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

Title: Single-cell genomics-based analysis of virus–host interactions in marine surface bacterioplankton

Abstract

Viral infections dynamically alter the composition and metabolic potential of marine microbial communities and the evolutionary trajectories of host populations with resulting feedback on biogeochemical cycles. It is quite possible that all microbial populations in the ocean are impacted by viral infections. Our knowledge of virus–host relationships, however, has been limited to a minute fraction of cultivated host groups. Here, we utilized single-cell sequencing to obtain genomic blueprints of viruses inside or attached to individual bacterial and archaeal cells captured in their native environment, circumventing the need for host and virus cultivation. Furthermore, a combination of comparative genomics, metagenomic fragment recruitment, sequence anomalies and irregularities in sequence coverage depth and genome recovery were utilized to detect viruses and to decipher modes of virus–host interactions. Members of all three tailed phage families were identified in 20 out of 58 phylogenetically and geographically diverse single amplified genomes (SAGs) of marine bacteria and archaea. At least four phage–host interactions had the characteristics of late lytic infections, all of which were found in metabolically active cells. One virus had genetic potential for lysogeny. Our findings include first known viruses of Thaumarchaeota, Marinimicrobia, Verrucomicrobia and Gammaproteobacteria clusters SAR86 and SAR92. Viruses were also found inmore » SAGs of Alphaproteobacteria and Bacteroidetes. A high fragment recruitment of viral metagenomic reads confirmed that most of the SAG-associated viruses are abundant in the ocean. This study demonstrates that single-cell genomics, in conjunction with sequence-based computational tools, enable in situ, cultivation-independent insights into host–virus interactions in complex microbial communities.« less

Authors:
 [1];  [1];  [2];  [3];  [4];  [5];  [2];  [6];  [7];  [1]
  1. Bigelow Lab. for Ocean Sciences, East Boothbay, ME (United States)
  2. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evoloutionary Biology
  3. Chinese Univ. of Hong Kong (China). School of Life Sciences
  4. National Biodefense Analysis and Countermeasure Center, Frederick, MD (United States)
  5. Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Microbiology and Immunology
  6. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  7. Univ. of Delaware, Newark, DE (United States). Dept. of Plant and Soil Sciences
Publication Date:
Research Org.:
Dept. of Energy Joint Genome Inst., Walnut Creek, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1347108
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 9; Journal Issue: 11; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
58 GEOSCIENCES

Citation Formats

Labonté, Jessica M., Swan, Brandon K., Poulos, Bonnie, Luo, Haiwei, Koren, Sergey, Hallam, Steven J., Sullivan, Matthew B., Woyke, Tanja, Eric Wommack, K., and Stepanauskas, Ramunas. Single-cell genomics-based analysis of virus–host interactions in marine surface bacterioplankton. United States: N. p., 2015. Web. doi:10.1038/ismej.2015.48.
Labonté, Jessica M., Swan, Brandon K., Poulos, Bonnie, Luo, Haiwei, Koren, Sergey, Hallam, Steven J., Sullivan, Matthew B., Woyke, Tanja, Eric Wommack, K., & Stepanauskas, Ramunas. Single-cell genomics-based analysis of virus–host interactions in marine surface bacterioplankton. United States. doi:10.1038/ismej.2015.48.
Labonté, Jessica M., Swan, Brandon K., Poulos, Bonnie, Luo, Haiwei, Koren, Sergey, Hallam, Steven J., Sullivan, Matthew B., Woyke, Tanja, Eric Wommack, K., and Stepanauskas, Ramunas. Tue . "Single-cell genomics-based analysis of virus–host interactions in marine surface bacterioplankton". United States. doi:10.1038/ismej.2015.48. https://www.osti.gov/servlets/purl/1347108.
@article{osti_1347108,
title = {Single-cell genomics-based analysis of virus–host interactions in marine surface bacterioplankton},
author = {Labonté, Jessica M. and Swan, Brandon K. and Poulos, Bonnie and Luo, Haiwei and Koren, Sergey and Hallam, Steven J. and Sullivan, Matthew B. and Woyke, Tanja and Eric Wommack, K. and Stepanauskas, Ramunas},
abstractNote = {Viral infections dynamically alter the composition and metabolic potential of marine microbial communities and the evolutionary trajectories of host populations with resulting feedback on biogeochemical cycles. It is quite possible that all microbial populations in the ocean are impacted by viral infections. Our knowledge of virus–host relationships, however, has been limited to a minute fraction of cultivated host groups. Here, we utilized single-cell sequencing to obtain genomic blueprints of viruses inside or attached to individual bacterial and archaeal cells captured in their native environment, circumventing the need for host and virus cultivation. Furthermore, a combination of comparative genomics, metagenomic fragment recruitment, sequence anomalies and irregularities in sequence coverage depth and genome recovery were utilized to detect viruses and to decipher modes of virus–host interactions. Members of all three tailed phage families were identified in 20 out of 58 phylogenetically and geographically diverse single amplified genomes (SAGs) of marine bacteria and archaea. At least four phage–host interactions had the characteristics of late lytic infections, all of which were found in metabolically active cells. One virus had genetic potential for lysogeny. Our findings include first known viruses of Thaumarchaeota, Marinimicrobia, Verrucomicrobia and Gammaproteobacteria clusters SAR86 and SAR92. Viruses were also found in SAGs of Alphaproteobacteria and Bacteroidetes. A high fragment recruitment of viral metagenomic reads confirmed that most of the SAG-associated viruses are abundant in the ocean. This study demonstrates that single-cell genomics, in conjunction with sequence-based computational tools, enable in situ, cultivation-independent insights into host–virus interactions in complex microbial communities.},
doi = {10.1038/ismej.2015.48},
journal = {The ISME Journal},
number = 11,
volume = 9,
place = {United States},
year = {2015},
month = {4}
}

