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Title: Alpha‐ and beta‐mannan utilization by marine Bacteroidetes

Abstract

Summary Marine microscopic algae carry out about half of the global carbon dioxide fixation into organic matter. They provide organic substrates for marine microbes such as members of the Bacteroidetes that degrade algal polysaccharides using carbohydrate‐active enzymes (CAZymes). In Bacteroidetes genomes CAZyme encoding genes are mostly grouped in distinct regions termed polysaccharide utilization loci (PULs). While some studies have shown involvement of PULs in the degradation of algal polysaccharides, the specific substrates are for the most part still unknown. We investigated four marine Bacteroidetes isolated from the southern North Sea that harbour putative mannan‐specific PULs. These PULs are similarly organized as PULs in human gut Bacteroides that digest α‐ and β‐mannans from yeasts and plants respectively. Using proteomics and defined growth experiments with polysaccharides as sole carbon sources we could show that the investigated marine Bacteroidetes express the predicted functional proteins required for α‐ and β‐mannan degradation. Our data suggest that algal mannans play an as yet unknown important role in the marine carbon cycle, and that biochemical principles established for gut or terrestrial microbes also apply to marine bacteria, even though their PULs are evolutionarily distant.

Authors:
 [1];  [2];  [3];  [4];  [3];  [5];  [4];  [4];  [6];  [7];  [4];  [2]; ORCiD logo [3];  [4]
  1. Max Planck Institute for Marine Microbiology Bremen Germany, Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology of China Institute of Hydrobiology, Chinese Academy of Sciences Wuhan China, University of Chinese Academy of Sciences Beijing China, College of Ocean Hebei Agricultural University Qinhuangdao China
  2. Max Planck Institute for Marine Microbiology Bremen Germany, MARUM, Center for Marine Environmental Sciences University of Bremen Bremen Germany
  3. Pharmaceutical Biotechnology Institute of Pharmacy, University Greifswald Greifswald Germany, Institute of Marine Biotechnology Greifswald Germany
  4. Max Planck Institute for Marine Microbiology Bremen Germany
  5. MARUM, Center for Marine Environmental Sciences University of Bremen Bremen Germany
  6. Institute of Microbiology University Greifswald Greifswald Germany
  7. Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology of China Institute of Hydrobiology, Chinese Academy of Sciences Wuhan China
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1477889
Alternate Identifier(s):
OSTI ID: 1477890
Grant/Contract Number:  
DE‐AC02‐05CH11231
Resource Type:
Published Article
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Name: Environmental Microbiology Journal Volume: 20 Journal Issue: 11; Journal ID: ISSN 1462-2912
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Chen, Jing, Robb, Craig S., Unfried, Frank, Kappelmann, Lennart, Markert, Stephanie, Song, Tao, Harder, Jens, Avcı, Burak, Becher, Dörte, Xie, Ping, Amann, Rudolf I., Hehemann, Jan‐Hendrik, Schweder, Thomas, and Teeling, Hanno. Alpha‐ and beta‐mannan utilization by marine Bacteroidetes. United Kingdom: N. p., 2018. Web. doi:10.1111/1462-2920.14414.
Chen, Jing, Robb, Craig S., Unfried, Frank, Kappelmann, Lennart, Markert, Stephanie, Song, Tao, Harder, Jens, Avcı, Burak, Becher, Dörte, Xie, Ping, Amann, Rudolf I., Hehemann, Jan‐Hendrik, Schweder, Thomas, & Teeling, Hanno. Alpha‐ and beta‐mannan utilization by marine Bacteroidetes. United Kingdom. https://doi.org/10.1111/1462-2920.14414
Chen, Jing, Robb, Craig S., Unfried, Frank, Kappelmann, Lennart, Markert, Stephanie, Song, Tao, Harder, Jens, Avcı, Burak, Becher, Dörte, Xie, Ping, Amann, Rudolf I., Hehemann, Jan‐Hendrik, Schweder, Thomas, and Teeling, Hanno. Tue . "Alpha‐ and beta‐mannan utilization by marine Bacteroidetes". United Kingdom. https://doi.org/10.1111/1462-2920.14414.
@article{osti_1477889,
title = {Alpha‐ and beta‐mannan utilization by marine Bacteroidetes},
author = {Chen, Jing and Robb, Craig S. and Unfried, Frank and Kappelmann, Lennart and Markert, Stephanie and Song, Tao and Harder, Jens and Avcı, Burak and Becher, Dörte and Xie, Ping and Amann, Rudolf I. and Hehemann, Jan‐Hendrik and Schweder, Thomas and Teeling, Hanno},
abstractNote = {Summary Marine microscopic algae carry out about half of the global carbon dioxide fixation into organic matter. They provide organic substrates for marine microbes such as members of the Bacteroidetes that degrade algal polysaccharides using carbohydrate‐active enzymes (CAZymes). In Bacteroidetes genomes CAZyme encoding genes are mostly grouped in distinct regions termed polysaccharide utilization loci (PULs). While some studies have shown involvement of PULs in the degradation of algal polysaccharides, the specific substrates are for the most part still unknown. We investigated four marine Bacteroidetes isolated from the southern North Sea that harbour putative mannan‐specific PULs. These PULs are similarly organized as PULs in human gut Bacteroides that digest α‐ and β‐mannans from yeasts and plants respectively. Using proteomics and defined growth experiments with polysaccharides as sole carbon sources we could show that the investigated marine Bacteroidetes express the predicted functional proteins required for α‐ and β‐mannan degradation. Our data suggest that algal mannans play an as yet unknown important role in the marine carbon cycle, and that biochemical principles established for gut or terrestrial microbes also apply to marine bacteria, even though their PULs are evolutionarily distant.},
doi = {10.1111/1462-2920.14414},
journal = {Environmental Microbiology},
number = 11,
volume = 20,
place = {United Kingdom},
year = {Tue Oct 16 00:00:00 EDT 2018},
month = {Tue Oct 16 00:00:00 EDT 2018}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1111/1462-2920.14414

