyme annotation Yin, Yanbin; Mao, Xizeng; Yang, Jincai Nucleic Acids Research, Vol. 40, Issue W1 https://doi.org/10.1093/nar/gks479	journal	May 2012
Scaling and assessment of data quality Evans, Philip Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82 https://doi.org/10.1107/S0907444905036693	journal	December 2005
MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Cox, Jürgen; Mann, Matthias Nature Biotechnology, Vol. 26, Issue 12 https://doi.org/10.1038/nbt.1511	journal	November 2008
Outer membrane vesicles from Fibrobacter succinogenes S85 contain an array of carbohydrate-active enzymes with versatile polysaccharide-degrading capacity Arntzen, Magnus Ø.; Várnai, Anikó; Mackie, Roderick I. Environmental Microbiology, Vol. 19, Issue 7 https://doi.org/10.1111/1462-2920.13770	journal	May 2017
Characterization of a family 5 glycoside hydrolase isolated from the outer membrane of cellulolytic Cytophaga hutchinsonii Zhu, Yongtao; Zhou, Hong; Bi, Yanlin Applied Microbiology and Biotechnology, Vol. 97, Issue 9 https://doi.org/10.1007/s00253-012-4259-x	journal	July 2012
KEGG as a reference resource for gene and protein annotation Kanehisa, Minoru; Sato, Yoko; Kawashima, Masayuki Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1070	journal	October 2015
Accurate Proteome-wide Label-free Quantification by Delayed Normalization and Maximal Peptide Ratio Extraction, Termed MaxLFQ Cox, Jürgen; Hein, Marco Y.; Luber, Christian A. Molecular & Cellular Proteomics, Vol. 13, Issue 9 https://doi.org/10.1074/mcp.M113.031591	journal	June 2014
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM Battye, T. Geoff G.; Kontogiannis, Luke; Johnson, Owen Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910048675	journal	March 2011
Decision making in xia 2 Winter, Graeme; Lobley, Carina M. C.; Prince, Stephen M. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913015308	journal	June 2013
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Expression and characteristics of a Ca2+-dependent endoglucanase from Cytophaga hutchinsonii Zhang, Cong; Zhang, Weican; Lu, Xuemei Applied Microbiology and Biotechnology, Vol. 99, Issue 22 https://doi.org/10.1007/s00253-015-6746-3	journal	July 2015
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
Extra virgin olive oil improved body weight and insulin sensitivity in high fat diet-induced obese LDLr−/−.Leiden mice without attenuation of steatohepatitis Álvarez-Amor, Leticia; Sierra, Amparo Luque; Cárdenas, Antonio Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-87761-3	journal	April 2021
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
Identification of protein secretion systems in bacterial genomes Abby, Sophie S.; Cury, Jean; Guglielmini, Julien Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep23080	journal	March 2016
Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar Miller, G. L. Analytical Chemistry, Vol. 31, Issue 3 https://doi.org/10.1021/ac60147a030	journal	March 1959
Deletion of the Cytophaga hutchinsonii type IX secretion system gene sprP results in defects in gliding motility and cellulose utilization Zhu, Yongtao; McBride, Mark J. Applied Microbiology and Biotechnology, Vol. 98, Issue 2 https://doi.org/10.1007/s00253-013-5355-2	journal	November 2013
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Polysaccharide Utilization Loci: Fueling Microbial Communities Grondin, Julie M.; Tamura, Kazune; Déjean, Guillaume Journal of Bacteriology, Vol. 199, Issue 15 https://doi.org/10.1128/JB.00860-16	journal	January 2017
The outer-membrane export signal of Porphyromonas gingivalis type IX secretion system (T9SS) is a conserved C-terminal β-sandwich domain de Diego, Iñaki; Ksiazek, Miroslaw; Mizgalska, Danuta Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep23123	journal	March 2016
Revealing Nature's Cellulase Diversity The Digestion Mechanism of Caldicellulosiruptor bescii CelA Brunecky, R.; Alahuhta, M.; Xu, Q. Science, Vol. 342, Issue 6165, p. 1513-1516 https://doi.org/10.1126/science.1244273	journal	December 2013
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Flavobacterium gliding motility and the type IX secretion system McBride, Mark J.; Nakane, Daisuke Current Opinion in Microbiology, Vol. 28 https://doi.org/10.1016/j.mib.2015.07.016	journal	December 2015
The Perseus computational platform for comprehensive analysis of (prote)omics data Tyanova, Stefka; Temu, Tikira; Sinitcyn, Pavel Nature Methods, Vol. 13, Issue 9 https://doi.org/10.1038/nmeth.3901	journal	June 2016
The Genome of the Anaerobic Fungus Orpinomyces sp. Strain C1A Reveals the Unique Evolutionary History of a Remarkable Plant Biomass Degrader Youssef, Noha H.; Couger, M. B.; Struchtemeyer, Christopher G. Applied and Environmental Microbiology, Vol. 79, Issue 15 https://doi.org/10.1128/AEM.00821-13	journal	May 2013
Overview of the CCP4 suite and current developments. Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52322	text	January 2011
Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life Parks, Donovan H.; Rinke, Christian; Chuvochina, Maria Nature Microbiology, Vol. 2, Issue 11 https://doi.org/10.1038/s41564-017-0012-7	journal	September 2017
