The complex physiology of Cellvibrio japonicus xylan degradation relies on a single cytoplasmic β-xylosidase for xylo-oligosaccharide utilization

Blake, Andrew D.; Beri, Nina R.; Guttman, Hadassa S.; Cheng, Raymond; Gardner, Jeffrey G.

doi:10.1111/mmi.13903

Title: The complex physiology of Cellvibrio japonicus xylan degradation relies on a single cytoplasmic β-xylosidase for xylo-oligosaccharide utilization

Journal Article · Thu Dec 21 00:00:00 EST 2017 · Molecular Microbiology

DOI:https://doi.org/10.1111/mmi.13903· OSTI ID:1415270

Blake, Andrew D. ^[1]; Beri, Nina R. ^[1]; Guttman, Hadassa S. ^[1]; Cheng, Raymond ^[1];

^[1]

Univ. of Maryland Baltimore County (UMBC), Baltimore, MD (United States). Dept. of Biological Sciences

Summary Lignocellulose degradation by microbes plays a central role in global carbon cycling, human gut metabolism and renewable energy technologies. While considerable effort has been put into understanding the biochemical aspects of lignocellulose degradation, much less work has been done to understand how these enzymes work in an in vivo context. Here, we report a systems level study of xylan degradation in the saprophytic bacterium Cellvibrio japonicus . Transcriptome analysis indicated seven genes that encode carbohydrate active enzymes were up‐regulated during growth with xylan containing media. In‐frame deletion analysis of these genes found that only gly43F is critical for utilization of xylo‐oligosaccharides, xylan, and arabinoxylan. Heterologous expression of gly43F was sufficient for the utilization of xylo‐oligosaccharides in Escherichia coli . Additional analysis found that the xyn11A , xyn11B , abf43L , abf43K , and abf51A gene products were critical for utilization of arabinoxylan. Furthermore, a predicted transporter (CJA_1315) was required for effective utilization of xylan substrates, and we propose this unannotated gene be called xntA (xylan transporter A). Our major findings are (i) C. japonicus employs both secreted and surface associated enzymes for xylan degradation, which differs from the strategy used for cellulose degradation, and (ii) a single cytoplasmic β‐xylosidase is essential for the utilization of xylo‐oligosaccharides.

View Accepted Manuscript (DOE)

View Accepted Manuscript (Publisher)

Cite

Export

Save

Research Organization:: Univ. of Maryland Baltimore County (UMBC), Baltimore, MD (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: SC0014183; DE‐SC0014183

OSTI ID:: 1415270

Alternate ID(s):: OSTI ID: 1416401

Journal Information:: Molecular Microbiology, Vol. 107, Issue 5; ISSN 0950-382X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 17 works

Citation information provided by
Web of Science

References (53)

