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Title: The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’

Abstract

Prochlorococcus, an abundant phototroph in the oceans, are infected by members of three families of viruses: myo-, podo- and siphoviruses. Genomes of myo- and podoviruses isolated on Prochlorococcus contain DNA replication machinery and virion structural genes homologous to those from coliphages T4 and T7 respectively. They also contain a suite of genes of cyanobacterial origin, most notably photosynthesis genes, which are expressed during infection and appear integral to the evolutionary trajectory of both host and phage. Here we present the first genome of a cyanobacterial siphovirus, P-SS2, which was isolated from Atlantic slope waters using a Prochlorococcus host (MIT9313). The P-SS2 genome is larger than, and considerably divergent from, previously sequenced siphoviruses. It appears most closely related to lambdoid siphoviruses, with which it shares 13 functional homologues. The ~108 kb P-SS2 genome encodes 131 predicted proteins and notably lacks photosynthesis genes which have consistently been found in other marine cyanophage, but does contain 14 other cyanobacterial homologues. While only six structural proteins were identified from the genome sequence, 35 proteins were detected experimentally; these mapped onto capsid and tail structural modules in the genome. P-SS2 is potentially capable of integration into its host as inferred from bioinformatically identified genetic machinerymore » int, bet, exo and a 53 bp attachment site. The host attachment site appears to be a genomic island that is tied to insertion sequence (IS) activity that could facilitate mobility of a gene involved in the nitrogenstress response. The homologous region and a secondary IS-element hot-spot in Synechococcus RS9917 are further evidence of IS-mediated genome evolution coincident with a probable relic prophage integration event. This siphovirus genome provides a glimpse into the biology of a deep-photic zone phage as well as the ocean cyanobacterial prophage and IS element ‘mobilome’.« less

Authors:
 [1];  [2];  [3];  [1];  [2];  [2];  [1]
+ Show Author Affiliations
  1. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
  2. Harvard Partners, Cambridge, MA (United States)
  3. Univ. of Arizona, Tucson, AZ (United States)
Publication Date:
Research Org.:
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1625898
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 11; Journal Issue: 11; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology

Citation Formats

Sullivan, Matthew B., Krastins, Bryan, Hughes, Jennifer L., Kelly, Libusha, Chase, Michael, Sarracino, David, and Chisholm, Sallie W. The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’. United States: N. p., 2009. Web. doi:10.1111/j.1462-2920.2009.02081.x.
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Sullivan, Matthew B., Krastins, Bryan, Hughes, Jennifer L., Kelly, Libusha, Chase, Michael, Sarracino, David, & Chisholm, Sallie W. The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’. United States. https://doi.org/10.1111/j.1462-2920.2009.02081.x
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Sullivan, Matthew B., Krastins, Bryan, Hughes, Jennifer L., Kelly, Libusha, Chase, Michael, Sarracino, David, and Chisholm, Sallie W. Tue . "The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’". United States. https://doi.org/10.1111/j.1462-2920.2009.02081.x. https://www.osti.gov/servlets/purl/1625898.
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@article{osti_1625898,
title = {The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’},
author = {Sullivan, Matthew B. and Krastins, Bryan and Hughes, Jennifer L. and Kelly, Libusha and Chase, Michael and Sarracino, David and Chisholm, Sallie W.},
abstractNote = {Prochlorococcus, an abundant phototroph in the oceans, are infected by members of three families of viruses: myo-, podo- and siphoviruses. Genomes of myo- and podoviruses isolated on Prochlorococcus contain DNA replication machinery and virion structural genes homologous to those from coliphages T4 and T7 respectively. They also contain a suite of genes of cyanobacterial origin, most notably photosynthesis genes, which are expressed during infection and appear integral to the evolutionary trajectory of both host and phage. Here we present the first genome of a cyanobacterial siphovirus, P-SS2, which was isolated from Atlantic slope waters using a Prochlorococcus host (MIT9313). The P-SS2 genome is larger than, and considerably divergent from, previously sequenced siphoviruses. It appears most closely related to lambdoid siphoviruses, with which it shares 13 functional homologues. The ~108 kb P-SS2 genome encodes 131 predicted proteins and notably lacks photosynthesis genes which have consistently been found in other marine cyanophage, but does contain 14 other cyanobacterial homologues. While only six structural proteins were identified from the genome sequence, 35 proteins were detected experimentally; these mapped onto capsid and tail structural modules in the genome. P-SS2 is potentially capable of integration into its host as inferred from bioinformatically identified genetic machinery int, bet, exo and a 53 bp attachment site. The host attachment site appears to be a genomic island that is tied to insertion sequence (IS) activity that could facilitate mobility of a gene involved in the nitrogenstress response. The homologous region and a secondary IS-element hot-spot in Synechococcus RS9917 are further evidence of IS-mediated genome evolution coincident with a probable relic prophage integration event. This siphovirus genome provides a glimpse into the biology of a deep-photic zone phage as well as the ocean cyanobacterial prophage and IS element ‘mobilome’.},
doi = {10.1111/j.1462-2920.2009.02081.x},
journal = {Environmental Microbiology},
number = 11,
volume = 11,
place = {United States},
year = {Tue Oct 27 00:00:00 EDT 2009},
month = {Tue Oct 27 00:00:00 EDT 2009}
}
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    • DOI: 10.3389/fmicb.2018.00189

    Improved bacterial recombineering by parallelized protein discovery
    journal, May 2020

    • Wannier, Timothy M.; Nyerges, Akos; Kuchwara, Helene M.
    • Proceedings of the National Academy of Sciences, Vol. 117, Issue 24
    • DOI: 10.1073/pnas.2001588117

