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

Title: Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes

Abstract

Microbes are critical in carbon and nutrient cycling in freshwater ecosystems. Members of the Verrucomicrobiaare ubiquitous in such systems, and yet their roles and ecophysiology are not well understood. In this study, we recovered 19 Verrucomicrobia draft genomes by sequencing 184 time-series metagenomes from a eutrophic lake and a humic bog that differ in carbon source and nutrient availabilities. These genomes span four of the seven previously defined Verrucomicrobia subdivisions and greatly expand knowledge of the genomic diversity of freshwater Verrucomicrobia. Genome analysis revealed their potential role as (poly)saccharide degraders in freshwater, uncovered interesting genomic features for this lifestyle, and suggested their adaptation to nutrient availabilities in their environments. Verrucomicrobia populations differ significantly between the two lakes in glycoside hydrolase gene abundance and functional profiles, reflecting the autochthonous and terrestrially derived allochthonous carbon sources of the two ecosystems, respectively. Interestingly, a number of genomes recovered from the bog contained gene clusters that potentially encode a novel porin-multiheme cytochrome c complex and might be involved in extracellular electron transfer in the anoxic humus-rich environment. Notably, most epilimnion genomes have large numbers of so-called “ Planctomycete-specific” cytochrome c-encoding genes, which exhibited distribution patterns nearly opposite to those seen with glycoside hydrolase genes,more » probably associated with the different levels of environmental oxygen availability and carbohydrate complexity between lakes/layers. Overall, the recovered genomes represent a major step toward understanding the role, ecophysiology, and distribution of Verrucomicrobia in freshwater. Freshwater Verrucomicrobia spp. are cosmopolitan in lakes and rivers, and yet their roles and ecophysiology are not well understood, as cultured freshwater Verrucomicrobia spp. are restricted to one subdivision of this phylum. We greatly expanded the known genomic diversity of this freshwater lineage by recovering 19 Verrucomicrobia draft genomes from 184 metagenomes collected from a eutrophic lake and a humic bog across multiple years. Most of these genomes represent the first freshwater representatives of several Verrucomicrobia subdivisions. Genomic analysis revealed Verrucomicrobia to be potential (poly)saccharide degraders and suggested their adaptation to carbon sources of different origins in the two contrasting ecosystems. We identified putative extracellular electron transfer genes and so-called “ Planctomycete-specific” cytochrome c-encoding genes and identified their distinct distribution patterns between the lakes/layers. Overall, our analysis greatly advances the understanding of the function, ecophysiology, and distribution of freshwater Verrucomicrobia, while highlighting their potential role in freshwater carbon cycling.« less

Authors:
 [1];  [2];  [3];  [4];  [3];  [3];  [3]; ORCiD logo [5]
  1. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology and Dept. of Geoscience
  2. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Uppsala Univ. (Sweden). Limnology and Science for Life Lab. and Dept. of Ecology and Genetics
  5. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology and Dept. of Civil and Environmental Engineering
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Scientific User Facilities Division; USDA National Inst. of Food and Agriculture (NIFA); National Science Foundation (NSF)
OSTI Identifier:
1459395
Grant/Contract Number:  
AC02-05CH11231; MCB-0702395; NTL-LTER DEB-1440297; DEB-1344254; 1002996
Resource Type:
Accepted Manuscript
Journal Name:
mSphere
Additional Journal Information:
Journal Volume: 2; Journal Issue: 5; Journal ID: ISSN 2379-5042
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

