skip to main content
OSTI.GOV 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

Journal Article · · The ISME Journal
 [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

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.

Research Organization:
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1347108
Journal Information:
The ISME Journal, Vol. 9, Issue 11; ISSN 1751-7362
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 144 works
Citation information provided by
Web of Science

References (93)

Prophage insertion sites journal May 2003
Shifting the genomic gold standard for the prokaryotic species definition journal October 2009
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 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
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome journal January 2009
Probing Individual Environmental Bacteria for Viruses by Using Microfluidic Digital PCR journal June 2011
Marine viruses — major players in the global ecosystem journal October 2007
Virioplankton: Viruses in Aquatic Ecosystems journal March 2000
Viral tagging reveals discrete populations in Synechococcus viral genome sequence space journal July 2014
Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments journal August 2007
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands journal July 2006
Cultivation of the ubiquitous SAR11 marine bacterioplankton clade journal August 2002
Phage-bacteria relationships and CRISPR elements revealed by a metagenomic survey of the rumen microbiome: Rumen viral metagenome journal October 2011
Metagenomic Analysis of Lysogeny in Tampa Bay: Implications for Prophage Gene Expression journal September 2008
Abundant SAR11 viruses in the ocean journal February 2013
Using CRISPRs as a metagenomic tool to identify microbial hosts of a diffuse flow hydrothermal vent viral assemblage: CRISPR spacers reveal hosts of marine vent viral assemblage journal April 2011
Sequencing genomes from single cells by polymerase cloning journal May 2006
Lysogeny in marine Synechococcus journal January 2002
Single-Cell Genomics Reveals Organismal Interactions in Uncultivated Marine Protists journal May 2011
Viruses in the sea journal September 2005
Phage Genomics journal January 2002
Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton journal August 2013
Basic local alignment search tool journal October 1990
Assembling the Marine Metagenome, One Cell at a Time journal April 2009
A Rapid Bootstrap Algorithm for the RAxML Web Servers journal October 2008
MUSCLE: multiple sequence alignment with high accuracy and high throughput journal March 2004
Potential for Chemolithoautotrophy Among Ubiquitous Bacteria Lineages in the Dark Ocean journal September 2011
Comparative genomics of the mycobacteriophages: insights into bacteriophage evolution journal June 2008
Twelve previously unknown phage genera are ubiquitous in global oceans journal July 2013
Seasonal Variation in Lysogeny as Depicted by Prophage Induction in Tampa Bay, Florida journal September 2002
Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean journal June 2013
Expanding the Marine Virosphere Using Metagenomics journal December 2013
Contrasting Life Strategies of Viruses that Infect Photo- and Heterotrophic Bacteria, as Revealed by Viral Tagging journal October 2012
The Uncultured Microbial Majority journal October 2003
Genomic DNA Amplification from a Single Bacterium journal June 2005
The elemental composition of virus particles: implications for marine biogeochemical cycles journal June 2014
Draft genome sequence of strain HIMB100, a cultured representative of the SAR116 clade of marine Alphaproteobacteria journal December 2011
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences journal May 2006
Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? journal June 2008
Comparative dna Analysis Across Diverse Genomes journal December 1998
Contrasting genomic patterns and infection strategies of two co-existing B acteroidetes podovirus genera : Infection strategies of co-existing podoviruse journal February 2014
Regional Variation in Lytic and Lysogenic Viral Infection in the Southern Ocean and Its Contribution to Biogeochemical Cycling journal July 2012
Assembling Single-Cell Genomes and Mini-Metagenomes From Chimeric MDA Products journal October 2013
PIPS: Pathogenicity Island Prediction Software journal February 2012