The Structure and Function of an Arabinan-specific α-1,2-Arabinofuranosidase Identified from Screening the Activities of Bacterial GH43 Glycoside Hydrolases Cartmell, Alan; McKee, Lauren S.; Peña, Maria J. Journal of Biological Chemistry, Vol. 286, Issue 17 https://doi.org/10.1074/jbc.M110.215962	journal	February 2011
In-Frame Deletions Allow Functional Characterization of Complex Cellulose Degradation Phenotypes in Cellvibrio japonicus Nelson, Cassandra E.; Gardner, Jeffrey G. Applied and Environmental Microbiology, Vol. 81, Issue 17 https://doi.org/10.1128/AEM.00847-15	journal	June 2015
The Metagenome of an Anaerobic Microbial Community Decomposing Poplar Wood Chips van der Lelie, Daniel; Taghavi, Safiyh; McCorkle, Sean M. PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0036740	journal	May 2012
ExbBD-Dependent Transport of Maltodextrins through the Novel MalA Protein across the Outer Membrane of Caulobacter crescentus Neugebauer, H.; Herrmann, C.; Kammer, W. Journal of Bacteriology, Vol. 187, Issue 24 https://doi.org/10.1128/JB.187.24.8300-8311.2005	journal	November 2005
Systems analysis in Cellvibrio japonicus resolves predicted redundancy of β-glucosidases and determines essential physiological functions : Functional analysis of Nelson, Cassandra E.; Rogowski, Artur; Morland, Carl Molecular Microbiology, Vol. 104, Issue 2 https://doi.org/10.1111/mmi.13625	journal	February 2017
Hemicelluloses Scheller, Henrik Vibe; Ulvskov, Peter Annual Review of Plant Biology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev-arplant-042809-112315	journal	June 2010
Xylan biosynthesis Rennie, Emilie A.; Scheller, Henrik Vibe Current Opinion in Biotechnology, Vol. 26 https://doi.org/10.1016/j.copbio.2013.11.013	journal	April 2014
Understanding How the Complex Molecular Architecture of Mannan-degrading Hydrolases Contributes to Plant Cell Wall Degradation Zhang, Xiaoyang; Rogowski, Artur; Zhao, Lei Journal of Biological Chemistry, Vol. 289, Issue 4 https://doi.org/10.1074/jbc.M113.527770	journal	December 2013
Xylanase B and an arabinofuranosidase from Pseudomonas fluorescens subsp. cellulosa contain identical cellulose-binding domains and are encoded by adjacent genes Kellett, L. E.; Poole, D. M.; Ferreira, L. M. Biochemical Journal, Vol. 272, Issue 2 https://doi.org/10.1042/bj2720369	journal	December 1990
Consolidated bioprocessing of cellulosic biomass: an update Lynd, Lee R.; van Zyl, Willem H.; McBride, John E. Current Opinion in Biotechnology, Vol. 16, Issue 5, p. 577-583 https://doi.org/10.1016/j.copbio.2005.08.009	journal	October 2005
Global Gene Expression Patterns in Clostridium thermocellum as Determined by Microarray Analysis of Chemostat Cultures on Cellulose or Cellobiose Riederer, Allison; Takasuka, Taichi E.; Makino, Shin-ichi Applied and Environmental Microbiology, Vol. 77, Issue 4 https://doi.org/10.1128/AEM.02008-10	journal	December 2010
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
New substrates for TonB-dependent transport: do we only see the ‘tip of the iceberg’? Schauer, Kristine; Rodionov, Dmitry A.; de Reuse, Hilde Trends in Biochemical Sciences, Vol. 33, Issue 7 https://doi.org/10.1016/j.tibs.2008.04.012	journal	July 2008
Endo-β-1,4-xylanase families: differences in catalytic properties Biely, P.; Vršanská, M.; Tenkanen, M. Journal of Biotechnology, Vol. 57, Issue 1-3 https://doi.org/10.1016/S0168-1656(97)00096-5	journal	September 1997
Prediction of lipoprotein signal peptides in Gram-negative bacteria Juncker, Agnieszka S.; Willenbrock, Hanni; von Heijne, Gunnar Protein Science, Vol. 12, Issue 8 https://doi.org/10.1110/ps.0303703	journal	August 2003
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Cantarel, B. L.; Coutinho, P. M.; Rancurel, C. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn663	journal	January 2009
Structural and Biochemical Analysis of Cellvibrio japonicus Xylanase 10C : HOW VARIATION IN SUBSTRATE-BINDING CLEFT INFLUENCES THE CATALYTIC PROFILE OF FAMILY GH-10 XYLANASES Pell, Gavin; Szabo, Lóránd; Charnock, Simon J. Journal of Biological Chemistry, Vol. 279, Issue 12 https://doi.org/10.1074/jbc.M311947200	journal	December 2003
