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Title: Three Prochlorococcus Cyanophage Genomes: Signature Features and Ecological Interpretations

Abstract

The oceanic cyanobacteria Prochlorococcus are globally important, ecologically diverse primary producers. It is thought that their viruses (phages) mediate population sizes and affect the evolutionary trajectories of their hosts. Here we present an analysis of genomes from three Prochlorococcus phages: a podovirus and two myoviruses. The morphology, overall genome features, and gene content of these phages suggest that they are quite similar to T7-like (P-SSP7) and T4-like (P-SSM2 and P-SSM4) phages. Using the existing phage taxonomic framework as a guideline, we examined genome sequences to establish ‘‘core’’ genes for each phage group. We found the podovirus contained 15 of 26 core T7-like genes and the two myoviruses contained 43 and 42 of 75 core T4-like genes. In addition to these core genes, each genome contains a significant number of ‘‘cyanobacterial’’ genes, i.e., genes with significant best BLAST hits to genes found in cyanobacteria. Some of these, we speculate, represent ‘‘signature’’ cyanophage genes. For example, all three phage genomes contain photosynthetic genes (psbA, hliP) that are thought to help maintain host photosynthetic activity during infection, as well as an aldolase family gene (talC) that could facilitate alternative routes of carbon metabolism during infection. The podovirus genome also contains an integrase genemore » (int) and other features that suggest it is capable of integrating into its host. If indeed it is, this would be unprecedented among cultured T7-like phages or marine cyanophages and would have significant evolutionary and ecological implications for phage and host. Further, both myoviruses contain phosphate-inducible genes (phoH and pstS) that are likely to be important for phage and host responses to phosphate stress, a commonly limiting nutrient in marine systems. Thus, these marine cyanophages appear to be variations of two well-known phages—T7 and T4—but contain genes that, if functional, reflect adaptations for infection of photosynthetic hosts in low-nutrient oceanic environments.« less

Authors:
 [1];  [2];  [3];  [4];  [5]
+ Show Author Affiliations
  1. Woods Hole Oceanographic Institution, Woods Hole, MA (United States). Joint Program in Biological Oceanography; Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
  2. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Civil and Environmental Engineering
  3. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Biology
  4. San Diego State Univ., CA (United States). Dept. of Biology
  5. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Civil and Environmental Engineering and Dept. of Biology
Publication Date:
Research Org.:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); Stanford Univ., CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Science Foundation (NSF)
OSTI Identifier:
1627138
Grant/Contract Number:  
AC02-05CH11231; W-7405-ENG-48; AC03-76SF00098; W-7405-ENG-36; FC02-99ER62873; FG02-99ER62814; FG02-02ER63445; OCE-9820035
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Biology (Online)
Additional Journal Information:
Journal Name: PLoS Biology (Online); Journal Volume: 3; Journal Issue: 5; Journal ID: ISSN 1545-7885
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biochemistry & molecular biology; Life sciences & biomedicine - other topics; Bacteriophages; Viral genomics; Gene prediction; Cyanobacteria; Genomics; Sequence alignment; Nucleotides; Photosynthesis

