skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: In marine Bacteroidetes the bulk of glycan degradation during algae blooms is mediated by few clades using a restricted set of genes

Abstract

We investigated Bacteroidetes during spring algae blooms in the southern North Sea in 2010–2012 using a time series of 38 deeply sequenced metagenomes. Initial partitioning yielded 6455 bins, from which we extracted 3101 metagenome-assembled genomes (MAGs) including 1286 Bacteroidetes MAGs covering ~120 mostly uncultivated species. We identified 13 dominant, recurrent Bacteroidetes clades carrying a restricted set of conserved polysaccharide utilization loci (PULs) that likely mediate the bulk of bacteroidetal algal polysaccharide degradation. The majority of PULs were predicted to target the diatom storage polysaccharide laminarin, alpha-glucans, alpha-mannose-rich substrates, and sulfated xylans. Metaproteomics at 14 selected points in time revealed expression of SusC-like proteins from PULs targeting all of these substrates. Analyses of abundant key players and their PUL repertoires over time furthermore suggested that fewer and simpler polysaccharides dominated early bloom stages, and that more complex polysaccharides became available as blooms progressed.

Authors:
ORCiD logo [1];  [1];  [1];  [2]; ORCiD logo [3]; ORCiD logo [4];  [1];  [1]
  1. Max Planck Inst. for Marine Microbiology, Bremen (Germany)
  2. USDOE Joint Genome Inst. (JGI), Walnut Creek, CA (United States)
  3. Univ. Greifswald (Germany)
  4. Univ. Greifswald (Germany); Inst. of Marine Biotechnology, Greifswald (Germany)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); USDOE Joint Genome Inst. (JGI), Walnut Creek, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Max Planck Society; German Research Foundation (DFG)
OSTI Identifier:
1624027
Grant/Contract Number:  
AC02-05CH11231; AM 73/9-1; TE 813/2-1; BE 3869/4-1; SCHW 595/10-1
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 13; Journal Issue: 11; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Environmental Sciences & Ecology; Microbiology; Biodiversity; Metagenomics; Microbial Ecology; Proteomics

Citation Formats

Krüger, Karen, Chafee, Meghan, Francis, T. Ben, Glavina del Rio, Tijana, Becher, Dörte, Schweder, Thomas, Amann, Rudolf I., and Teeling, Hanno. In marine Bacteroidetes the bulk of glycan degradation during algae blooms is mediated by few clades using a restricted set of genes. United States: N. p., 2019. Web. https://doi.org/10.1038/s41396-019-0476-y.
Krüger, Karen, Chafee, Meghan, Francis, T. Ben, Glavina del Rio, Tijana, Becher, Dörte, Schweder, Thomas, Amann, Rudolf I., & Teeling, Hanno. In marine Bacteroidetes the bulk of glycan degradation during algae blooms is mediated by few clades using a restricted set of genes. United States. https://doi.org/10.1038/s41396-019-0476-y
Krüger, Karen, Chafee, Meghan, Francis, T. Ben, Glavina del Rio, Tijana, Becher, Dörte, Schweder, Thomas, Amann, Rudolf I., and Teeling, Hanno. Wed . "In marine Bacteroidetes the bulk of glycan degradation during algae blooms is mediated by few clades using a restricted set of genes". United States. https://doi.org/10.1038/s41396-019-0476-y. https://www.osti.gov/servlets/purl/1624027.
@article{osti_1624027,
title = {In marine Bacteroidetes the bulk of glycan degradation during algae blooms is mediated by few clades using a restricted set of genes},
author = {Krüger, Karen and Chafee, Meghan and Francis, T. Ben and Glavina del Rio, Tijana and Becher, Dörte and Schweder, Thomas and Amann, Rudolf I. and Teeling, Hanno},
abstractNote = {We investigated Bacteroidetes during spring algae blooms in the southern North Sea in 2010–2012 using a time series of 38 deeply sequenced metagenomes. Initial partitioning yielded 6455 bins, from which we extracted 3101 metagenome-assembled genomes (MAGs) including 1286 Bacteroidetes MAGs covering ~120 mostly uncultivated species. We identified 13 dominant, recurrent Bacteroidetes clades carrying a restricted set of conserved polysaccharide utilization loci (PULs) that likely mediate the bulk of bacteroidetal algal polysaccharide degradation. The majority of PULs were predicted to target the diatom storage polysaccharide laminarin, alpha-glucans, alpha-mannose-rich substrates, and sulfated xylans. Metaproteomics at 14 selected points in time revealed expression of SusC-like proteins from PULs targeting all of these substrates. Analyses of abundant key players and their PUL repertoires over time furthermore suggested that fewer and simpler polysaccharides dominated early bloom stages, and that more complex polysaccharides became available as blooms progressed.},
doi = {10.1038/s41396-019-0476-y},
journal = {The ISME Journal},
number = 11,
volume = 13,
place = {United States},
year = {2019},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 6 works
Citation information provided by
Web of Science