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

Citation Metrics:
Cited by: 39 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies
journal, May 2012

  • Akhter, Sajia; Aziz, Ramy K.; Edwards, Robert A.
  • Nucleic Acids Research, Vol. 40, Issue 16
  • DOI: 10.1093/nar/gks406

Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Phage-bacteria relationships and CRISPR elements revealed by a metagenomic survey of the rumen microbiome: Rumen viral metagenome
journal, October 2011


Marine Viruses: Truth or Dare
journal, January 2012


Phage Genomics
journal, January 2002


Prophage insertion sites
journal, May 2003


Prophage Genomics
journal, June 2003


ProtTest 3: fast selection of best-fit models of protein evolution
journal, February 2011


Contrasting Life Strategies of Viruses that Infect Photo- and Heterotrophic Bacteria, as Revealed by Viral Tagging
journal, October 2012


Viral tagging reveals discrete populations in Synechococcus viral genome sequence space
journal, July 2014

  • Deng, Li; Ignacio-Espinoza, J. Cesar; Gregory, Ann C.
  • Nature, Vol. 513, Issue 7517
  • DOI: 10.1038/nature13459

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

Regional Variation in Lytic and Lysogenic Viral Infection in the Southern Ocean and Its Contribution to Biogeochemical Cycling
journal, July 2012

  • Evans, Claire; Brussaard, Corina P. D.
  • Applied and Environmental Microbiology, Vol. 78, Issue 18
  • DOI: 10.1128/AEM.01388-12

Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere
journal, August 2005

  • Filee, J.; Tetart, F.; Suttle, C. A.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 35
  • DOI: 10.1073/pnas.0503404102

Statistical structure of host-phage interactions
journal, June 2011

  • Flores, C. O.; Meyer, J. R.; Valverde, S.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 28
  • DOI: 10.1073/pnas.1101595108

Phage_Finder: Automated identification and classification of prophage regions in complete bacterial genome sequences
journal, October 2006


Viruses in Marine Planktonic Systems
journal, January 1993


Analyzing genomes with cumulative skew diagrams
journal, May 1998


Draft genome sequence of strain HIMB100, a cultured representative of the SAR116 clade of marine Alphaproteobacteria
journal, December 2011

  • Grote, Jana; Bayindirli, Cansu; Bergauer, Kristin
  • Standards in Genomic Sciences, Vol. 5, Issue 3
  • DOI: 10.4056/sigs.1854551

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

Comparative genomics of the mycobacteriophages: insights into bacteriophage evolution
journal, June 2008


