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

Gilbert, Rosalind A.; Kelly, William J.; Altermann, Eric; Leahy, Sinead C.; Minchin, Catherine; Ouwerkerk, Diane; Klieve, Athol V.

doi:10.3389/fmicb.2017.02340

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

Journal Article · Tue Dec 05 00:00:00 EST 2017 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2017.02340· OSTI ID:1524080

Gilbert, Rosalind A. ^[1]; Kelly, William J. ^[2]; Altermann, Eric ^[3]; Leahy, Sinead C. ^[4]; Minchin, Catherine ^[5]; Ouwerkerk, Diane ^[6]; Klieve, Athol V. ^[7]

Ecosciences Precinct, Brisbane, QLD (Australia). Dept. of Agriculture and Fisheries; Univ. of Queensland, St. Lucia, QLD (Australia). Queensland Alliance for Agriculture and Food Innovation
Donvis Ltd., Palmerston North (New Zealand)
Grasslands Research Centre, Palmerston North (New Zealand). AgResearch Limited; Massey Univ., Palmerston North (New Zealand). Riddet Inst.
Grasslands Research Centre, Palmerston North (New Zealand). AgResearch Limited; New Zealand Agricultural Greenhouse Gas Research Centre, Palmerston (New Zealand)
EcoSciences Precinct, Brisbane, QLD (Australia). Dept. of Agrculture and Fisheries
EcoSciences Precinct, Brisbane, QLD (Australia). Dept. of Agrculture and Fisheries; Univ. of Queensland, St. Lucia, QLD (Australia). Queensland Alliance for Agriculture and Food Innovation
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

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE

OSTI ID:: 1524080

Journal Information:: Frontiers in Microbiology, Vol. 8; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 19 works

Citation information provided by
Web of Science

References (83)