Citation Formats

Sullivan, Matthew B., Coleman, Maureen L., Weigele, Peter, Rohwer, Forest, and Chisholm, Sallie W. Three Prochlorococcus Cyanophage Genomes: Signature Features and Ecological Interpretations. United States: N. p., 2005. Web. doi:10.1371/journal.pbio.0030144.
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Sullivan, Matthew B., Coleman, Maureen L., Weigele, Peter, Rohwer, Forest, & Chisholm, Sallie W. Three Prochlorococcus Cyanophage Genomes: Signature Features and Ecological Interpretations. United States. https://doi.org/10.1371/journal.pbio.0030144
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Sullivan, Matthew B., Coleman, Maureen L., Weigele, Peter, Rohwer, Forest, and Chisholm, Sallie W. Tue . "Three Prochlorococcus Cyanophage Genomes: Signature Features and Ecological Interpretations". United States. https://doi.org/10.1371/journal.pbio.0030144. https://www.osti.gov/servlets/purl/1627138.
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@article{osti_1627138,
title = {Three Prochlorococcus Cyanophage Genomes: Signature Features and Ecological Interpretations},
author = {Sullivan, Matthew B. and Coleman, Maureen L. and Weigele, Peter and Rohwer, Forest and Chisholm, Sallie W.},
abstractNote = {The oceanic cyanobacteria Prochlorococcus are globally important, ecologically diverse primary producers. It is thought that their viruses (phages) mediate population sizes and affect the evolutionary trajectories of their hosts. Here we present an analysis of genomes from three Prochlorococcus phages: a podovirus and two myoviruses. The morphology, overall genome features, and gene content of these phages suggest that they are quite similar to T7-like (P-SSP7) and T4-like (P-SSM2 and P-SSM4) phages. Using the existing phage taxonomic framework as a guideline, we examined genome sequences to establish ‘‘core’’ genes for each phage group. We found the podovirus contained 15 of 26 core T7-like genes and the two myoviruses contained 43 and 42 of 75 core T4-like genes. In addition to these core genes, each genome contains a significant number of ‘‘cyanobacterial’’ genes, i.e., genes with significant best BLAST hits to genes found in cyanobacteria. Some of these, we speculate, represent ‘‘signature’’ cyanophage genes. For example, all three phage genomes contain photosynthetic genes (psbA, hliP) that are thought to help maintain host photosynthetic activity during infection, as well as an aldolase family gene (talC) that could facilitate alternative routes of carbon metabolism during infection. The podovirus genome also contains an integrase gene (int) and other features that suggest it is capable of integrating into its host. If indeed it is, this would be unprecedented among cultured T7-like phages or marine cyanophages and would have significant evolutionary and ecological implications for phage and host. Further, both myoviruses contain phosphate-inducible genes (phoH and pstS) that are likely to be important for phage and host responses to phosphate stress, a commonly limiting nutrient in marine systems. Thus, these marine cyanophages appear to be variations of two well-known phages—T7 and T4—but contain genes that, if functional, reflect adaptations for infection of photosynthetic hosts in low-nutrient oceanic environments.},
doi = {10.1371/journal.pbio.0030144},
journal = {PLoS Biology (Online)},
number = 5,
volume = 3,
place = {United States},
year = {Tue Apr 19 00:00:00 EDT 2005},
month = {Tue Apr 19 00:00:00 EDT 2005}
}
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    Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism
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    A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans
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    Twelve previously unknown phage genera are ubiquitous in global oceans
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    Distinct Features of Cyanophage-encoded T-type Phycobiliprotein Lyase ΦCpeT: THE ROLE OF AUXILIARY METABOLIC GENES
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    Viruses in aquatic ecosystems: important advancements of the last 20 years and prospects for the future in the field of microbial oceanography and limnology
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    Microbial Dark Matter Investigations: How Microbial Studies Transform Biological Knowledge and Empirically Sketch a Logic of Scientific Discovery
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    Phage-bacteria interaction network in human oral microbiome: Human oral virome
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    Newly isolated Nodularia phage influences cyanobacterial community dynamics
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    Novel Caudovirales associated with Marine Group I Thaumarchaeota assembled from metagenomes
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    Pelagiphages in the Podoviridae family integrate into host genomes
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    Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake
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    Factors affecting virus dynamics and microbial host - virus interactions in marine environments
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    Cyanophage MazG is a pyrophosphohydrolase but unable to hydrolyse magic spot nucleotides
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    Marine cyanophages and light
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    Portal protein diversity and phage ecology: Portal protein diversity and phage ecology
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    Occurrence of phosphate acquisition genes in Prochlorococcus cells from different ocean regions
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    From small hosts come big viruses: the complete genome of a second Ostreococcus tauri virus, OtV-1
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    Diverse and dynamic populations of cyanobacterial podoviruses in the Chesapeake Bay unveiled through DNA polymerase gene sequences
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    The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’
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    Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments: Comparative genomics of T4-like myoviruses
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    Marine viruses and global climate change
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    Ecology of viruses in soils: Past, present and future perspectives
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    Isolation and genomic characterization of the first phage infecting Iodobacteria : ϕPLPE, a myovirus having a novel set of features
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    Genomic and Seasonal Variations among Aquatic Phages Infecting the Baltic Sea Gammaproteobacterium Rheinheimera sp. Strain BAL341
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    Genomic Characterization of Cyanophage vB_AphaS-CL131 Infecting Filamentous Diazotrophic Cyanobacterium Aphanizomenon flos-aquae Reveals Novel Insights into Virus-Bacterium Interactions
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    Development of phoH as a Novel Signature Gene for Assessing Marine Phage Diversity
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    • Goldsmith, Dawn B.; Crosti, Giuseppe; Dwivedi, Bhakti
    • Applied and Environmental Microbiology, Vol. 77, Issue 21
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    A Novel Cyanophage with a Cyanobacterial Nonbleaching Protein A Gene in the Genome
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    • Journal of Virology, Vol. 86, Issue 1
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    Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust
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    • Van Goethem, Marc W.; Swenson, Tami L.; Trubl, Gareth
    • mBio, Vol. 10, Issue 6
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    Genomic fluidity: an integrative view of gene diversity within microbial populations
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    • Kislyuk, Andrey O.; Haegeman, Bart; Bergman, Nicholas H.
    • BMC Genomics, Vol. 12, Issue 1
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    Genome organisation of the Acinetobacter lytic phage ZZ1 and comparison with other T4-like Acinetobacter phages
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    Comparative metagenomic analyses reveal viral-induced shifts of host metabolism towards nucleotide biosynthesis
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    • Enav, Hagay; Mandel-Gutfreund, Yael; Béjà, Oded
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    Prevalence and Evolution of Core Photosystem II Genes in Marine Cyanobacterial Viruses and Their Hosts
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    The Sorcerer II Global Ocean Sampling Expedition: Expanding the Universe of Protein Families
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    The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific
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    Expanding the Marine Virosphere Using Metagenomics
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    The Sorcerer II Global Ocean Sampling Expedition: Metagenomic Characterization of Viruses within Aquatic Microbial Samples
    journal, January 2008