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
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
Flavobacterium johnsoniae Chitinase ChiA Is Required for Chitin Utilization and Is Secreted by the Type IX Secretion System Kharade, S. S.; McBride, M. J. Journal of Bacteriology, Vol. 196, Issue 5 https://doi.org/10.1128/JB.01170-13	journal	December 2013
HMMER web server: interactive sequence similarity searching Finn, R. D.; Clements, J.; Eddy, S. R. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr367	journal	May 2011
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
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
A protein secretion system linked to bacteroidete gliding motility and pathogenesis Sato, K.; Naito, M.; Yukitake, H. Proceedings of the National Academy of Sciences, Vol. 107, Issue 1 https://doi.org/10.1073/pnas.0912010107	journal	December 2009
Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen Hess, M.; Sczyrba, A.; Egan, R. Science, Vol. 331, Issue 6016 https://doi.org/10.1126/science.1200387	journal	January 2011
Reversed-phase chromatography with multiple fraction concatenation strategy for proteome profiling of human MCF10A cells Wang, Yuexi; Yang, Feng; Gritsenko, Marina A. PROTEOMICS, Vol. 11, Issue 10 https://doi.org/10.1002/pmic.201000722	journal	April 2011
Unique aspects of the grass cell wall Vogel, J. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.03.002	journal	June 2008
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis Jäger, Gernot; Girfoglio, Michele; Dollo, Florian RWTH Aachen University https://doi.org/10.18154/rwth-conv-043922	text	January 2011
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, A. Karlsruhe https://doi.org/10.5445/ir/1000045818	text	January 2014
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5) Aspeborg, Henrik; Coutinho, Pedro M.; Wang, Yang BioMed Central https://doi.org/10.14288/1.0074600	text	January 2012
Reversed-phase chromatography with multiple fraction concatenation strategy for proteome profiling of human MCF10A cells Wang, Yuexi; Yang, Feng; Gritsenko, Marina A. PROTEOMICS, Vol. 11, Issue 10 https://doi.org/10.1002/pmic.201000722	journal	April 2011
From cellulosomes to cellulosomics Bayer, Edward A.; Lamed, Raphael; White, Bryan A. The Chemical Record, Vol. 8, Issue 6, p. 364-377 https://doi.org/10.1002/tcr.20160	journal	January 2008
Deletion of the Cytophaga hutchinsonii type IX secretion system gene sprP results in defects in gliding motility and cellulose utilization Zhu, Yongtao; McBride, Mark J. Applied Microbiology and Biotechnology, Vol. 98, Issue 2 https://doi.org/10.1007/s00253-013-5355-2	journal	November 2013
Outer membrane proteins related to SusC and SusD are not required for Cytophaga hutchinsonii cellulose utilization Zhu, Yongtao; Kwiatkowski, Kurt J.; Yang, Tengteng Applied Microbiology and Biotechnology, Vol. 99, Issue 15 https://doi.org/10.1007/s00253-015-6555-8	journal	April 2015
Expression and characteristics of a Ca2+-dependent endoglucanase from Cytophaga hutchinsonii Zhang, Cong; Zhang, Weican; Lu, Xuemei Applied Microbiology and Biotechnology, Vol. 99, Issue 22 https://doi.org/10.1007/s00253-015-6746-3	journal	July 2015
Analysis of the bovine rumen microbiome reveals a diversity of Sus-like polysaccharide utilization loci from the bacterial phylum Bacteroidetes Rosewarne, Carly P.; Pope, Phillip B.; Cheung, Jane L. Journal of Industrial Microbiology & Biotechnology, Vol. 41, Issue 3 https://doi.org/10.1007/s10295-013-1395-y	journal	January 2014
Chemical profiles of switchgrass Hu, Zhoujian; Sykes, Robert; Davis, Mark F. Bioresource Technology, Vol. 101, Issue 9 https://doi.org/10.1016/j.biortech.2009.12.033	journal	May 2010
Flavobacterium gliding motility and the type IX secretion system McBride, Mark J.; Nakane, Daisuke Current Opinion in Microbiology, Vol. 28 https://doi.org/10.1016/j.mib.2015.07.016	journal	December 2015
Unique aspects of the grass cell wall Vogel, J. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.03.002	journal	June 2008
Mating pair stabilization mediates bacterial conjugation species specificity Low, Wen Wen; Wong, Joshua L. C.; Beltran, Leticia C. Nature Microbiology, Vol. 7, Issue 7 https://doi.org/10.1038/s41564-022-01146-4	journal	June 2022
Metabolic networks for nitrogen utilization in Prevotella ruminicola 23 Kim, Jong Nam; Méndez–García, Celia; Geier, Renae R. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-08463-3	journal	August 2017
Hepatitis C virus enhances Rubicon expression, leading to autophagy inhibition and intracellular innate immune activation Shiode, Yuto; Hikita, Hayato; Tanaka, Satoshi Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-72294-y	journal	September 2020
Structural Features of a Bacteroidetes-Affiliated Cellulase Linked with a Polysaccharide Utilization Locus Naas, A. E.; MacKenzie, A. K.; Dalhus, B. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep11666	journal	July 2015
Identification of protein secretion systems in bacterial genomes Abby, Sophie S.; Cury, Jean; Guglielmini, Julien Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep23080	journal	March 2016