He, Shaomei, Stevens, Sarah L. R., Chan, Leong-Keat, Bertilsson, Stefan, Glavina del Rio, Tijana, Tringe, Susannah G., Malmstrom, Rex R., and McMahon, Katherine D. Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes. United States: N. p., 2017. Web. doi:10.1128/mSphere.00277-17.
He, Shaomei, Stevens, Sarah L. R., Chan, Leong-Keat, Bertilsson, Stefan, Glavina del Rio, Tijana, Tringe, Susannah G., Malmstrom, Rex R., & McMahon, Katherine D. Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes. United States. doi:10.1128/mSphere.00277-17.
He, Shaomei, Stevens, Sarah L. R., Chan, Leong-Keat, Bertilsson, Stefan, Glavina del Rio, Tijana, Tringe, Susannah G., Malmstrom, Rex R., and McMahon, Katherine D. Wed . "Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes". United States. doi:10.1128/mSphere.00277-17. https://www.osti.gov/servlets/purl/1459395.
@article{osti_1459395,
title = {Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes},
author = {He, Shaomei and Stevens, Sarah L. R. and Chan, Leong-Keat and Bertilsson, Stefan and Glavina del Rio, Tijana and Tringe, Susannah G. and Malmstrom, Rex R. and McMahon, Katherine D.},
abstractNote = {Microbes are critical in carbon and nutrient cycling in freshwater ecosystems. Members of theVerrucomicrobiaare ubiquitous in such systems, and yet their roles and ecophysiology are not well understood. In this study, we recovered 19 Verrucomicrobia draft genomes by sequencing 184 time-series metagenomes from a eutrophic lake and a humic bog that differ in carbon source and nutrient availabilities. These genomes span four of the seven previously defined Verrucomicrobia subdivisions and greatly expand knowledge of the genomic diversity of freshwater Verrucomicrobia. Genome analysis revealed their potential role as (poly)saccharide degraders in freshwater, uncovered interesting genomic features for this lifestyle, and suggested their adaptation to nutrient availabilities in their environments.Verrucomicrobia populations differ significantly between the two lakes in glycoside hydrolase gene abundance and functional profiles, reflecting the autochthonous and terrestrially derived allochthonous carbon sources of the two ecosystems, respectively. Interestingly, a number of genomes recovered from the bog contained gene clusters that potentially encode a novel porin-multiheme cytochrome c complex and might be involved in extracellular electron transfer in the anoxic humus-rich environment. Notably, most epilimnion genomes have large numbers of so-called “Planctomycete-specific” cytochrome c-encoding genes, which exhibited distribution patterns nearly opposite to those seen with glycoside hydrolase genes, probably associated with the different levels of environmental oxygen availability and carbohydrate complexity between lakes/layers. Overall, the recovered genomes represent a major step toward understanding the role, ecophysiology, and distribution of Verrucomicrobia in freshwater. Freshwater Verrucomicrobia spp. are cosmopolitan in lakes and rivers, and yet their roles and ecophysiology are not well understood, as cultured freshwater Verrucomicrobia spp. are restricted to one subdivision of this phylum. We greatly expanded the known genomic diversity of this freshwater lineage by recovering 19 Verrucomicrobia draft genomes from 184 metagenomes collected from a eutrophic lake and a humic bog across multiple years. Most of these genomes represent the first freshwater representatives of several Verrucomicrobia subdivisions. Genomic analysis revealed Verrucomicrobia to be potential (poly)saccharide degraders and suggested their adaptation to carbon sources of different origins in the two contrasting ecosystems. We identified putative extracellular electron transfer genes and so-called “Planctomycete-specific” cytochrome c-encoding genes and identified their distinct distribution patterns between the lakes/layers. Overall, our analysis greatly advances the understanding of the function, ecophysiology, and distribution of freshwater Verrucomicrobia, while highlighting their potential role in freshwater carbon cycling.},
doi = {10.1128/mSphere.00277-17},
journal = {mSphere},
number = 5,
volume = 2,
place = {United States},
year = {2017},
month = {9}
}

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

Citation Metrics:
Cited by: 11 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Rapid Screening for Freshwater Bacterial Groups by Using Reverse Line Blot Hybridization
journal, October 2003


A Guide to the Natural History of Freshwater Lake Bacteria
journal, March 2011

  • Newton, R. J.; Jones, S. E.; Eiler, A.
  • Microbiology and Molecular Biology Reviews, Vol. 75, Issue 1
  • DOI: 10.1128/MMBR.00028-10

Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes
journal, December 2004


Development of a 16S rRNA-targeted probe set for Verrucomicrobia and its application for fluorescence in situ hybridization in a humic lake
journal, April 2010


Coraliomargarita akajimensis gen. nov., sp. nov., a novel member of the phylum 'Verrucomicrobia' isolated from seawater in Japan
journal, May 2007

  • Yoon, J.; Yasumoto-Hirose, M.; Katsuta, A.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 5
  • DOI: 10.1099/ijs.0.64755-0

Detection and Cultivation of Soil Verrucomicrobia
journal, December 2005


Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’
journal, October 2016


Terrimicrobium sacchariphilum gen. nov., sp. nov., an anaerobic bacterium of the class 'Spartobacteria' in the phylum Verrucomicrobia, isolated from a rice paddy field
journal, February 2014

  • Qiu, Y. -L.; Kuang, X. -z.; Shi, X. -s.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 5
  • DOI: 10.1099/ijs.0.060244-0

Real-time PCR detection of Holophagae (Acidobacteria) and Verrucomicrobia subdivision 1 groups in bulk and leek (Allium porrum) rhizosphere soils
journal, November 2010

  • da Rocha, Ulisses Nunes; van Elsas, Jan Dirk; van Overbeek, Leonard Simon
  • Journal of Microbiological Methods, Vol. 83, Issue 2
  • DOI: 10.1016/j.mimet.2010.08.003

Genomic and Physiological Characterization of the Verrucomicrobia Isolate Diplosphaera colitermitum gen. nov., sp. nov., Reveals Microaerophily and Nitrogen Fixation Genes
journal, December 2011

  • Wertz, John T.; Kim, Eunji; Breznak, John A.
  • Applied and Environmental Microbiology, Vol. 78, Issue 5
  • DOI: 10.1128/AEM.06466-11

Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium
journal, September 2004

  • Derrien, M.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 5
  • DOI: 10.1099/ijs.0.02873-0

Rubritalea marina gen. nov., sp. nov., a marine representative of the phylum 'Verrucomicrobia', isolated from a sponge (Porifera)
journal, September 2006

  • Scheuermayer, M.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 9
  • DOI: 10.1099/ijs.0.64360-0

Opitutus terrae gen. nov., sp. nov., to accommodate novel strains of the division 'Verrucomicrobia' isolated from rice paddy soil
journal, November 2001

  • Chin, K. J.; Liesack, W.; Janssen, P. H.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 51, Issue 6
  • DOI: 10.1099/00207713-51-6-1965

Brevifollis gellanilyticus gen. nov., sp. nov., a gellan-gum-degrading bacterium of the phylum Verrucomicrobia
journal, February 2013

  • Otsuka, S.; Suenaga, T.; Vu, H. T.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 8
  • DOI: 10.1099/ijs.0.048793-0

Phylogeny of Prosthecobacter, the Fusiform Caulobacters: Members of a Recently Discovered Division of the Bacteria
journal, October 1996

  • Hedlund, B. P.; Gosink, J. J.; Staley, J. T.
  • International Journal of Systematic Bacteriology, Vol. 46, Issue 4
  • DOI: 10.1099/00207713-46-4-960

Roseimicrobium gellanilyticum gen. nov., sp. nov., a new member of the class Verrucomicrobiae
journal, October 2012

  • Otsuka, S.; Ueda, H.; Suenaga, T.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 6
  • DOI: 10.1099/ijs.0.041848-0

Methanotrophy below pH 1 by a new Verrucomicrobia species
journal, November 2007

  • Pol, Arjan; Heijmans, Klaas; Harhangi, Harry R.
  • Nature, Vol. 450, Issue 7171
  • DOI: 10.1038/nature06222

Global distribution and diversity of marine Verrucomicrobia
journal, February 2012

  • Freitas, Sara; Hatosy, Stephen; Fuhrman, Jed A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.3

Verrucomicrobia Are Candidates for Polysaccharide-Degrading Bacterioplankton in an Arctic Fjord of Svalbard
journal, April 2014