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Cited by: 16 works
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Works referenced in this record:

Biochemical Analysis of Thermotoga maritima GH36 α-Galactosidase (Tm GalA) Confirms the Mechanistic Commonality of Clan GH-D Glycoside Hydrolases
journal, March 2007

  • Comfort, Donald A.; Bobrov, Kirill S.; Ivanen, Dina R.
  • Biochemistry, Vol. 46, Issue 11, p. 3319-3330
  • DOI: 10.1021/bi061521n

N-Acetylglucosamine Recognition by a Family 32 Carbohydrate-Binding Module from Clostridium perfringens NagH
journal, July 2009

  • Ficko-Blean, Elizabeth; Boraston, Alisdair B.
  • Journal of Molecular Biology, Vol. 390, Issue 2
  • DOI: 10.1016/j.jmb.2009.04.066

Genomes OnLine Database (GOLD) v.6: data updates and feature enhancements
journal, October 2016

  • Mukherjee, Supratim; Stamatis, Dimitri; Bertsch, Jon
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw992

Hemicelluloses
journal, June 2010


Discovery of β-1,4-d-Mannosyl- N -acetyl-d-glucosamine Phosphorylase Involved in the Metabolism of N -Glycans
journal, August 2013

  • Nihira, Takanori; Suzuki, Erika; Kitaoka, Motomitsu
  • Journal of Biological Chemistry, Vol. 288, Issue 38
  • DOI: 10.1074/jbc.M113.469080

Niches of two polysaccharide-degrading Polaribacter isolates from the North Sea during a spring diatom bloom
journal, December 2014

  • Xing, Peng; Hahnke, Richard L.; Unfried, Frank
  • The ISME Journal, Vol. 9, Issue 6
  • DOI: 10.1038/ismej.2014.225

A β-mannan utilization locus in Bacteroides ovatus involves a GH36 α-galactosidase active on galactomannans
journal, June 2016