    The Secret Life of the Anthrax Agent Bacillus anthracis: Bacteriophage-Mediated Ecological Adaptations
    journal, August 2009

    Evolutionary Strategies of Viruses, Bacteria and Archaea in Hydrothermal Vent Ecosystems Revealed through Metagenomics
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    Life-Style and Genome Structure of Marine Pseudoalteromonas Siphovirus B8b Isolated from the Northwestern Mediterranean Sea
    journal, January 2015

    Metagenomic Characterisation of the Viral Community of Lough Neagh, the Largest Freshwater Lake in Ireland
    journal, February 2016

    Gene Expression Patterns during Light and Dark Infection of Prochlorococcus by Cyanophage
    journal, October 2016

    The Ferrojan Horse Hypothesis: Iron-Virus Interactions in the Ocean
    journal, June 2016

    Reannotation of the Ribonucleotide Reductase in a Cyanophage Reveals Life History Strategies Within the Virioplankton
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    • Harrison, Amelia O.; Moore, Ryan M.; Polson, Shawn W.
    • Frontiers in Microbiology, Vol. 10
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    A Novel, Highly Related Jumbo Family of Bacteriophages That Were Isolated Against Erwinia
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    • Sharma, Ruchira; Pielstick, Brittany A.; Bell, Kimberly A.
    • Frontiers in Microbiology, Vol. 10
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    Metabolic Genes within Cyanophage Genomes: Implications for Diversity and Evolution
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    A Student’s Guide to Giant Viruses Infecting Small Eukaryotes: From Acanthamoeba to Zooxanthellae
    journal, March 2017

    • Wilhelm, Steven; Bird, Jordan; Bonifer, Kyle
    • Viruses, Vol. 9, Issue 3
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    Phages in nature
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    • Clokie, Martha R. J.; Millard, Andrew D.; Letarov, Andrey V.
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    Novel group of podovirus infecting the marine bacterium Alteromonas macleodii
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    Diversity and evolutionary relationships of T7-like podoviruses infecting marine cyanobacteria: Evolutionary relationships of T7-like cyanopodoviruses
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    A simple and efficient method for concentration of ocean viruses by chemical flocculation: Virus concentration by flocculation with iron
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    Bacterial Vesicles in Marine Ecosystems
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    Host-hijacking and planktonic piracy: how phages command the microbial high seas
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    • Warwick-Dugdale, Joanna; Buchholz, Holger H.; Allen, Michael J.
    • Virology Journal, Vol. 16, Issue 1
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    Jumbo Bacteriophages: An Overview
    journal, March 2017