Figures / Tables:

Fig. 1 Fig. 1: a Maximum-likelihood tree of Mash-clusters based on concatenated marker proteins according to the GTDB-Tk genome phylogeny. Only Mash-clusters (mc) were included that contained at least two MAGs ≥70% completeness, plus additional 29 singleton MAGs with ≥70% completeness, and ≤10% contamination. Mash-clusters reaching high abundances (>5 RPKM at onemore » time-point or 38 RPKM at all time-points combined) during the sampling period are highlighted together with their taxonomic affiliations. Scale bar: mean number of amino acid substitutions per site. Outgroup: Oceanithermus profundus. b Violin plots of MAG assembly size distributions within clades of abundant Mash-clusters (colored areas). Area width corresponds to MAG numbers. Solid lines represent median and deciles, and dashed lines represent quartiles« less

Save / Share:

Works referenced in this record:

Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities
journal, October 2009

  • Andersson, Anders F.; Riemann, Lasse; Bertilsson, Stefan
  • The ISME Journal, Vol. 4, Issue 2
  • DOI: 10.1038/ismej.2009.108

Defining seasonal marine microbial community dynamics
journal, August 2011

  • Gilbert, Jack A.; Steele, Joshua A.; Caporaso, J. Gregory
  • The ISME Journal, Vol. 6, Issue 2
  • DOI: 10.1038/ismej.2011.107

Marine microbial community dynamics and their ecological interpretation
journal, February 2015

  • Fuhrman, Jed A.; Cram, Jacob A.; Needham, David M.
  • Nature Reviews Microbiology, Vol. 13, Issue 3
  • DOI: 10.1038/nrmicro3417

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

Recurrent patterns of microdiversity in a temperate coastal marine environment
journal, October 2017

  • Chafee, Meghan; Fernàndez-Guerra, Antonio; Buttigieg, Pier Luigi
  • The ISME Journal, Vol. 12, Issue 1
  • DOI: 10.1038/ismej.2017.165

Dynamics and interactions of highly resolved marine plankton via automated high-frequency sampling
journal, June 2018


Master recyclers: features and functions of bacteria associated with phytoplankton blooms
journal, August 2014

  • Buchan, Alison; LeCleir, Gary R.; Gulvik, Christopher A.
  • Nature Reviews Microbiology, Vol. 12, Issue 10
  • DOI: 10.1038/nrmicro3326

Production of carbohydrates by marine planktonic diatoms. I. Comparison of nine different species in culture
journal, July 1974


Diatom-Specific Oligosaccharide and Polysaccharide Structures Help to Unravel Biosynthetic Capabilities in Diatoms
journal, September 2015

  • Gügi, Bruno; Le Costaouec, Tinaïg; Burel, Carole
  • Marine Drugs, Vol. 13, Issue 9
  • DOI: 10.3390/md13095993

Mini-review: Phytoplankton-derived polysaccharides in the marine environment and their interactions with heterotrophic bacteria: Phytoplankton-derived polysaccharides
journal, August 2018

  • Mühlenbruch, Marco; Grossart, Hans-Peter; Eigemann, Falk
  • Environmental Microbiology, Vol. 20, Issue 8
  • DOI: 10.1111/1462-2920.14302

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


Functional Genomic and Metabolic Studies of the Adaptations of a Prominent Adult Human Gut Symbiont, Bacteroides thetaiotaomicron , to the Suckling Period
journal, September 2006

  • Bjursell, Magnus K.; Martens, Eric C.; Gordon, Jeffrey I.
  • Journal of Biological Chemistry, Vol. 281, Issue 47
  • DOI: 10.1074/jbc.M606509200

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

The evolution of cooperation within the gut microbiota
journal, April 2016

  • Rakoff-Nahoum, Seth; Foster, Kevin R.; Comstock, Laurie E.
  • Nature, Vol. 533, Issue 7602
  • DOI: 10.1038/nature17626

An alternative polysaccharide uptake mechanism of marine bacteria
journal, March 2017