Enzymatic assembly of DNA molecules up to several hundred kilobases Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan Nature Methods, Vol. 6, Issue 5, p. 343-345 https://doi.org/10.1038/nmeth.1318	journal	April 2009
Cloning, Characterization, and Functional Expression of the Klebsiella oxytoca Xylodextrin Utilization Operon (xynTB) in Escherichia coli Qian, Y.; Yomano, L. P.; Preston, J. F. Applied and Environmental Microbiology, Vol. 69, Issue 10, p. 5957-5967 https://doi.org/10.1128/AEM.69.10.5957-5967.2003	journal	October 2003
Proton-coupled sugar transport in the prototypical major facilitator superfamily protein XylE Wisedchaisri, Goragot; Park, Min-Sun; Iadanza, Matthew G. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5521	journal	August 2014
Bacteria engineered for fuel ethanol production: current status Dien, B. S.; Cotta, M. A.; Jeffries, T. W. Applied Microbiology and Biotechnology, Vol. 63, Issue 3, p. 258-266 https://doi.org/10.1007/s00253-003-1444-y	journal	December 2003
Xylan degradation, a metabolic property shared by rumen and human colonic Bacteroidetes: Xylan degradation by gut Bacteroidetes Dodd, Dylan; Mackie, Roderick I.; Cann, Isaac K. O. Molecular Microbiology, Vol. 79, Issue 2 https://doi.org/10.1111/j.1365-2958.2010.07473.x	journal	December 2010
Solutions to the Public Goods Dilemma in Bacterial Biofilms Drescher, Knut; Nadell, Carey D.; Stone, Howard A. Current Biology, Vol. 24, Issue 1 https://doi.org/10.1016/j.cub.2013.10.030	journal	January 2014
A survey of best practices for RNA-seq data analysis Conesa, Ana; Madrigal, Pedro; Tarazona, Sonia Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-0881-8	journal	January 2016
Microbial contributions to climate change through carbon cycle feedbacks Bardgett, Richard D.; Freeman, Chris; Ostle, Nicholas J. The ISME Journal, Vol. 2, Issue 8 https://doi.org/10.1038/ismej.2008.58	journal	July 2008
Comparative Phenotype and Genome Analysis of Cellvibrio sp. PR1, a Xylanolytic and Agarolytic Bacterium from the Pearl River Xie, Zhangzhang; Lin, Weitie; Luo, Jianfei BioMed Research International, Vol. 2017, p. 1-10 https://doi.org/10.1155/2017/6304248	journal	January 2017
Microbial Cellulose Utilization: Fundamentals and Biotechnology Lynd, L. R.; Weimer, P. J.; van Zyl, W. H. Microbiology and Molecular Biology Reviews, Vol. 66, Issue 3, p. 506-577 https://doi.org/10.1128/MMBR.66.3.506-577.2002	journal	September 2002
Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl8 and pUC19 vectors Yanisch-Perron, Celeste; Vieira, Jeffrey; Messing, Joachim Gene, Vol. 33, Issue 1 https://doi.org/10.1016/0378-1119(85)90120-9	journal	January 1985
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
Pseudomonas cellulosa expresses a single membrane-bound glycoside hydrolase family 51 arabinofuranosidase Beylot, Marie-Helene; Emami, Kaveh; McKIE, Vincent A. Biochemical Journal, Vol. 358, Issue 3 https://doi.org/10.1042/bj3580599	journal	September 2001
Insights into the mechanism of enzymatic hydrolysis of xylan Moreira, L. R. S.; Filho, E. X. F. Applied Microbiology and Biotechnology, Vol. 100, Issue 12 https://doi.org/10.1007/s00253-016-7555-z	journal	April 2016
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
Structural and Functional Analysis of a Lytic Polysaccharide Monooxygenase Important for Efficient Utilization of Chitin in Cellvibrio japonicus Forsberg, Zarah; Nelson, Cassandra E.; Dalhus, Bjørn Journal of Biological Chemistry, Vol. 291, Issue 14 https://doi.org/10.1074/jbc.M115.700161	journal	February 2016
Lysogeny at Mid-Twentieth Century: P1, P2, and Other Experimental Systems Bertani, G. Journal of Bacteriology, Vol. 186, Issue 3 https://doi.org/10.1128/JB.186.3.595-600.2004	journal	January 2004
Insights into Plant Cell Wall Degradation from the Genome Sequence of the Soil Bacterium Cellvibrio japonicus DeBoy, R. T.; Mongodin, E. F.; Fouts, D. E. Journal of Bacteriology, Vol. 190, Issue 15, p. 5455-5463 https://doi.org/10.1128/JB.01701-07	journal	June 2008
Genome analyses highlight the different biological roles of cellulases Medie, Felix Mba; Davies, Gideon J.; Drancourt, Michel Nature Reviews Microbiology, Vol. 10, Issue 3 https://doi.org/10.1038/nrmicro2729	journal	January 2012