  • Reddy, Sumitha K.; Bågenholm, Viktoria; Pudlo, Nicholas A.
  • FEBS Letters, Vol. 590, Issue 14
  • DOI: 10.1002/1873-3468.12250

Biochemical and Structural Characterization of the Complex Agarolytic Enzyme System from the Marine Bacterium Zobellia galactanivorans
journal, July 2012

  • Hehemann, Jan-Hendrik; Correc, Gaëlle; Thomas, François
  • Journal of Biological Chemistry, Vol. 287, Issue 36
  • DOI: 10.1074/jbc.M112.377184

Systems-wide temporal proteomic profiling in glucose-starved Bacillus subtilis
journal, December 2010

  • Otto, Andreas; Bernhardt, Jörg; Meyer, Hanna
  • Nature Communications, Vol. 1, Issue 1
  • DOI: 10.1038/ncomms1137

genoPlotR: comparative gene and genome visualization in R
journal, July 2010


Structural characterization of a branched (1 → 6)-α-mannan and β-glucans isolated from the fruiting bodies of Cantharellus cibarius
journal, August 2016


Sulfated Polysaccharides in Red and Brown Algae
journal, June 1979


Adaptive mechanisms that provide competitive advantages to marine bacteroidetes during microalgal blooms
journal, July 2018


Relevance of seed polysaccharides and flavonoids for the classification of the leguminosae: A chemotaxonomic approach
journal, August 1993


Structural and biochemical characterization of the laminarinase Zg LamC GH16 from Zobellia galactanivorans suggests preferred recognition of branched laminarin
journal, January 2015

  • Labourel, Aurore; Jam, Murielle; Legentil, Laurent
  • Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 2
  • DOI: 10.1107/S139900471402450X

Dilution cultivation of marine heterotrophic bacteria abundant after a spring phytoplankton bloom in the North Sea: Isolation of abundant bacteria linked to a diatom bloom
journal, May 2014

  • Hahnke, Richard L.; Bennke, Christin M.; Fuchs, Bernhard M.
  • Environmental Microbiology, Vol. 17, Issue 10
  • DOI: 10.1111/1462-2920.12479

Galactomannan structure and β-mannanase and β-mannosidase activity in germinating legume seeds
journal, June 1975


Molecular characteristics and biological activities of anionic macromolecules from Codium fragile
journal, August 2013

  • Tabarsa, Mehdi; Karnjanapratum, Supatra; Cho, MyoungLae
  • International Journal of Biological Macromolecules, Vol. 59
  • DOI: 10.1016/j.ijbiomac.2013.04.022

Specificity of Polysaccharide Use in Intestinal Bacteroides Species Determines Diet-Induced Microbiota Alterations
journal, June 2010


Characterization of a novel GH2 family α-l-arabinofuranosidase from hyperthermophilic bacterium Thermotoga thermarum
journal, February 2014


Blue silver: A very sensitive colloidal Coomassie G-250 staining for proteome analysis
journal, May 2004

  • Candiano, Giovanni; Bruschi, Maurizio; Musante, Luca
  • ELECTROPHORESIS, Vol. 25, Issue 9
  • DOI: 10.1002/elps.200305844

Diverse patterns of cell wall mannan/galactomannan occurrence in seeds of the Leguminosae
journal, January 2013

  • Bento, João Francisco; Mazzaro, Irineu; de Almeida Silva, Lia Magalhães
  • Carbohydrate Polymers, Vol. 92, Issue 1
  • DOI: 10.1016/j.carbpol.2012.08.113

An overview of mannan structure and mannan-degrading enzyme systems
journal, April 2008


New structural insights into the cell-wall polysaccharide of the diatom Phaeodactylum tricornutum
journal, September 2017


Recurring patterns in bacterioplankton dynamics during coastal spring algae blooms
journal, April 2016

  • Teeling, Hanno; Fuchs, Bernhard M.; Bennke, Christin M.
  • eLife, Vol. 5
  • DOI: 10.7554/eLife.11888