  • Cardman, Z.; Arnosti, C.; Durbin, A.
  • Applied and Environmental Microbiology, Vol. 80, Issue 12
  • DOI: 10.1128/AEM.00899-14

Capturing Single Cell Genomes of Active Polysaccharide Degraders: An Unexpected Contribution of Verrucomicrobia
journal, April 2012


Metagenomic De Novo Assembly of an Aquatic Representative of the Verrucomicrobial Class Spartobacteria
journal, May 2013

  • Herlemann, Daniel P. R.; Lundin, Daniel; Labrenz, Matthias
  • mBio, Vol. 4, Issue 3
  • DOI: 10.1128/mBio.00569-12

Effect of Nutrient Loading on Bacterioplankton Community Composition in Lake Mesocosms
journal, January 2006


Diversity of cyanobacteria and heterotrophic bacteria in cyanobacterial blooms in Lake Joutikas, Finland
journal, January 2004

  • Kolmonen, E.; Sivonen, K.; Rapala, J.
  • Aquatic Microbial Ecology, Vol. 36
  • DOI: 10.3354/ame036201

Distribution of Typical Freshwater Bacterial Groups Is Associated with pH, Temperature, and Lake Water Retention Time
journal, December 2005


Verrucomicrobium spinosum gen. nov., sp. nov.: a Fimbriated Prosthecate Bacterium
journal, November 1987


Divergent members of the bacterial division Verrucomicrobiales in a temperate freshwater lake
journal, February 1998


Physical responses of small temperate lakes to variation in dissolved organic carbon concentrations
journal, May 2013


The influence of habitat heterogeneity on freshwater bacterial community composition and dynamics
journal, April 2008


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

Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations
journal, January 2016

  • Bendall, Matthew L.; Stevens, Sarah LR; Chan, Leong-Keat
  • The ISME Journal, Vol. 10, Issue 7
  • DOI: 10.1038/ismej.2015.241

Alterococcus agarolyticus , gen.nov., sp.nov., a halophilic thermophilic bacterium capable of agar degradation
journal, July 1998

  • Shieh, Wung Yang; Jean, Wen Dar
  • Canadian Journal of Microbiology, Vol. 44, Issue 7
  • DOI: 10.1139/w98-051

Annual Patterns in Bacterioplankton Community Variability in a Humic Lake
journal, October 2004


Synchrony in aquatic microbial community dynamics
journal, May 2007

  • Kent, Angela D.; Yannarell, Anthony C.; Rusak, James A.
  • The ISME Journal, Vol. 1, Issue 1
  • DOI: 10.1038/ismej.2007.6

Characterization of a Planctomycetal Organelle: a Novel Bacterial Microcompartment for the Aerobic Degradation of Plant Saccharides
journal, January 2014

  • Erbilgin, Onur; McDonald, Kent L.; Kerfeld, Cheryl A.
  • Applied and Environmental Microbiology, Vol. 80, Issue 7
  • DOI: 10.1128/AEM.03887-13

Plant Carbohydrate Scavenging through TonB-Dependent Receptors: A Feature Shared by Phytopathogenic and Aquatic Bacteria
journal, February 2007


Chemical Structures and Bioactivities of Sulfated Polysaccharides from Marine Algae
journal, February 2011

  • Jiao, Guangling; Yu, Guangli; Zhang, Junzeng
  • Marine Drugs, Vol. 9, Issue 2
  • DOI: 10.3390/md9020196

Production, isolation and preliminary characterization of the exopolysaccharide of the cyanobacterium Spirulina platensis
journal, June 1993

  • Filali Mouhim, R.; Cornet, J. -F.; Fontane, T.
  • Biotechnology Letters, Vol. 15, Issue 6
  • DOI: 10.1007/BF00138541

Freshwater Plants Synthesize Sulfated Polysaccharides: Heterogalactans from Water Hyacinth (Eicchornia crassipes)
journal, January 2012

