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Title: Life-Style and Genome Structure of Marine Pseudoalteromonas Siphovirus B8b Isolated from the Northwestern Mediterranean Sea

Abstract

Marine viruses (phages) alter bacterial diversity and evolution with impacts on marine biogeochemical cycles, and yet few well-developed model systems limit opportunities for hypothesis testing. We isolate phage B8b from the Mediterranean Sea using Pseudoalteromonas sp. QC-44 as a host and characterize it using myriad techniques. Morphologically, phage B8b was classified as a member of the Siphoviridae family. One-step growth analyses showed that this siphovirus had a latent period of 70 min and released 172 new viral particles per cell. In the host range analysis against 89 bacterial host strains revealed that phage B8b infected 3 Pseudoalteromonas strains (52 tested, >99.9% 16S rRNA gene nucleotide identity) and 1 non-Pseudoaltermonas strain belonging to Alteromonas sp. (37 strains from 6 genera tested), which helps bound the phylogenetic distance possible in a phage-mediated horizontal gene transfer event. The Pseudoalteromonas phage B8b genome size was 42.7 kb, with clear structural and replication modules where the former were delineated leveraging identification of 16 structural genes by virion structural proteomics, only 4 of which had any similarity to known structural proteins. In nature, this phage was common in coastal marine environments in both photic and aphotic layers (found in 26.5% of available viral metagenomes), but notmore » abundant in any sample (average per sample abundance was 0.65% of the reads). Together these data improve our understanding of siphoviruses in nature, and provide foundational information for a new 'rare virosphere' phage-host model system.« less

Authors:
 [1];  [2];  [2];  [1];  [2];  [1];  [3];  [1];  [2];  [1];  [4]
  1. Inst. of Ocean Sciences (CSIC), Barcelona (Spain)
  2. Univ. of Arizona, Tucson, AZ (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. United States Geological Survey, Reston, VA (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE; Work for Others (WFO)
OSTI Identifier:
1286995
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Lara, Elena, Holmfeldt, Karin, Solonenko, Natalie, Sà, Elisabet Laia, Ignacio-Espinoza, J. Cesar, Cornejo-Castillo, Francisco M., Verberkmoes, Nathan C., Vaqué, Dolors, Sullivan, Matthew B., Acinas, Silvia G., and Kellogg, Christina A. Life-Style and Genome Structure of Marine Pseudoalteromonas Siphovirus B8b Isolated from the Northwestern Mediterranean Sea. United States: N. p., 2015. Web. doi:10.1371/journal.pone.0114829.
Lara, Elena, Holmfeldt, Karin, Solonenko, Natalie, Sà, Elisabet Laia, Ignacio-Espinoza, J. Cesar, Cornejo-Castillo, Francisco M., Verberkmoes, Nathan C., Vaqué, Dolors, Sullivan, Matthew B., Acinas, Silvia G., & Kellogg, Christina A. Life-Style and Genome Structure of Marine Pseudoalteromonas Siphovirus B8b Isolated from the Northwestern Mediterranean Sea. United States. https://doi.org/10.1371/journal.pone.0114829
Lara, Elena, Holmfeldt, Karin, Solonenko, Natalie, Sà, Elisabet Laia, Ignacio-Espinoza, J. Cesar, Cornejo-Castillo, Francisco M., Verberkmoes, Nathan C., Vaqué, Dolors, Sullivan, Matthew B., Acinas, Silvia G., and Kellogg, Christina A. Wed . "Life-Style and Genome Structure of Marine Pseudoalteromonas Siphovirus B8b Isolated from the Northwestern Mediterranean Sea". United States. https://doi.org/10.1371/journal.pone.0114829. https://www.osti.gov/servlets/purl/1286995.
@article{osti_1286995,
title = {Life-Style and Genome Structure of Marine Pseudoalteromonas Siphovirus B8b Isolated from the Northwestern Mediterranean Sea},
author = {Lara, Elena and Holmfeldt, Karin and Solonenko, Natalie and Sà, Elisabet Laia and Ignacio-Espinoza, J. Cesar and Cornejo-Castillo, Francisco M. and Verberkmoes, Nathan C. and Vaqué, Dolors and Sullivan, Matthew B. and Acinas, Silvia G. and Kellogg, Christina A.},
abstractNote = {Marine viruses (phages) alter bacterial diversity and evolution with impacts on marine biogeochemical cycles, and yet few well-developed model systems limit opportunities for hypothesis testing. We isolate phage B8b from the Mediterranean Sea using Pseudoalteromonas sp. QC-44 as a host and characterize it using myriad techniques. Morphologically, phage B8b was classified as a member of the Siphoviridae family. One-step growth analyses showed that this siphovirus had a latent period of 70 min and released 172 new viral particles per cell. In the host range analysis against 89 bacterial host strains revealed that phage B8b infected 3 Pseudoalteromonas strains (52 tested, >99.9% 16S rRNA gene nucleotide identity) and 1 non-Pseudoaltermonas strain belonging to Alteromonas sp. (37 strains from 6 genera tested), which helps bound the phylogenetic distance possible in a phage-mediated horizontal gene transfer event. The Pseudoalteromonas phage B8b genome size was 42.7 kb, with clear structural and replication modules where the former were delineated leveraging identification of 16 structural genes by virion structural proteomics, only 4 of which had any similarity to known structural proteins. In nature, this phage was common in coastal marine environments in both photic and aphotic layers (found in 26.5% of available viral metagenomes), but not abundant in any sample (average per sample abundance was 0.65% of the reads). Together these data improve our understanding of siphoviruses in nature, and provide foundational information for a new 'rare virosphere' phage-host model system.},
doi = {10.1371/journal.pone.0114829},
journal = {PLoS ONE},
number = 1,
volume = 10,
place = {United States},
year = {Wed Jan 14 00:00:00 EST 2015},
month = {Wed Jan 14 00:00:00 EST 2015}
}