Evaluation of reference genes for real-time quantitative PCR in the marine flavobacterium Zobellia galactanivorans
journal, January 2011

  • Thomas, François; Barbeyron, Tristan; Michel, Gurvan
  • Journal of Microbiological Methods, Vol. 84, Issue 1
  • DOI: 10.1016/j.mimet.2010.10.016

Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria
journal, November 2017

  • Ficko-Blean, Elizabeth; Préchoux, Aurélie; Thomas, François
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/s41467-017-01832-6

Enzymatic cell wall degradation of Chlorella vulgaris and other microalgae for biofuels production
journal, September 2012


Localization of ?-galactomannan on the surface of Schizosaccharomyces pombe cells by scanning electron microscopy
journal, January 1977

  • Horisberger, Marc; Rosset, Jacqueline
  • Archives of Microbiology, Vol. 112, Issue 2
  • DOI: 10.1007/BF00429323

Prediction of lipoprotein signal peptides in Gram-negative bacteria
journal, August 2003

  • Juncker, Agnieszka S.; Willenbrock, Hanni; von Heijne, Gunnar
  • Protein Science, Vol. 12, Issue 8
  • DOI: 10.1110/ps.0303703

Microbial Stress-Response Physiology and its Implications for Ecosystem Function
journal, June 2007

  • Schimel, Joshua; Balser, Teri C.; Wallenstein, Matthew
  • Ecology, Vol. 88, Issue 6
  • DOI: 10.1890/06-0219

RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006


Deciphering ocean carbon in a changing world
journal, March 2016

  • Moran, Mary Ann; Kujawinski, Elizabeth B.; Stubbins, Aron
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 12
  • DOI: 10.1073/pnas.1514645113

Secretion of Bacterial Lipoproteins: Through the Cytoplasmic Membrane, the Periplasm and Beyond
journal, August 2014


Phylogenetic diversity of Flavobacteria isolated from the North Sea on solid media
journal, October 2013


Polysaccharide utilisation loci of Bacteroidetes from two contrasting open ocean sites in the North Atlantic
journal, July 2016

  • Bennke, Christin M.; Krüger, Karen; Kappelmann, Lennart
  • Environmental Microbiology, Vol. 18, Issue 12
  • DOI: 10.1111/1462-2920.13429

SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes
journal, May 2012


The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

Identification and Characterization of a Novel Periplasmic Polygalacturonic Acid Binding Protein from Yersinia enterolitica
journal, April 2007

  • Abbott, D. Wade; Hrynuik, Susanne; Boraston, Alisdair B.
  • Journal of Molecular Biology, Vol. 367, Issue 4
  • DOI: 10.1016/j.jmb.2007.01.030

The β-Glucanase Zg LamA from Zobellia galactanivorans Evolved a Bent Active Site Adapted for Efficient Degradation of Algal Laminarin
journal, December 2013

  • Labourel, Aurore; Jam, Murielle; Jeudy, Alexandra
  • Journal of Biological Chemistry, Vol. 289, Issue 4
  • DOI: 10.1074/jbc.M113.538843

Analysis of a New Family of Widely Distributed Metal-independent α-Mannosidases Provides Unique Insight into the Processing of N -Linked Glycans
journal, March 2011

  • Gregg, Katie J.; Zandberg, Wesley F.; Hehemann, Jan-Hendrik
  • Journal of Biological Chemistry, Vol. 286, Issue 17
  • DOI: 10.1074/jbc.M111.223172

An acetylated galactoglucomannan from Picea abies L. Karst
journal, June 2002


Acetylation and characterization of spruce (Picea abies) galactoglucomannans
journal, April 2010


Preliminary Studies on the Synthesis of Polysaccharides in the Algae
journal, October 1951


The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013

  • Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1178

The Cellvibrio japonicus Mannanase Cj Man26C Displays a Unique exo -Mode of Action That Is Conferred by Subtle Changes to the Distal Region of the Active Site
journal, September 2008