  • Dantas-Santos, Nednaldo; Gomes, Dayanne Lopes; Costa, Leandro Silva
  • International Journal of Molecular Sciences, Vol. 13, Issue 1
  • DOI: 10.3390/ijms13010961

The Role of Nitrogen Fixation in Cyanobacterial Bloom Toxicity in a Temperate, Eutrophic Lake
journal, February 2013


Outer Membrane c-Type Cytochromes Required for Fe(III) and Mn(IV) Oxide Reduction in Geobacter sulfurreducens
journal, December 2005


Genomic analyses of bacterial porin-cytochrome gene clusters
journal, November 2014


Outer-membrane cytochrome-independent reduction of extracellular electron acceptors in Shewanella oneidensis
journal, April 2012


Protective Role of tolC in Efflux of the Electron Shuttle Anthraquinone-2,6-Disulfonate
journal, March 2002


Role of Geobacter sulfurreducens Outer Surface c-Type Cytochromes in Reduction of Soil Humic Acid and Anthraquinone-2,6-Disulfonate
journal, February 2010

  • Voordeckers, J. W.; Kim, B. -C.; Izallalen, M.
  • Applied and Environmental Microbiology, Vol. 76, Issue 7
  • DOI: 10.1128/AEM.02250-09

Humic substances as electron acceptors for microbial respiration
journal, August 1996

  • Lovley, Derek R.; Coates, John D.; Blunt-Harris, Elizabeth L.
  • Nature, Vol. 382, Issue 6590
  • DOI: 10.1038/382445a0

Humic substances as fully regenerable electron acceptors in recurrently anoxic environments
journal, February 2014

  • Klüpfel, Laura; Piepenbrock, Annette; Kappler, Andreas
  • Nature Geoscience, Vol. 7, Issue 3
  • DOI: 10.1038/ngeo2084

Novel protein domains and motifs in the marine planctomycete Rhodopirellula baltica
journal, July 2004


Analysis of Genome Content Evolution in PVC Bacterial Super-Phylum: Assessment of Candidate Genes Associated with Cellular Organization and Lifestyle
journal, December 2012

  • Kamneva, Olga K.; Knight, Stormy J.; Liberles, David A.
  • Genome Biology and Evolution, Vol. 4, Issue 12
  • DOI: 10.1093/gbe/evs113

Bacterial Community Composition and Dynamics Spanning Five Years in Freshwater Bog Lakes
journal, June 2017


MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities
journal, January 2015


IMG 4 version of the integrated microbial genomes comparative analysis system
journal, October 2013

  • Markowitz, Victor M.; Chen, I-Min A.; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt963

PhyloSift: phylogenetic analysis of genomes and metagenomes
journal, January 2014

  • Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric
  • PeerJ, Vol. 2
  • DOI: 10.7717/peerj.243

New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010

  • Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
  • Systematic Biology, Vol. 59, Issue 3
  • DOI: 10.1093/sysbio/syq010

Characterization of the first cultured representative of Verrucomicrobia subdivision 5 indicates the proposal of a novel phylum
journal, June 2016

  • Spring, Stefan; Bunk, Boyke; Spröer, Cathrin
  • The ISME Journal, Vol. 10, Issue 12
  • DOI: 10.1038/ismej.2016.84

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

Prediction of protein subcellular localization
journal, June 2006

  • Yu, Chin-Sheng; Chen, Yu-Ching; Lu, Chih-Hao
  • Proteins: Structure, Function, and Bioinformatics, Vol. 64, Issue 3
  • DOI: 10.1002/prot.21018

PRED-TMBB: a web server for predicting the topology of  -barrel outer membrane proteins
journal, July 2004

  • Bagos, P. G.; Liakopoulos, T. D.; Spyropoulos, I. C.
  • Nucleic Acids Research, Vol. 32, Issue Web Server
  • DOI: 10.1093/nar/gkh417

    Works referencing / citing this record:

    Determining lineage-specific bacterial growth curves with a novel approach based on amplicon reads normalization using internal standard (ARNIS)
    journal, July 2018