Regulation of the Xylan-degrading Apparatus of Cellvibrio japonicus by a Novel Two-component System Emami, Kaveh; Topakas, Evangelos; Nagy, Tibor Journal of Biological Chemistry, Vol. 284, Issue 2 https://doi.org/10.1074/jbc.M805100200	journal	October 2008
Dividing the Large Glycoside Hydrolase Family 43 into Subfamilies: a Motivation for Detailed Enzyme Characterization Mewis, Keith; Lenfant, Nicolas; Lombard, Vincent Applied and Environmental Microbiology, Vol. 82, Issue 6 https://doi.org/10.1128/AEM.03453-15	journal	January 2016
Systems biology defines the biological significance of redox‐active proteins during cellulose degradation in an aerobic bacterium Gardner, Jeffrey G.; Crouch, Lucy; Labourel, Aurore Molecular Microbiology, Vol. 94, Issue 5 https://doi.org/10.1111/mmi.12821	journal	October 2014
Requirement of the Type II Secretion System for Utilization of Cellulosic Substrates by Cellvibrio japonicus Gardner, J. G.; Keating, D. H. Applied and Environmental Microbiology, Vol. 76, Issue 15 https://doi.org/10.1128/AEM.00454-10	journal	June 2010
Towards enzymatic breakdown of complex plant xylan structures: State of the art Biely, Peter; Singh, Suren; Puchart, Vladimír Biotechnology Advances, Vol. 34, Issue 7 https://doi.org/10.1016/j.biotechadv.2016.09.001	journal	November 2016
Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans Figurski, D. H.; Helinski, D. R. Proceedings of the National Academy of Sciences, Vol. 76, Issue 4 https://doi.org/10.1073/pnas.76.4.1648	journal	April 1979
Evidence for Temporal Regulation of the Two Pseudomonas cellulosa Xylanases Belonging to Glycoside Hydrolase Family 11 Emami, K.; Nagy, T.; Fontes, C. M. G. A. Journal of Bacteriology, Vol. 184, Issue 15 https://doi.org/10.1128/JB.184.15.4124-4133.2002	journal	August 2002
TCDB: the Transporter Classification Database for membrane transport protein analyses and information Saier, M. H. Nucleic Acids Research, Vol. 34, Issue 90001 https://doi.org/10.1093/nar/gkj001	journal	January 2006
Structural determinants of the substrate specificities of xylanases from different glycoside hydrolase families Pollet, Annick; Delcour, Jan A.; Courtin, Christophe M. Critical Reviews in Biotechnology, Vol. 30, Issue 3 https://doi.org/10.3109/07388551003645599	journal	March 2010
Transcriptomic analysis of Clostridium thermocellum ATCC 27405 cellulose fermentation Raman, Babu; McKeown, Catherine K; Rodriguez, Miguel BMC Microbiology, Vol. 11, Issue 1, Article No. 134 https://doi.org/10.1186/1471-2180-11-134	journal	January 2011
Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum Schäfer, Andreas; Tauch, Andreas; Jäger, Wolfgang Gene, Vol. 145, Issue 1, p. 69-73 https://doi.org/10.1016/0378-1119(94)90324-7	journal	July 1994
Polysaccharide degradation systems of the saprophytic bacterium Cellvibrio japonicus Gardner, Jeffrey G. World Journal of Microbiology and Biotechnology, Vol. 32, Issue 7 https://doi.org/10.1007/s11274-016-2068-6	journal	June 2016
How the walls come crumbling down: recent structural biochemistry of plant polysaccharide degradation Gilbert, H.; Stalbrand, H.; Brumer, H. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.03.004	journal	June 2008
Custom fabrication of biomass containment devices using 3-D printing enables bacterial growth analyses with complex insoluble substrates Nelson, Cassandra E.; Beri, Nina R.; Gardner, Jeffrey G. Journal of Microbiological Methods, Vol. 130 https://doi.org/10.1016/j.mimet.2016.09.013	journal	November 2016
Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes Levasseur, Anthony; Drula, Elodie; Lombard, Vincent Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41 https://doi.org/10.1186/1754-6834-6-41	journal	January 2013
Pseudomonas cellulosa expresses a single membrane-bound glycoside hydrolase family 51 arabinofuranosidase Beylot, Marie-Helene; Emami, Kaveh; McKIE, Vincent A. Biochemical Journal, Vol. 358, Issue 3 https://doi.org/10.1042/0264-6021:3580599	journal	September 2001
Solutions to the public goods dilemma in bacterial biofilms Drescher, Knut; Nadell, Carey D.; Stone, Howard A. Cell Press https://doi.org/10.5451/unibas-ep83562	text	January 2014

