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Title: Toward Understanding Phage:Host Interactions in the Rumen; Complete Genome Sequences of Lytic Phages Infecting Rumen Bacteria

Abstract

The rumen is known to harbor dense populations of bacteriophages (phages) predicted to be capable of infecting a diverse range of rumen bacteria. While bacterial genome sequencing projects are revealing the presence of phages which can integrate their DNA into the genome of their host to form stable, lysogenic associations, little is known of the genetics of phages which utilize lytic replication. These phages infect and replicate within the host, culminating in host lysis, and the release of progeny phage particles. While lytic phages for rumen bacteria have been previously isolated, their genomes have remained largely uncharacterized. Here we report the first complete genome sequences of lytic phage isolates specifically infecting three genera of rumen bacteria: Bacteroides, Ruminococcus, and Streptococcus. All phages were classified within the viral order Caudovirales and include two phage morphotypes, representative of the Siphoviridae and Podoviridae families. The phage genomes displayed modular organization and conserved viral genes were identified which enabled further classification and determination of closest phage relatives. Co-examination of bacterial host genomes led to the identification of several genes responsible for modulating phage:host interactions, including CRISPR/Cas elements and restriction-modification phage defense systems. These findings provide new genetic information and insights into how lytic phagesmore » may interact with bacteria of the rumen microbiome.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [7]
  1. Ecosciences Precinct, Brisbane, QLD (Australia). Dept. of Agriculture and Fisheries; Univ. of Queensland, St. Lucia, QLD (Australia). Queensland Alliance for Agriculture and Food Innovation
  2. Donvis Ltd., Palmerston North (New Zealand)
  3. Grasslands Research Centre, Palmerston North (New Zealand). AgResearch Limited; Massey Univ., Palmerston North (New Zealand). Riddet Inst.
  4. Grasslands Research Centre, Palmerston North (New Zealand). AgResearch Limited; New Zealand Agricultural Greenhouse Gas Research Centre, Palmerston (New Zealand)
  5. EcoSciences Precinct, Brisbane, QLD (Australia). Dept. of Agrculture and Fisheries
  6. EcoSciences Precinct, Brisbane, QLD (Australia). Dept. of Agrculture and Fisheries; Univ. of Queensland, St. Lucia, QLD (Australia). Queensland Alliance for Agriculture and Food Innovation
  7. Univ. of Queensland, St. Lucia, QLD (Australia). Queensland Alliance for Agriculture and Food Innovation; Univ. of Queensland, Gatton, QLD (Australia). School of Agriculture and Food Sciences
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
Sponsoring Org.:
USDOE
OSTI Identifier:
1524080
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; bacteriophage; phage; rumen; Streptococcus; Bacteroides; Ruminococcus; Siphoviridae; Podoviridae

Citation Formats

Gilbert, Rosalind A., Kelly, William J., Altermann, Eric, Leahy, Sinead C., Minchin, Catherine, Ouwerkerk, Diane, and Klieve, Athol V. Toward Understanding Phage:Host Interactions in the Rumen; Complete Genome Sequences of Lytic Phages Infecting Rumen Bacteria. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.02340.
Gilbert, Rosalind A., Kelly, William J., Altermann, Eric, Leahy, Sinead C., Minchin, Catherine, Ouwerkerk, Diane, & Klieve, Athol V. Toward Understanding Phage:Host Interactions in the Rumen; Complete Genome Sequences of Lytic Phages Infecting Rumen Bacteria. United States. https://doi.org/10.3389/fmicb.2017.02340
Gilbert, Rosalind A., Kelly, William J., Altermann, Eric, Leahy, Sinead C., Minchin, Catherine, Ouwerkerk, Diane, and Klieve, Athol V. Tue . "Toward Understanding Phage:Host Interactions in the Rumen; Complete Genome Sequences of Lytic Phages Infecting Rumen Bacteria". United States. https://doi.org/10.3389/fmicb.2017.02340. https://www.osti.gov/servlets/purl/1524080.
@article{osti_1524080,
title = {Toward Understanding Phage:Host Interactions in the Rumen; Complete Genome Sequences of Lytic Phages Infecting Rumen Bacteria},
author = {Gilbert, Rosalind A. and Kelly, William J. and Altermann, Eric and Leahy, Sinead C. and Minchin, Catherine and Ouwerkerk, Diane and Klieve, Athol V.},
abstractNote = {The rumen is known to harbor dense populations of bacteriophages (phages) predicted to be capable of infecting a diverse range of rumen bacteria. While bacterial genome sequencing projects are revealing the presence of phages which can integrate their DNA into the genome of their host to form stable, lysogenic associations, little is known of the genetics of phages which utilize lytic replication. These phages infect and replicate within the host, culminating in host lysis, and the release of progeny phage particles. While lytic phages for rumen bacteria have been previously isolated, their genomes have remained largely uncharacterized. Here we report the first complete genome sequences of lytic phage isolates specifically infecting three genera of rumen bacteria: Bacteroides, Ruminococcus, and Streptococcus. All phages were classified within the viral order Caudovirales and include two phage morphotypes, representative of the Siphoviridae and Podoviridae families. The phage genomes displayed modular organization and conserved viral genes were identified which enabled further classification and determination of closest phage relatives. Co-examination of bacterial host genomes led to the identification of several genes responsible for modulating phage:host interactions, including CRISPR/Cas elements and restriction-modification phage defense systems. These findings provide new genetic information and insights into how lytic phages may interact with bacteria of the rumen microbiome.},
doi = {10.3389/fmicb.2017.02340},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {Tue Dec 05 00:00:00 EST 2017},
month = {Tue Dec 05 00:00:00 EST 2017}
}

Journal Article:
Free Publicly Available Full Text
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Cited by: 19 works
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Figures / Tables:

TABLE 1 TABLE 1 : Summary of original phage descriptions (classification according to viral particle morphology, genome lengths calculated by restriction enzyme digestion of phage genomic DNA and particle dimensions) and description of bacterial host strains.

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The Rumen Bacteria and Protozoa
journal, October 1964


BLAST+: architecture and applications
journal, January 2009

  • Camacho, Christiam; Coulouris, George; Avagyan, Vahram
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-421

Metagenomics of rumen bacteriophage from thirteen lactating dairy cattle
journal, January 2013

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  • BMC Microbiology, Vol. 13, Issue 1
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The Epigenomic Landscape of Prokaryotes
journal, February 2016


Comparative (Meta)genomic Analysis and Ecological Profiling of Human Gut-Specific Bacteriophage φB124-14
journal, April 2012


Molecular Characterization of Podoviral Bacteriophages Virulent for Clostridium perfringens and Their Comparison with Members of the Picovirinae
journal, May 2012


Linking Virus Genomes with Host Taxonomy
journal, March 2016

  • Mihara, Tomoko; Nishimura, Yosuke; Shimizu, Yugo
  • Viruses, Vol. 8, Issue 3
  • DOI: 10.3390/v8030066

Works referencing / citing this record:

Review: Ruminal microbiome and microbial metabolome: effects of diet and ruminant host
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Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber
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Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem
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