The outer-membrane export signal of Porphyromonas gingivalis type IX secretion system (T9SS) is a conserved C-terminal β-sandwich domain de Diego, Iñaki; Ksiazek, Miroslaw; Mizgalska, Danuta Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep23123	journal	March 2016
A protein secretion system linked to bacteroidete gliding motility and pathogenesis Sato, K.; Naito, M.; Yukitake, H. Proceedings of the National Academy of Sciences, Vol. 107, Issue 1 https://doi.org/10.1073/pnas.0912010107	journal	December 2009
Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores Pope, P. B.; Denman, S. E.; Jones, M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 33 https://doi.org/10.1073/pnas.1005297107	journal	July 2010
Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation Letunic, I.; Bork, P. Bioinformatics, Vol. 23, Issue 1 https://doi.org/10.1093/bioinformatics/btl529	journal	October 2006
PRED-TMBB2: improved topology prediction and detection of beta-barrel outer membrane proteins Tsirigos, Konstantinos D.; Elofsson, Arne; Bagos, Pantelis G. Bioinformatics, Vol. 32, Issue 17 https://doi.org/10.1093/bioinformatics/btw444	journal	September 2016
HMMER web server: interactive sequence similarity searching Finn, R. D.; Clements, J.; Eddy, S. R. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr367	journal	May 2011
IMG/M 4 version of the integrated metagenome comparative analysis system Markowitz, Victor M.; Chen, I-Min A.; Chu, Ken Nucleic Acids Research, Vol. 42, Issue D1, p. D568-D573 https://doi.org/10.1093/nar/gkt919	journal	October 2013
KEGG as a reference resource for gene and protein annotation Kanehisa, Minoru; Sato, Yoko; Kawashima, Masayuki Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1070	journal	October 2015
Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen Hess, M.; Sczyrba, A.; Egan, R. Science, Vol. 331, Issue 6016 https://doi.org/10.1126/science.1200387	journal	January 2011
Isolation of Succinivibrionaceae Implicated in Low Methane Emissions from Tammar Wallabies Pope, P. B.; Smith, W.; Denman, S. E. Science, Vol. 333, Issue 6042 https://doi.org/10.1126/science.1205760	journal	June 2011
Revealing Nature's Cellulase Diversity The Digestion Mechanism of Caldicellulosiruptor bescii CelA Brunecky, R.; Alahuhta, M.; Xu, Q. Science, Vol. 342, Issue 6165, p. 1513-1516 https://doi.org/10.1126/science.1244273	journal	December 2013
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
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
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
Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5) Aspeborg, Henrik; Coutinho, Pedro M.; Wang, Yang BioMed Central https://doi.org/10.14288/1.0074600	text	January 2012

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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

Journal Article · 2018 · Microbiome · OSTI ID:1437543

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

Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber

Journal Article · 2020 · The ISME Journal · OSTI ID:1756378

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

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 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 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 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 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 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 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 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 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 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 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 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 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 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 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 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 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 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 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 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 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 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 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 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 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
“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
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 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 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 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
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 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 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 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 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 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 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

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

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