Single cell genomics: an individual look at microbes journal October 2012
The Pacific Ocean Virome (POV): A Marine Viral Metagenomic Dataset and Associated Protein Clusters for Quantitative Viral Ecology journal February 2013
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence journal March 1997
Easyfig: a genome comparison visualizer journal January 2011
Bacteriophage sensitivity patterns among bacteria isolated from marine waters journal September 1981
Cyanophages infecting the oceanic cyanobacterium Prochlorococcus journal August 2003
Phylogenomic Evidence for the Presence of a Flagellum and cbb3 Oxidase in the Free-Living Mitochondrial Ancestor journal June 2011
Genomic properties of Marine Group A bacteria indicate a role in the marine sulfur cycle journal September 2013
Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans journal June 2013
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs journal February 2008
Genome sequences of siphoviruses infecting marine Synechococcus unveil a diverse cyanophage group and extensive phage-host genetic exchanges: Genomics of four Synechococcus siphoviruses journal December 2011
Flow cytometric detection and enumeration of DNA and RNA viruses infecting marine eukaryotic microalgae journal April 2007
Modeling ecological drivers in marine viral communities using comparative metagenomics and network analyses journal July 2014
Genomic sequencing of uncultured microorganisms from single cells journal August 2012
Phage_Finder: Automated identification and classification of prophage regions in complete bacterial genome sequences journal October 2006
ProtTest 3: fast selection of best-fit models of protein evolution journal February 2011
Three Prochlorococcus Cyanophage Genomes: Signature Features and Ecological Interpretations journal April 2005
PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies journal May 2012
Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere journal August 2005
Capturing Single Cell Genomes of Active Polysaccharide Degraders: An Unexpected Contribution of Verrucomicrobia journal April 2012
Viruses in Marine Planktonic Systems journal January 1993
Statistical structure of host-phage interactions journal June 2011
Prophinder: a computational tool for prophage prediction in prokaryotic genomes journal January 2008
BEDTools: a flexible suite of utilities for comparing genomic features journal January 2010
The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’ journal November 2009
Ecology of prokaryotic viruses journal May 2004
Marine Viruses: Truth or Dare journal January 2012
Analyzing genomes with cumulative skew diagrams journal May 1998
Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics journal August 2014
Single-cell and population level viral infection dynamics revealed by phageFISH, a method to visualize intracellular and free viruses: phageFISH - visualizing intracellular and free viruses journal March 2013
Prophage Genomics journal June 2003
Viruses of the Archaea: a unifying view journal November 2006
Prevalence of Broad-Host-Range Lytic Bacteriophages of Sphaerotilus natans, Escherichia coli, andPseudomonas aeruginosa journal February 1998
Prochlorococcus, a Marine Photosynthetic Prokaryote of Global Significance journal March 1999
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence journal March 1997
Isolation and characterization of the novel Pseudomonas stutzeri bacteriophage 8P journal January 2021
Metaviromics coupled with phage-host identification to open the viral ‘black box’ journal February 2021
SPOCD1 is an essential executor of piRNA-directed de novo DNA methylation journal July 2020
Contrasting Life Strategies of Viruses That Infect Photo- and Heterotrophic Bacteria, as Revealed by Viral Tagging journal March 2013
Strain-Resolved Dynamics of the Lung Microbiome in Patients with Cystic Fibrosis journal April 2021
Prophage Genomics journal September 2003
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0 text January 2010
Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice journal June 2014
The fate and biogeochemical cycling of viral elements journal November 2014
Insight into the unknown marine virus majority journal July 2013
Complete Genome Sequence of "Candidatus Puniceispirillum marinum" IMCC1322, a Representative of the SAR116 Clade in the Alphaproteobacteria journal April 2010
The need for speed journal January 2009
Gene swapping in the dead zone journal October 2014