  • Reintjes, Greta; Arnosti, Carol; Fuchs, Bernhard M.
  • The ISME Journal, Vol. 11, Issue 7
  • DOI: 10.1038/ismej.2017.26

Genetic evidence that outer membrane binding of starch is required for starch utilization by Bacteroides thetaiotaomicron.
journal, January 1989


Starch Catabolism by a Prominent Human Gut Symbiont Is Directed by the Recognition of Amylose Helices
journal, July 2008


Structural basis for nutrient acquisition by dominant members of the human gut microbiota
journal, January 2017

  • Glenwright, Amy J.; Pothula, Karunakar R.; Bhamidimarri, Satya P.
  • Nature, Vol. 541, Issue 7637
  • DOI: 10.1038/nature20828

SusE facilitates starch uptake independent of starch binding in B. thetaiotaomicron : SusE promotes starch uptake in
journal, April 2018

  • Foley, Matthew H.; Martens, Eric C.; Koropatkin, Nicole M.
  • Molecular Microbiology, Vol. 108, Issue 5
  • DOI: 10.1111/mmi.13949

Polysaccharide Utilization Loci: Fueling Microbial Communities
journal, January 2017

  • Grondin, Julie M.; Tamura, Kazune; Déjean, Guillaume
  • Journal of Bacteriology, Vol. 199, Issue 15
  • DOI: 10.1128/JB.00860-16

Metagenomics reveals functional synergy and novel polysaccharide utilization loci in the Castor canadensis fecal microbiome
journal, July 2018


Ninety-nine de novo assembled genomes from the moose (Alces alces) rumen microbiome provide new insights into microbial plant biomass degradation
journal, July 2017

  • Svartström, Olov; Alneberg, Johannes; Terrapon, Nicolas
  • The ISME Journal, Vol. 11, Issue 11
  • DOI: 10.1038/ismej.2017.108

Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota
journal, April 2010

  • Hehemann, Jan-Hendrik; Correc, Gaëlle; Barbeyron, Tristan
  • Nature, Vol. 464, Issue 7290
  • DOI: 10.1038/nature08937

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

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

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

Biochemical characterization of an ulvan lyase from the marine flavobacterium Formosa agariphila KMM 3901T
journal, June 2018

  • Reisky, Lukas; Stanetty, Christian; Mihovilovic, Marko D.
  • Applied Microbiology and Biotechnology, Vol. 102, Issue 16
  • DOI: 10.1007/s00253-018-9142-y

Genomic content of uncultured Bacteroidetes from contrasting oceanic provinces in the North Atlantic Ocean: Genomic content of uncultivated marine Bacteroidetes
journal, September 2011


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

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

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


Metagenome-assembled genomes uncover a global brackish microbiome
journal, December 2015


Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life
journal, September 2017

  • Parks, Donovan H.; Rinke, Christian; Chuvochina, Maria
  • Nature Microbiology, Vol. 2, Issue 11
  • DOI: 10.1038/s41564-017-0012-7

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


Binning metagenomic contigs by coverage and composition
journal, September 2014

  • Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino
  • Nature Methods, Vol. 11, Issue 11
  • DOI: 10.1038/nmeth.3103

Anvi’o: an advanced analysis and visualization platform for ‘omics data
journal, January 2015

  • Eren, A. Murat; Esen, Özcan C.; Quince, Christopher
  • PeerJ, Vol. 3
  • DOI: 10.7717/peerj.1319

Candidatus Prosiliicoccus vernus, a spring phytoplankton bloom associated member of the Flavobacteriaceae
journal, January 2019

  • Francis, T. Ben; Krüger, Karen; Fuchs, Bernhard M.
  • Systematic and Applied Microbiology, Vol. 42, Issue 1
  • DOI: 10.1016/j.syapm.2018.08.007

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Mash: fast genome and metagenome distance estimation using MinHash
journal, June 2016


A new genomic blueprint of the human gut microbiota
journal, February 2019


DNA–DNA hybridization values and their relationship to whole-genome sequence similarities
journal, January 2007

  • Klappenbach, Joel A.; Goris, Johan; Vandamme, Peter
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 1
  • DOI: 10.1099/ijs.0.64483-0

Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003


A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life
journal, August 2018

  • Parks, Donovan H.; Chuvochina, Maria; Waite, David W.
  • Nature Biotechnology, Vol. 36, Issue 10
  • DOI: 10.1038/nbt.4229

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016

  • Letunic, Ivica; Bork, Peer
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw290