  • Cartmell, Alan; Topakas, Evangelos; Ducros, Valérie M-A.
  • Journal of Biological Chemistry, Vol. 283, Issue 49
  • DOI: 10.1074/jbc.M804053200

Polysaccharide utilization loci of North Sea Flavobacteriia as basis for using SusC/D-protein expression for predicting major phytoplankton glycans
journal, August 2018

  • Kappelmann, Lennart; Krüger, Karen; Hehemann, Jan-Hendrik
  • The ISME Journal, Vol. 13, Issue 1
  • DOI: 10.1038/s41396-018-0242-6

Complex pectin metabolism by gut bacteria reveals novel catalytic functions
journal, March 2017

  • Ndeh, Didier; Rogowski, Artur; Cartmell, Alan
  • Nature, Vol. 544, Issue 7648
  • DOI: 10.1038/nature21725

Statistical Analysis of Membrane Proteome Expression Changes in Saccharomyces c erevisiae
journal, September 2006

  • Zybailov, Boris; Mosley, Amber L.; Sardiu, Mihaela E.
  • Journal of Proteome Research, Vol. 5, Issue 9
  • DOI: 10.1021/pr060161n

Isolation of Marine Bacteria Capable of Producing Specific Lyases for Alginate Degradation
journal, September 1982


The system of sulfated α-(1 → 3)-linked d-mannans from the red seaweed Nothogenia fastigiata: Structures, antiherpetic and anticoagulant properties
journal, October 1997


Substrate-Controlled Succession of Marine Bacterioplankton Populations Induced by a Phytoplankton Bloom
journal, May 2012


Galactomannan Catabolism Conferred by a Polysaccharide Utilization Locus of Bacteroides ovatus : ENZYME SYNERGY AND CRYSTAL STRUCTURE OF A β-MANNANASE
journal, November 2016

  • Bågenholm, Viktoria; Reddy, Sumitha K.; Bouraoui, Hanene
  • Journal of Biological Chemistry, Vol. 292, Issue 1
  • DOI: 10.1074/jbc.M116.746438

Mechanistic insights into a Ca2+-dependent family of α-mannosidases in a human gut symbiont
journal, December 2009

  • Zhu, Yanping; Suits, Michael D. L.; Thompson, Andrew J.
  • Nature Chemical Biology, Vol. 6, Issue 2
  • DOI: 10.1038/nchembio.278

A new arabinomannan from the cell wall of the chlorococcal algae Chlorella vulgaris
journal, May 2012


The mannobiose-forming exo-mannanase involved in a new mannan catabolic pathway in Bacteroides fragilis
journal, November 2013

  • Kawaguchi, Kazuki; Senoura, Takeshi; Ito, Shigeaki
  • Archives of Microbiology, Vol. 196, Issue 1
  • DOI: 10.1007/s00203-013-0938-y

The Mnn2 Mannosyltransferase Family Modulates Mannoprotein Fibril Length, Immune Recognition and Virulence of Candida albicans
journal, April 2013


Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism
journal, January 2015

  • Cuskin, Fiona; Lowe, Elisabeth C.; Temple, Max J.
  • Nature, Vol. 517, Issue 7533
  • DOI: 10.1038/nature13995

Domains in plexins: links to integrins and transcription factors
journal, July 1999


Functional characterization of polysaccharide utilization loci in the marine Bacteroidetes ‘Gramella forsetii’ KT0803
journal, February 2014

  • Kabisch, Antje; Otto, Andreas; König, Sten
  • The ISME Journal, Vol. 8, Issue 7
  • DOI: 10.1038/ismej.2014.4

N-glycan structure dictates extension of protein folding or onset of disposal
journal, May 2007


The Proteomics Identifications (PRIDE) database and associated tools: status in 2013
journal, November 2012

  • Vizcaíno, Juan Antonio; Côté, Richard G.; Csordas, Attila
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1262

Linear mannan in the endosperm of Schizolobium amazonicum
journal, February 2001


A minor, protein-containing galactomannan from a sodium carbonate extract of Cordyceps sinensis
journal, November 1986