Bacteriophage T12 of Streptococcus pyogenes integrates into the gene encoding a serine tRNA McShan, W. Michael; Tang, Y. ‐F.; Ferretti, Joseph J. Molecular Microbiology, Vol. 23, Issue 4 https://doi.org/10.1046/j.1365-2958.1997.2591616.x	journal	February 1997
Complete genome sequence of bacteriophage P2559Y, a marine phage that infects Croceibacter atlanticus HTCC2559 Kang, Ilnam; Kang, Dongmin; Cho, Jang-Cheon Marine Genomics, Vol. 29 https://doi.org/10.1016/j.margen.2016.07.001	journal	October 2016
HAMAP in 2015: updates to the protein family classification and annotation system Pedruzzi, Ivo; Rivoire, Catherine; Auchincloss, Andrea H. Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1002	journal	October 2014
REBASE—a database for DNA restriction and modification: enzymes, genes and genomes Roberts, Richard J.; Vincze, Tamas; Posfai, Janos Nucleic Acids Research, Vol. 43, Issue D1, p. D298-D299 https://doi.org/10.1093/nar/gku1046	journal	November 2014
Comparative (Meta)genomic Analysis and Ecological Profiling of Human Gut-Specific Bacteriophage φB124-14 Ogilvie, Lesley A.; Caplin, Jonathan; Dedi, Cinzia PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0035053	journal	April 2012
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data Kearse, M.; Moir, R.; Wilson, A. Bioinformatics, Vol. 28, Issue 12 https://doi.org/10.1093/bioinformatics/bts199	journal	April 2012
Diversity and evolution of class 2 CRISPR–Cas systems Shmakov, Sergey; Smargon, Aaron; Scott, David Nature Reviews Microbiology, Vol. 15, Issue 3 https://doi.org/10.1038/nrmicro.2016.184	journal	January 2017
The Rumen Bacteria and Protozoa Hungate, R. E.; Bryant, M. P.; Mah, R. A. Annual Review of Microbiology, Vol. 18, Issue 1 https://doi.org/10.1146/annurev.mi.18.100164.001023	journal	October 1964
Identifying bacterial genes and endosymbiont DNA with Glimmer Delcher, Arthur L.; Bratke, Kirsten A.; Powers, Edwin C. Bioinformatics, Vol. 23, Issue 6 https://doi.org/10.1093/bioinformatics/btm009	journal	January 2007
Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology Gibson, Molly K.; Forsberg, Kevin J.; Dantas, Gautam The ISME Journal, Vol. 9, Issue 1 https://doi.org/10.1038/ismej.2014.106	journal	July 2014
Ruminal Viruses (Bacteriophages, Archaeaphages) Gilbert, Rosalind A.; Klieve, Athol V. Rumen Microbiology: From Evolution to Revolution https://doi.org/10.1007/978-81-322-2401-3_9	book	January 2015
Genetic homogeneity and phage susceptibility of ruminal strains of Streptococcus bovis isolated in Australia Klieve, A. V.; Heck, G. L.; Prance, M. A. Letters in Applied Microbiology, Vol. 29, Issue 2 https://doi.org/10.1046/j.1365-2672.1999.00596.x	journal	August 1999
A General Empirical Model of Protein Evolution Derived from Multiple Protein Families Using a Maximum-Likelihood Approach Whelan, Simon; Goldman, Nick Molecular Biology and Evolution, Vol. 18, Issue 5 https://doi.org/10.1093/oxfordjournals.molbev.a003851	journal	May 2001
CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats Grissa, I.; Vergnaud, G.; Pourcel, C. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm360	journal	May 2007
An Improved General Amino Acid Replacement Matrix Le, S. Q.; Gascuel, O. Molecular Biology and Evolution, Vol. 25, Issue 7 https://doi.org/10.1093/molbev/msn067	journal	April 2008
Characterization of the bacteriophage phi29-encoded protein p16.7: a membrane protein involved in phage DNA replication Meijer, Wilfried J. J.; Serna-Rico, Alejandro; Salas, Margarita Molecular Microbiology, Vol. 39, Issue 3 https://doi.org/10.1046/j.1365-2958.2001.02260.x	journal	February 2001
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J. Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680 https://doi.org/10.1093/nar/22.22.4673	journal	January 1994
Genomics, evolution, and molecular epidemiology of the Streptococcus bovis / Streptococcus equinus complex (SBSEC) Jans, Christoph; Meile, Leo; Lacroix, Christophe Infection, Genetics and Evolution, Vol. 33 https://doi.org/10.1016/j.meegid.2014.09.017	journal	July 2015
High-quality draft assemblies of mammalian genomes from massively parallel sequence data Gnerre, S.; MacCallum, I.; Przybylski, D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 4 https://doi.org/10.1073/pnas.1017351108	journal	December 2010
Isolation and characterization of lytic phages fromBacterioides ruminicola ssbrevis Klieve, Athol V.; Gregg, Keith; Bauchop, Tom Current Microbiology, Vol. 23, Issue 4 https://doi.org/10.1007/BF02092277	journal	October 1991
TIGRFAMs and Genome Properties in 2013 Haft, Daniel H.; Selengut, Jeremy D.; Richter, Roland A. Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1234	journal	November 2012
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Structural Analysis of a New Cryptic Plasmid pAR67 Isolated fromRuminococcus albusAR67 Ohara, Hiroki; Miyagi, Tomoko; Kaneichi, Koji Plasmid, Vol. 39, Issue 1 https://doi.org/10.1006/plas.1997.1324	journal	January 1998
Complete Genome Sequence of the Novel Phage MG-B1 Infecting Bacillus weihenstephanensis Redondo, R. A. F.; Kupczok, A.; Stift, G. Genome Announcements, Vol. 1, Issue 3 https://doi.org/10.1128/genomeA.00216-13	journal	May 2013