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


Accelerated Profile HMM Searches
journal, October 2011


dbCAN: a web resource for automated carbohydrate-active enzyme annotation
journal, May 2012

  • Yin, Yanbin; Mao, Xizeng; Yang, Jincai
  • Nucleic Acids Research, Vol. 40, Issue W1
  • DOI: 10.1093/nar/gks479

Pfam: the protein families database
journal, November 2013

  • Finn, Robert D.; Bateman, Alex; Clements, Jody
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1223

TIGRFAMs and Genome Properties: tools for the assignment of molecular function and biological process in prokaryotic genomes
journal, January 2007

  • Selengut, J. D.; Haft, D. H.; Davidsen, T.
  • Nucleic Acids Research, Vol. 35, Issue Database
  • DOI: 10.1093/nar/gkl1043

Fast and sensitive protein alignment using DIAMOND
journal, November 2014

  • Buchfink, Benjamin; Xie, Chao; Huson, Daniel H.
  • Nature Methods, Vol. 12, Issue 1
  • DOI: 10.1038/nmeth.3176

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

Automatic prediction of polysaccharide utilization loci in Bacteroidetes species
journal, October 2014


PULDB: the expanded database of Polysaccharide Utilization Loci
journal, October 2017

  • Terrapon, Nicolas; Lombard, Vincent; Drula, Élodie
  • Nucleic Acids Research, Vol. 46, Issue D1
  • DOI: 10.1093/nar/gkx1022

MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013

  • Katoh, K.; Standley, D. M.
  • Molecular Biology and Evolution, Vol. 30, Issue 4
  • DOI: 10.1093/molbev/mst010

FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


metaSPAdes: a new versatile metagenomic assembler
journal, March 2017

  • Nurk, Sergey; Meleshko, Dmitry; Korobeynikov, Anton
  • Genome Research, Vol. 27, Issue 5
  • DOI: 10.1101/gr.213959.116

2016 update of the PRIDE database and its related tools
journal, September 2016

  • Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi
  • Nucleic Acids Research, Vol. 44, Issue 22
  • DOI: 10.1093/nar/gkw880

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Refinements to Label Free Proteome Quantitation: How to Deal with Peptides Shared by Multiple Proteins
journal, March 2010

  • Zhang, Ying; Wen, Zhihui; Washburn, Michael P.
  • Analytical Chemistry, Vol. 82, Issue 6
  • DOI: 10.1021/ac9023999

Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea
journal, August 2017

  • Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas
  • Nature Biotechnology, Vol. 35, Issue 8
  • DOI: 10.1038/nbt.3893

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


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

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

Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom
journal, February 2016


Seasonal microbial community dynamics correlate with phytoplankton-derived polysaccharides in surface coastal waters
journal, October 2013

  • Taylor, Joe D.; Cottingham, Samuel D.; Billinge, Jack
  • The ISME Journal, Vol. 8, Issue 1
  • DOI: 10.1038/ismej.2013.178

Draft Genome Sequence of Newly Isolated Agarolytic Bacteria Cellulophaga omnivescoria sp. nov. W5C Carrying Several Gene Loci for Marine Polysaccharide Degradation
journal, March 2018

  • Valdehuesa, Kris Niño G.; Ramos, Kristine Rose M.; Moron, Llewelyn S.
  • Current Microbiology, Vol. 75, Issue 7
  • DOI: 10.1007/s00284-018-1467-3

Assembling the Marine Metagenome, One Cell at a Time
journal, April 2009


Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean
journal, June 2013

  • Swan, B. K.; Tupper, B.; Sczyrba, A.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 28
  • DOI: 10.1073/pnas.1304246110

Combined Carbohydrates Support Rich Communities of Particle-Associated Marine Bacterioplankton
journal, January 2017


Reciprocal Prioritization to Dietary Glycans by Gut Bacteria in a Competitive Environment Promotes Stable Coexistence
journal, October 2017


Phylogenetically conserved resource partitioning in the coastal microbial loop
journal, August 2017


    Works referencing / citing this record:

    Short‐term changes in polysaccharide utilization mechanisms of marine bacterioplankton during a spring phytoplankton bloom
    journal, March 2020

    • Reintjes, Greta; Fuchs, Bernhard M.; Scharfe, Mirco
    • Environmental Microbiology, Vol. 22, Issue 5
    • DOI: 10.1111/1462-2920.14971

    A pipeline for targeted metagenomics of environmental bacteria
    journal, February 2020


      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.