    A novel uncultured marine cyanophage lineage with lysogenic potential linked to a putative marine Synechococcus ‘relic’ prophage
    journal, June 2019

    • Flores‐Uribe, José; Philosof, Alon; Sharon, Itai
    • Environmental Microbiology Reports, Vol. 11, Issue 4
    • DOI: 10.1111/1758-2229.12773

    Metabolic Genes within Cyanophage Genomes: Implications for Diversity and Evolution
    journal, September 2016

    Complete Genome Sequence of a Novel Marine Siphovirus, pVp-1, Infecting Vibrio parahaemolyticus
    journal, June 2012

    • Kim, Ji Hyung; Jun, Jin Woo; Choresca, Casiano H.
    • Journal of Virology, Vol. 86, Issue 12
    • DOI: 10.1128/jvi.00742-12

    Single-cell genomics-based analysis of virus–host interactions in marine surface bacterioplankton
    journal, April 2015

    • Labonté, Jessica M.; Swan, Brandon K.; Poulos, Bonnie
    • The ISME Journal, Vol. 9, Issue 11
    • DOI: 10.1038/ismej.2015.48

    Newly isolated Nodularia phage influences cyanobacterial community dynamics
    journal, December 2016

    • Coloma, S. E.; Dienstbier, A.; Bamford, D. H.
    • Environmental Microbiology, Vol. 19, Issue 1
    • DOI: 10.1111/1462-2920.13601

    Prochlorococcus: the structure and function of collective diversity
    journal, December 2014

    • Biller, Steven J.; Berube, Paul M.; Lindell, Debbie
    • Nature Reviews Microbiology, Vol. 13, Issue 1
    • DOI: 10.1038/nrmicro3378

    Intriguing Interaction of Bacteriophage-Host Association: An Understanding in the Era of Omics
    journal, April 2017

    • Parmar, Krupa M.; Gaikwad, Saurabh L.; Dhakephalkar, Prashant K.
    • Frontiers in Microbiology, Vol. 8
    • DOI: 10.3389/fmicb.2017.00559

    Expanding the Marine Virosphere Using Metagenomics
    journal, December 2013

    Diversity and evolutionary relationships of T7-like podoviruses infecting marine cyanobacteria: Evolutionary relationships of T7-like cyanopodoviruses
    journal, March 2013

    • Dekel-Bird, Naama P.; Avrani, Sarit; Sabehi, Gazalah
    • Environmental Microbiology, Vol. 15, Issue 5
    • DOI: 10.1111/1462-2920.12103

    Polar freshwater cyanophage S-EIV1 represents a new widespread evolutionary lineage of phages
    journal, March 2015

    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

    A New Freshwater Cyanosiphovirus Harboring Integrase
    journal, September 2018

    • Zhong, Kevin Xu; Suttle, Curtis A.; Baudoux, Anne-Claire
    • Frontiers in Microbiology, Vol. 9
    • DOI: 10.3389/fmicb.2018.02204

    Complete genome sequence of bacteriophage P8625, the first lytic phage that infects Verrucomicrobia
    journal, November 2015

    Genomic Characterization of Cyanophage vB_AphaS-CL131 Infecting Filamentous Diazotrophic Cyanobacterium Aphanizomenon flos-aquae Reveals Novel Insights into Virus-Bacterium Interactions
    journal, October 2018

    • Šulčius, Sigitas; Šimoliūnas, Eugenijus; Alzbutas, Gediminas
    • Applied and Environmental Microbiology, Vol. 85, Issue 1
    • DOI: 10.1128/aem.01311-18

    Metagenomic analysis of the viral community in Namib Desert hypoliths: Metaviromics of Namib hypoliths
    journal, July 2014

    • Adriaenssens, Evelien M.; Van Zyl, Lonnie; De Maayer, Pieter
    • Environmental Microbiology, Vol. 17, Issue 2
    • DOI: 10.1111/1462-2920.12528

    Cylindrospermopsis raciborskii Virus and host: genomic characterization and ecological relevance
    journal, October 2018

    • Martin, Robbie M.; Moniruzzaman, Mohammad; Mucci, Nicholas C.
    • Environmental Microbiology, Vol. 21, Issue 6
    • DOI: 10.1111/1462-2920.14425

    Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments: Comparative genomics of T4-like myoviruses
    journal, November 2010

    Prevalence of psbA-containing cyanobacterial podoviruses in the ocean
    journal, November 2013

    • Zheng, Qiang; Jiao, Nianzhi; Zhang, Rui
    • Scientific Reports, Vol. 3, Issue 1
    • DOI: 10.1038/srep03207

    A novel roseobacter phage possesses features of podoviruses, siphoviruses, prophages and gene transfer agents
    journal, July 2016

    • Zhan, Yuanchao; Huang, Sijun; Voget, Sonja
    • Scientific Reports, Vol. 6, Issue 1
    • DOI: 10.1038/srep30372

    A bioinformatic analysis of ribonucleotide reductase genes in phage genomes and metagenomes
    journal, January 2013

    • Dwivedi, Bhakti; Xue, Bingjie; Lundin, Daniel
    • BMC Evolutionary Biology, Vol. 13, Issue 1
    • DOI: 10.1186/1471-2148-13-33

    Assessing the Diversity and Specificity of Two Freshwater Viral Communities through Metagenomics
    journal, March 2012

    Is the Genetic Landscape of the Deep Subsurface Biosphere Affected by Viruses?
    journal, January 2011

    • Anderson, Rika E.; Brazelton, William J.; Baross, John A.
    • Frontiers in Microbiology, Vol. 2
    • DOI: 10.3389/fmicb.2011.00219

    Environmental bacteriophages: viruses of microbes in aquatic ecosystems
    journal, July 2014

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