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

    Abundant SAR11 viruses in the ocean
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    • Zhao, Yanlin; Temperton, Ben; Thrash, J. Cameron
    • Nature, Vol. 494, Issue 7437
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    Diel Infection of Cyanobacteria by Cyanophages
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    Bacteriophage behavioral ecology: How phages alter their bacterial host’s habits
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    • Hargreaves, Katherine R.; Kropinski, Andrew M.; Clokie, Martha RJ
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    Genomic plasticity in prokaryotes: the case of the square haloarchaeon
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    • Cuadros-Orellana, Sara; Martin-Cuadrado, Ana-Belen; Legault, Boris
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    Global abundance of microbial rhodopsins
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    Transcriptome dynamics of a broad host-range cyanophage and its hosts
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    • Doron, Shany; Fedida, Ayalla; Hernández-Prieto, Miguel A.
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    Challenges of ligand identification for the second wave of orphan riboswitch candidates
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    Assessment of viral community functional potential from viral metagenomes may be hampered by contamination with cellular sequences
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    • Roux, Simon; Krupovic, Mart; Debroas, Didier
    • Open Biology, Vol. 3, Issue 12
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    Targeted metagenomic recovery of four divergent viruses reveals shared and distinctive characteristics of giant viruses of marine eukaryotes
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    • Needham, David M.; Poirier, Camille; Hehenberger, Elisabeth
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    Genomic, transcriptomic, and structural analysis of Pseudomonas virus PA5oct highlights the molecular complexity among Jumbo phages
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    • Danis-Wlodarczyk, Katarzyna; Blasdel, Bob G.; Jang, Ho Bin
    • DOI: 10.1101/406421

    Portal protein diversity and phage ecology: Corrigendum
    journal, October 2011

    Metagenomic analysis of DNA viruses in a wastewater treatment plant in tropical climate: Viral metagenomics in a WWTP
    journal, October 2011

    A simple and efficient method for concentration of ocean viruses by chemical flocculation: Corrigendum
    journal, October 2011

    Viruses in aquatic ecosystems: important advancements of the last 20 years and prospects for the future in the field of microbial oceanography and limnology
    journal, June 2010

    • Jacquet, Stéphan; Miki, Takeshi; Noble, Rachel
    • Advances in Oceanography and Limnology, Vol. 1, Issue 1
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    Genomic and Seasonal Variations among Aquatic Phages Infecting the Baltic Sea Gammaproteobacterium Rheinheimera sp. Strain BAL341
    journal, July 2019

    • Nilsson, E.; Li, K.; Fridlund, J.
    • Applied and Environmental Microbiology, Vol. 85, Issue 18
    • DOI: 10.1128/aem.01003-19

    Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust
    journal, December 2019

    • Van Goethem, Marc W.; Swenson, Tami L.; Trubl, Gareth
    • mBio, Vol. 10, Issue 6
    • DOI: 10.1128/mbio.02287-19

    A supervised learning approach for taxonomic classification of core-photosystem-II genes and transcripts in the marine environment
    journal, January 2009

    • Tzahor, Shani; Man-Aharonovich, Dikla; Kirkup, Benjamin C.
    • BMC Genomics, Vol. 10, Issue 1
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    Genomic fluidity: an integrative view of gene diversity within microbial populations
    journal, January 2011

    • Kislyuk, Andrey O.; Haegeman, Bart; Bergman, Nicholas H.
    • BMC Genomics, Vol. 12, Issue 1
    • DOI: 10.1186/1471-2164-12-32

    Comparative analysis of two phenotypically-similar but genomically-distinct Burkholderia cenocepacia-specific bacteriophages
    journal, June 2012