Cited By (68)

Isolation and Complete Genome Sequence of a Novel Marinobacter Phage B23 journal September 2018
Lysogeny in nature: mechanisms, impact and ecology of temperate phages journal March 2017
Ecological dynamics and co-occurrence among marine phytoplankton, bacteria and myoviruses shows microdiversity matters journal April 2017
Minimum Information about an Uncultivated Virus Genome (MIUViG) journal December 2018
Marine viruses discovered via metagenomics shed light on viral strategies throughout the oceans journal July 2017
The enigmatic archaeal virosphere journal November 2017
A virus or more in (nearly) every cell: ubiquitous networks of virus–host interactions in extreme environments journal February 2018
Single-cell genomics uncover Pelagibacter as the putative host of the extremely abundant uncultured 37-F6 viral population in the ocean journal September 2018
Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes journal October 2018
Phage puppet masters of the marine microbial realm journal June 2018
An automated Raman-based platform for the sorting of live cells by functional properties journal March 2019
Defining the human gut host–phage network through single-cell viral tagging journal August 2019
Illuminating structural proteins in viral “dark matter” with metaproteomics journal February 2016
Spindle-shaped viruses infect marine ammonia-oxidizing thaumarchaea journal July 2019
Computational approaches to predict bacteriophage–host relationships journal December 2015
Current and Promising Approaches to Identify Horizontal Gene Transfer Events in Metagenomes journal August 2019
Targeted metagenomic recovery of four divergent viruses reveals shared and distinctive characteristics of giant viruses of marine eukaryotes
  • Needham, David M.; Poirier, Camille; Hehenberger, Elisabeth
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1786 https://doi.org/10.1098/rstb.2019.0086
journal October 2019
Contributions of single-cell genomics to our understanding of planktonic marine archaea journal October 2019
Viral Sequence Identification in Metagenomes using Natural Language Processing Techniques posted_content January 2020
Visualization of viral infection dynamics in a unicellular eukaryote and quantification of viral production using VirusFISH posted_content November 2019
VIBRANT: Automated recovery, annotation and curation of microbial viruses, and evaluation of virome function from genomic sequences posted_content November 2019
metaSPAdes: a new versatile metagenomic assembler journal March 2017
Large-scale maps of variable infection efficiencies in aquatic Bacteroidetes phage-host model systems : Variable phage-host infection interactions journal June 2016
New archaeal viruses discovered by metagenomic analysis of viral communities in enrichment cultures journal January 2019
Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake journal September 2019
Assessing the viral content of uncultured picoeukaryotes in the global‐ocean by single cell genomics journal September 2019
Major role of nitrite-oxidizing bacteria in dark ocean carbon fixation journal November 2017
Marine RNA Virus Quasispecies Are Distributed throughout the Oceans journal April 2019
Genomic analyses of two novel biofilm-degrading methicillin-resistant Staphylococcus aureus phages journal May 2019
VirFinder: a novel k-mer based tool for identifying viral sequences from assembled metagenomic data journal July 2017
Genome diversity of marine phages recovered from Mediterranean metagenomes: Size matters journal September 2017
Changes in Marine Prokaryote Composition with Season and Depth Over an Arctic Polar Year journal April 2017
Intriguing Interaction of Bacteriophage-Host Association: An Understanding in the Era of Omics journal April 2017
Rokubacteria: Genomic Giants among the Uncultured Bacterial Phyla journal November 2017
Archaeal Viruses from High-Temperature Environments journal February 2018
Optimization of viral resuspension methods for carbon-rich soils along a permafrost thaw gradient journal January 2016
vConTACT: an iVirus tool to classify double-stranded DNA viruses that infect Archaea and Bacteria journal January 2017
VirSorter: mining viral signal from microbial genomic data journal January 2015
The trajectory of microbial single-cell sequencing journal October 2017
Low activity of lytic pelagiphages in coastal marine waters journal June 2018
Genome mining- and synthetic biology-enabled production of hypermodified peptides journal September 2019
Assembly of long error-prone reads using de Bruijn graphs journal December 2016
A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators journal September 2019
hybridSPAdes: an algorithm for hybrid assembly of short and long reads journal November 2015
Accurate and complete genomes from metagenomes journal March 2020
Genome and epigenome of a novel marine Thaumarchaeota strain suggest viral infection, phosphorothioation DNA modification and multiple restriction systems: Genome and epigenome of a new marine thaumarchaeon journal May 2017
Integrated mobile genetic elements in Thaumarchaeota journal March 2019
Genomic and Seasonal Variations among Aquatic Phages Infecting the Baltic Sea Gammaproteobacterium Rheinheimera sp. Strain BAL341 journal July 2019
Virus-mediated archaeal hecatomb in the deep seafloor text January 2016
Minimum information about an uncultivated virus genome (MIUVIG) text January 2019
Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles journal July 2017
A viral reckoning: viruses emerge as essential manipulators of global ecosystems: Crystal ball journal October 2018
Understanding the ecology and evolution of host-parasite interactions across scales journal August 2015
Host-hijacking and planktonic piracy: how phages command the microbial high seas journal February 2019
Putative archaeal viruses from the mesopelagic ocean journal January 2017
Novel Caudovirales associated with Marine Group I Thaumarchaeota assembled from metagenomes journal December 2018
VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences journal June 2020
Single-cell metagenomics: challenges and applications journal April 2018
Single-virus genomics reveals hidden cosmopolitan and abundant viruses journal June 2017
Author Correction: Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles journal December 2017
Viral coinfection is shaped by host ecology and virus-virus interactions across diverse microbial taxa and environments journal February 2017
Capturing in situ Virus-Host Range and Interaction Dynamics through Gene Fusion with epicPCR preprint August 2020
Marine archaea and archaeal viruses under global change journal July 2017
Seasonal Dynamics and Metagenomic Characterization of Marine Viruses in Goseong Bay, Korea journal January 2017
Microbiome Big-Data Mining and Applications Using Single-Cell Technologies and Metagenomics Approaches Toward Precision Medicine journal October 2019
High Diversity of Myocyanophage in Various Aquatic Environments Revealed by High-Throughput Sequencing of Major Capsid Protein Gene With a New Set of Primers journal May 2018
Droplet Digital PCR for Estimating Absolute Abundances of Widespread Pelagibacter Viruses journal June 2019
Enteric Viral Co-Infections: Pathogenesis and Perspective journal August 2020