Contrasting genomic patterns and infection strategies of two co-existing B acteroidetes podovirus genera : Infection strategies of co-existing podoviruse
journal, February 2014

  • Holmfeldt, Karin; Howard-Varona, Cristina; Solonenko, Natalie
  • Environmental Microbiology, Vol. 16, Issue 8
  • DOI: 10.1111/1462-2920.12391

Cultivated Single-Stranded DNA Phages That Infect Marine Bacteroidetes Prove Difficult To Detect with DNA-Binding Stains
journal, December 2011

  • Holmfeldt, Karin; Odić, Duško; Sullivan, Matthew B.
  • Applied and Environmental Microbiology, Vol. 78, Issue 3
  • DOI: 10.1128/AEM.06580-11

Twelve previously unknown phage genera are ubiquitous in global oceans
journal, July 2013

  • Holmfeldt, K.; Solonenko, N.; Shah, M.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 31
  • DOI: 10.1073/pnas.1305956110

Modeling ecological drivers in marine viral communities using comparative metagenomics and network analyses
journal, July 2014

  • Hurwitz, B. L.; Westveld, A. H.; Brum, J. R.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 29
  • DOI: 10.1073/pnas.1319778111

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


Phylogenomics of T4 cyanophages: lateral gene transfer in the ‘core’ and origins of host genes: Molecular evolution of T4 myoviruses
journal, February 2012


The elemental composition of virus particles: implications for marine biogeochemical cycles
journal, June 2014

  • Jover, Luis F.; Effler, T. Chad; Buchan, Alison
  • Nature Reviews Microbiology, Vol. 12, Issue 7
  • DOI: 10.1038/nrmicro3289

Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans
journal, June 2013

  • Kang, I.; Oh, H. -M.; Kang, D.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 30
  • DOI: 10.1073/pnas.1219930110

Comparative dna Analysis Across Diverse Genomes
journal, December 1998


Phylogenetic Analysis Indicates Evolutionary Diversity and Environmental Segregation of Marine Podovirus DNA Polymerase Gene Sequences
journal, April 2009

  • Labonte, J. M.; Reid, K. E.; Suttle, C. A.
  • Applied and Environmental Microbiology, Vol. 75, Issue 11
  • DOI: 10.1128/AEM.02317-08

Ultrafast and memory-efficient alignment of short DNA sequences to the human genome
journal, January 2009


Genomic sequencing of uncultured microorganisms from single cells
journal, August 2012


Prophinder: a computational tool for prophage prediction in prokaryotic genomes
journal, January 2008


tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence
journal, March 1997


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


Metagenomic Analysis of Lysogeny in Tampa Bay: Implications for Prophage Gene Expression
journal, September 2008


Lysogeny in marine Synechococcus
journal, January 2002

  • McDaniel, L.; Houchin, L. A.; Williamson, S. J.
  • Nature, Vol. 415, Issue 6871
  • DOI: 10.1038/415496a

Expanding the Marine Virosphere Using Metagenomics
journal, December 2013


Bacteriophage sensitivity patterns among bacteria isolated from marine waters
journal, September 1981

  • Moebus, K.; Nattkemper, H.
  • Helgoländer Meeresuntersuchungen, Vol. 34, Issue 3
  • DOI: 10.1007/BF02074130

Assembling Single-Cell Genomes and Mini-Metagenomes From Chimeric MDA Products
journal, October 2013

  • Nurk, Sergey; Bankevich, Anton; Antipov, Dmitry
  • Journal of Computational Biology, Vol. 20, Issue 10
  • DOI: 10.1089/cmb.2013.0084

Complete Genome Sequence of "Candidatus Puniceispirillum marinum" IMCC1322, a Representative of the SAR116 Clade in the Alphaproteobacteria
journal, April 2010

  • Oh, H. -M.; Kwon, K. K.; Kang, I.
  • Journal of Bacteriology, Vol. 192, Issue 12
  • DOI: 10.1128/JB.00347-10

Viruses of the Archaea: a unifying view
journal, November 2006

  • Prangishvili, David; Forterre, Patrick; Garrett, Roger A.
  • Nature Reviews Microbiology, Vol. 4, Issue 11
  • DOI: 10.1038/nrmicro1527

BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010


Genomic DNA Amplification from a Single Bacterium
journal, June 2005


Cultivation of the ubiquitous SAR11 marine bacterioplankton clade
journal, August 2002

  • Rappé, Michael S.; Connon, Stephanie A.; Vergin, Kevin L.
  • Nature, Vol. 418, Issue 6898
  • DOI: 10.1038/nature00917

The Uncultured Microbial Majority
journal, October 2003


Shifting the genomic gold standard for the prokaryotic species definition
journal, October 2009

  • Richter, Michael; Rosselló-Móra, Ramon
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
  • DOI: 10.1073/pnas.0906412106

Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics
journal, August 2014


Phylogenomic Evidence for the Presence of a Flagellum and cbb3 Oxidase in the Free-Living Mitochondrial Ancestor
journal, June 2011

  • Sassera, D.; Lo, N.; Epis, S.
  • Molecular Biology and Evolution, Vol. 28, Issue 12
  • DOI: 10.1093/molbev/msr159

Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton
journal, August 2013

  • Schmidt, Helen F.; Sakowski, Eric G.; Williamson, Shannon J.
  • The ISME Journal, Vol. 8, Issue 1
  • DOI: 10.1038/ismej.2013.124

PIPS: Pathogenicity Island Prediction Software
journal, February 2012


A Rapid Bootstrap Algorithm for the RAxML Web Servers
journal, October 2008

  • Stamatakis, Alexandros; Hoover, Paul; Rougemont, Jacques
  • Systematic Biology, Vol. 57, Issue 5
  • DOI: 10.1080/10635150802429642

Single cell genomics: an individual look at microbes
journal, October 2012


Three Prochlorococcus Cyanophage Genomes: Signature Features and Ecological Interpretations
journal, April 2005


The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’
journal, November 2009


Cyanophages infecting the oceanic cyanobacterium Prochlorococcus
journal, August 2003

  • Sullivan, Matthew B.; Waterbury, John B.; Chisholm, Sallie W.
  • Nature, Vol. 424, Issue 6952
  • DOI: 10.1038/nature01929

Easyfig: a genome comparison visualizer
journal, January 2011


Marine viruses — major players in the global ecosystem
journal, October 2007


Viruses in the sea
journal, September 2005


Potential for Chemolithoautotrophy Among Ubiquitous Bacteria Lineages in the Dark Ocean
journal, September 2011


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

Probing Individual Environmental Bacteria for Viruses by Using Microfluidic Digital PCR
journal, June 2011


Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments
journal, August 2007


Flow cytometric detection and enumeration of DNA and RNA viruses infecting marine eukaryotic microalgae
journal, April 2007


Ecology of prokaryotic viruses
journal, May 2004


Seasonal Variation in Lysogeny as Depicted by Prophage Induction in Tampa Bay, Florida
journal, September 2002


Virioplankton: Viruses in Aquatic Ecosystems
journal, March 2000


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


Genomic properties of Marine Group A bacteria indicate a role in the marine sulfur cycle
journal, September 2013

  • Wright, Jody J.; Mewis, Keith; Hanson, Niels W.
  • The ISME Journal, Vol. 8, Issue 2
  • DOI: 10.1038/ismej.2013.152

Single-Cell Genomics Reveals Organismal Interactions in Uncultivated Marine Protists
journal, May 2011


Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008


Sequencing genomes from single cells by polymerase cloning
journal, May 2006

  • Zhang, Kun; Martiny, Adam C.; Reppas, Nikos B.
  • Nature Biotechnology, Vol. 24, Issue 6, p. 680-686
  • DOI: 10.1038/nbt1214

Abundant SAR11 viruses in the ocean
journal, February 2013

  • Zhao, Yanlin; Temperton, Ben; Thrash, J. Cameron
  • Nature, Vol. 494, Issue 7437
  • DOI: 10.1038/nature11921

    Works referencing / citing this record:

    Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes
    journal, October 2018


    Genomic analyses of two novel biofilm-degrading methicillin-resistant Staphylococcus aureus phages
    journal, May 2019

    • Dakheel, Khulood Hamid; Rahim, Raha Abdul; Neela, Vasantha Kumari
    • BMC Microbiology, Vol. 19, Issue 1
    • DOI: 10.1186/s12866-019-1484-9