Cited By (3)

Complete Genome Sequences of Cellvibrio japonicus Strains with Improved Growth When Using α-Diglucosides Garcia, Cecelia A.; Narrett, Jackson A.; Gardner, Jeffrey G. Microbiology Resource Announcements, Vol. 8, Issue 44 https://doi.org/10.1128/mra.01077-19	journal	October 2019
Two forms of phosphomannomutase in gammaproteobacteria: The overlooked membrane‐bound form of AlgC is required for twitching motility of Lysobacter enzymogenes Qian, Guoliang; Fei, Shifang; Galperin, Michael Y. Environmental Microbiology, Vol. 21, Issue 11 https://doi.org/10.1111/1462-2920.14615	journal	May 2019
High-throughput screening of environmental polysaccharide-degrading bacteria using biomass containment and complex insoluble substrates Monge, Estela C.; Levi, Marios; Forbin, Joseph N. Applied Microbiology and Biotechnology, Vol. 104, Issue 8 https://doi.org/10.1007/s00253-020-10469-3	journal	February 2020

Figures / Tables (7)

Fig. 1. C. japonicus CAZyme genes up-regulated during exponential growth using xylan.(p. 30)

Fig. 2. Secreted CAZymes are required for arabinoxylan utilization in C. japonicus.(p. 31)

Fig. 3. The Xyn11A and Xyn11B endo-xylanases are required for arabinoxylan utilization in C. japonicus.(p. 33)

Similar Records

Efficient chito–oligosaccharide utilization requires two TonB–dependent transporters and one hexosaminidase in Cellvibrio japonicus

Journal Article · Thu Mar 18 00:00:00 EDT 2021 · Molecular Microbiology · OSTI ID:1415270

Monge, Estela C.; Gardner, Jeffrey G.

Galactomannan utilization by Cellvibrio japonicus relies on a single essential α‐galactosidase encoded by the aga27A gene

Journal Article · Fri Jan 20 00:00:00 EST 2023 · Molecular Microbiology · OSTI ID:1415270

Novak, Jessica K.; Gardner, Jeffrey G.

Trehalose Degradation by Cellvibrio japonicus Exhibits No Functional Redundancy and Is Solely Dependent on the Tre37A Enzyme

Journal Article · Wed Oct 28 00:00:00 EDT 2020 · Applied and Environmental Microbiology · OSTI ID:1415270

Garcia, Cecelia A.; Narrett, Jackson A.; Gardner, Jeffrey G.

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
β-xylosidase
Cellvibrio japonicus
polysaccharide degradation
xylan
xylanase