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Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses
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Viruses manipulate the marine environment
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Abundant SAR11 viruses in the ocean
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Viral tagging reveals discrete populations in Synechococcus viral genome sequence space
journal, July 2014

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Viral metagenomics
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Site-specific molecular analysis of the bacteriota on worn spectacles
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Twelve previously unknown phage genera are ubiquitous in global oceans
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Genomic analysis of uncultured marine viral communities
journal, October 2002

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The rapid generation of mutation data matrices from protein sequences
journal, January 1992


Heuristic approach to deriving models for gene finding
journal, October 1999


Bacteriophage T4 Development Depends on the Physiology of its Host Escherichia Coli
journal, January 1997


Virus DNA packaging: the strategy used by phage ?
journal, June 1995


Annual changes of bacterial mortality due to viruses and protists in an oligotrophic coastal environment (NW Mediterranean)
journal, May 2009


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


Isolation of New Stenotrophomonas Bacteriophages and Genomic Characterization of Temperate Phage S1
journal, October 2008

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Randomly Amplified Polymorphic DNA PCR as a Tool for Assessment of Marine Viral Richness
journal, March 2008

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Gene Transfer by Transduction in the Marine Environment
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Isolation and characterization of a generalized transducing phage for Xanthomonas campestris pv. campestris.
journal, January 1994


The Temperate Marine Phage ΦHAP-1 of Halomonas aquamarina Possesses a Linear Plasmid-Like Prophage Genome
journal, April 2008

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Expression and Functional Characterization of the First Bacteriophage-Encoded Chaperonin
journal, July 2012

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Complete Genome Sequence of Temperate Bacteriophage AcaML1 from the Extreme Acidophile Acidithiobacillus caldus ATCC 51756
journal, October 2012

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Phages and the Evolution of Bacterial Pathogens: from Genomic Rearrangements to Lysogenic Conversion
journal, September 2004


The Uncultured Microbial Majority
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Metabolic reprogramming by viruses in the sunlit and dark ocean
journal, January 2013


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


The Sorcerer II Global Ocean Sampling Expedition: Metagenomic Characterization of Viruses within Aquatic Microbial Samples
journal, January 2008


Phage Morphology Recapitulates Phylogeny: The Comparative Genomics of a New Group of Myoviruses
journal, July 2012


Integrated Metagenomics/Metaproteomics Reveals Human Host-Microbiota Signatures of Crohn's Disease
journal, November 2012


Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters
journal, July 2003

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Annual variability in light modulation of bacterial heterotrophic activity in surface northwestern Mediterranean waters
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Prediction of effective genome size in metagenomic samples
text, January 2007


Exploring the Vast Diversity of Marine Viruses
journal, June 2007


Gene swapping in the dead zone
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Works referencing / citing this record:

Characterization and Complete Genome Sequence of a Novel Siphoviridae Bacteriophage BS5
journal, April 2017


Characterization and Genome Analysis of a Novel Alteromonas Phage JH01 Isolated from the Qingdao Coast of China
journal, August 2019


Phage-specific metabolic reprogramming of virocells
journal, January 2020

  • Howard-Varona, Cristina; Lindback, Morgan M.; Bastien, G. Eric
  • The ISME Journal, Vol. 14, Issue 4
  • DOI: 10.1038/s41396-019-0580-z

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

Microscale ecology regulates particulate organic matter turnover in model marine microbial communities
text, January 2018


Phage-specific metabolic reprogramming of virocells
journal, January 2020

  • Howard-Varona, Cristina; Lindback, Morgan M.; Bastien, G. Eric
  • The ISME Journal, Vol. 14, Issue 4
  • DOI: 10.1038/s41396-019-0580-z

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