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

Jessica M. Labonté, Brandon K. Swan, Bonnie Poulos, Haiwei Luo, Sergey Koren, Steven J. Hallam, Matthew Sullivan, Tanja Woyke, K. Eric Wommack, Ramunas Stepanauskas

Research output: Contribution to journalArticle

80 Citations (Scopus)

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. 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. Our 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.

Original languageEnglish (US)
Pages (from-to)2386-2399
Number of pages14
JournalISME Journal
Volume9
Issue number11
DOIs
StatePublished - Nov 1 2015

Fingerprint

bacterioplankton
Genomics
genomics
virus
Viruses
viruses
Genome
cells
Metagenomics
genome
Virus Diseases
Oceans and Seas
Bacteriophages
Virus Cultivation
Verrucomicrobia
Lysogeny
microbial communities
Bacteroidetes
microbial community
Caudovirales

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Microbiology

Cite this

Labonté, J. M., Swan, B. K., Poulos, B., Luo, H., Koren, S., Hallam, S. J., ... Stepanauskas, R. (2015). Single-cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton. ISME Journal, 9(11), 2386-2399. https://doi.org/10.1038/ismej.2015.48

Single-cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton. / Labonté, Jessica M.; Swan, Brandon K.; Poulos, Bonnie; Luo, Haiwei; Koren, Sergey; Hallam, Steven J.; Sullivan, Matthew; Woyke, Tanja; Eric Wommack, K.; Stepanauskas, Ramunas.

In: ISME Journal, Vol. 9, No. 11, 01.11.2015, p. 2386-2399.

Research output: Contribution to journalArticle

Labonté, JM, Swan, BK, Poulos, B, Luo, H, Koren, S, Hallam, SJ, Sullivan, M, Woyke, T, Eric Wommack, K & Stepanauskas, R 2015, 'Single-cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton', ISME Journal, vol. 9, no. 11, pp. 2386-2399. https://doi.org/10.1038/ismej.2015.48
Labonté, Jessica M. ; Swan, Brandon K. ; Poulos, Bonnie ; Luo, Haiwei ; Koren, Sergey ; Hallam, Steven J. ; Sullivan, Matthew ; Woyke, Tanja ; Eric Wommack, K. ; Stepanauskas, Ramunas. / Single-cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton. In: ISME Journal. 2015 ; Vol. 9, No. 11. pp. 2386-2399.
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