    Genome organisation of the Acinetobacter lytic phage ZZ1 and comparison with other T4-like Acinetobacter phages
    journal, January 2014

    Putative prophages related to lytic tailless marine dsDNA phage PM2 are widespread in the genomes of aquatic bacteria
    journal, January 2007

    Identification and investigation of ORFans in the viral world
    journal, January 2008

    Genomes of the T4-related bacteriophages as windows on microbial genome evolution
    journal, October 2010

    • Petrov, Vasiliy M.; Ratnayaka, Swarnamala; Nolan, James M.
    • Virology Journal, Vol. 7, Issue 1
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    A Shigella boydii bacteriophage which resembles Salmonella phage ViI
    journal, May 2011

    Comparative metagenomic analyses reveal viral-induced shifts of host metabolism towards nucleotide biosynthesis
    journal, January 2014

    • Enav, Hagay; Mandel-Gutfreund, Yael; Béjà, Oded
    • Microbiome, Vol. 2, Issue 1
    • DOI: 10.1186/2049-2618-2-9

    Diversity and evolution of phycobilisomes in marine Synechococcus spp.: a comparative genomics study
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    Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes
    journal, January 2010

    Prevalence and Evolution of Core Photosystem II Genes in Marine Cyanobacterial Viruses and Their Hosts
    journal, July 2006

    Analysis and Phylogeny of Small Heat Shock Proteins from Marine Viruses and Their Cyanobacteria Host
    journal, November 2013

    Evolutionary Strategies of Viruses, Bacteria and Archaea in Hydrothermal Vent Ecosystems Revealed through Metagenomics
    journal, October 2014

    Metagenomic Characterisation of the Viral Community of Lough Neagh, the Largest Freshwater Lake in Ireland
    journal, February 2016

    Gene Expression Patterns during Light and Dark Infection of Prochlorococcus by Cyanophage
    journal, October 2016

    Diel Infection of Cyanobacteria by Cyanophages
    journal, January 2016

    The Ferrojan Horse Hypothesis: Iron-Virus Interactions in the Ocean
    journal, June 2016

    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
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    Extreme environments as potential drivers of convergent evolution by exaptation: the Atacama Desert Coastal Range case
    journal, January 2012

    • Azua-Bustos, Armando; González-Silva, Carlos; Arenas-Fajardo, Cristián
    • Frontiers in Microbiology, Vol. 3
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    Bacteriophage T7 DNA polymerase – sequenase
    journal, April 2014

    Genomic characteristics and environmental distributions of the uncultivated Far-T4 phages
    journal, March 2015

    Jumbo Bacteriophages: An Overview
    journal, March 2017

    Metagenomic Analysis of Virioplankton from the Pelagic Zone of Lake Baikal
    journal, October 2019

    • Potapov, Sergey A.; Tikhonova, Irina V.; Krasnopeev, Andrey Yu.
    • Viruses, Vol. 11, Issue 11
    • DOI: 10.3390/v11110991

    A Student’s Guide to Giant Viruses Infecting Small Eukaryotes: From Acanthamoeba to Zooxanthellae
    journal, March 2017

    • Wilhelm, Steven; Bird, Jordan; Bonifer, Kyle
    • Viruses, Vol. 9, Issue 3
    • DOI: 10.3390/v9030046

    Two Synechococcus genes, Two Different Effects on Cyanophage Infection
    journal, June 2017

    • Fedida, Ayalla; Lindell, Debbie
    • Viruses, Vol. 9, Issue 6
    • DOI: 10.3390/v9060136

    Enriching public descriptions of marine phages using the Genomic Standards Consortium MIGS standard
    journal, April 2011

    • Duhaime, Melissa Beth; Kottmann, Renzo; Field, Dawn
    • Standards in Genomic Sciences, Vol. 4, Issue 2
    • DOI: 10.4056/sigs.621069

    Bacteriophage behavioral ecology: How phages alter their bacterial host’s habits
    journal, May 2014

    • Hargreaves, Katherine R.; Kropinski, Andrew M.; Clokie, Martha RJ
    • Bacteriophage, Vol. 4, Issue 3
    • DOI: 10.4161/bact.29866

    Gene swapping in the dead zone
    journal, October 2014

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