The role of Temperate Bacteriophage in the Production of Erythrogenic Toxin by Group a Streptococci Zabriskie, J. B. Journal of Experimental Medicine, Vol. 119, Issue 5 https://doi.org/10.1084/jem.119.5.761	journal	May 1964
PHASTER: a better, faster version of the PHAST phage search tool Arndt, David; Grant, Jason R.; Marcu, Ana Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw387	journal	May 2016
GAMOLA2, a Comprehensive Software Package for the Annotation and Curation of Draft and Complete Microbial Genomes Altermann, Eric; Lu, Jingli; McCulloch, Alan Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00346	journal	March 2017
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence Lowe, Todd M.; Eddy, Sean R. Nucleic Acids Research, Vol. 25, Issue 5 https://doi.org/10.1093/nar/25.5.0955	journal	March 1997
IMG: the integrated microbial genomes database and comparative analysis system Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1044	journal	December 2011
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
dbCAN: a web resource for automated carbohydrate-active enzyme annotation Yin, Yanbin; Mao, Xizeng; Yang, Jincai Nucleic Acids Research, Vol. 40, Issue W1 https://doi.org/10.1093/nar/gks479	journal	May 2012
Type II restriction endonucleases—a historical perspective and more Pingoud, Alfred; Wilson, Geoffrey G.; Wende, Wolfgang Nucleic Acids Research, Vol. 42, Issue 12 https://doi.org/10.1093/nar/gku447	journal	May 2014
A Taxonomic Review of Clostridium difficile Phages and Proposal of a Novel Genus, “Phimmp04likevirus” Hargreaves, Katherine; Clokie, Martha Viruses, Vol. 7, Issue 5 https://doi.org/10.3390/v7052534	journal	May 2015
Phage-bacteria relationships and CRISPR elements revealed by a metagenomic survey of the rumen microbiome: Rumen viral metagenome Berg Miller, Margret E.; Yeoman, Carl J.; Chia, Nicholas Environmental Microbiology, Vol. 14, Issue 1 https://doi.org/10.1111/j.1462-2920.2011.02593.x	journal	October 2011
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs Zerbino, D. R.; Birney, E. Genome Research, Vol. 18, Issue 5 https://doi.org/10.1101/gr.074492.107	journal	February 2008
Lysogeny in Streptococcus bovis Iverson, W. G.; Millis, Nancy F. Canadian Journal of Microbiology, Vol. 22, Issue 6 https://doi.org/10.1139/m76-123	journal	June 1976
progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement Darling, Aaron E.; Mau, Bob; Perna, Nicole T. PLoS ONE, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pone.0011147	journal	June 2010
Expanded microbial genome coverage and improved protein family annotation in the COG database Galperin, Michael Y.; Makarova, Kira S.; Wolf, Yuri I. Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1223	journal	November 2014
The Epigenomic Landscape of Prokaryotes Blow, Matthew J.; Clark, Tyson A.; Daum, Chris G. PLOS Genetics, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pgen.1005854	journal	February 2016
Characterization of Streptococcus bovis bacteriophages Iverson, W. G.; Millis, Nancy F. Canadian Journal of Microbiology, Vol. 22, Issue 6 https://doi.org/10.1139/m76-122	journal	June 1976
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
Comparative genome analysis of Streptococcus infantarius subsp. infantarius CJ18, an African fermented camel milk isolate with adaptations to dairy environment Jans, Christoph; Follador, Rainer; Hochstrasser, Mira BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-200	journal	January 2013
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
The Double-Stranded DNA Virosphere as a Modular Hierarchical Network of Gene Sharing Iranzo, Jaime; Krupovic, Mart; Koonin, Eugene V. mBio, Vol. 7, Issue 4 https://doi.org/10.1128/mBio.00978-16	journal	August 2016
Genome sequence of a serotype M3 strain of group A Streptococcus: Phage-encoded toxins, the high-virulence phenotype, and clone emergence Beres, S. B.; Sylva, G. L.; Barbian, K. D. Proceedings of the National Academy of Sciences, Vol. 99, Issue 15 https://doi.org/10.1073/pnas.152298499	journal	July 2002
Isolation and characterization of a new ruminal bacteriophage lytic toStreptococcus bovis Štyriak, Igor; Španová, Alena; Montagová, Hana Current Microbiology, Vol. 28, Issue 6 https://doi.org/10.1007/BF01570201	journal	June 1994
Complex pectin metabolism by gut bacteria reveals novel catalytic functions Ndeh, Didier; Rogowski, Artur; Cartmell, Alan Nature, Vol. 544, Issue 7648 https://doi.org/10.1038/nature21725	journal	March 2017
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen Krogh, Anders; Larsson, Björn; von Heijne, Gunnar Journal of Molecular Biology, Vol. 305, Issue 3 https://doi.org/10.1006/jmbi.2000.4315	journal	January 2001
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro Molecular Biology and Evolution, Vol. 33, Issue 7 https://doi.org/10.1093/molbev/msw054	journal	March 2016
Linking Virus Genomes with Host Taxonomy Mihara, Tomoko; Nishimura, Yosuke; Shimizu, Yugo Viruses, Vol. 8, Issue 3 https://doi.org/10.3390/v8030066	journal	March 2016
29 Family of Phages Meijer, W. J. J.; Horcajadas, J. A.; Salas, M. Microbiology and Molecular Biology Reviews, Vol. 65, Issue 2 https://doi.org/10.1128/mmbr.65.2.261-287.2001	journal	June 2001
Genomic structure of phage B40-8 of Bacteroides fragilis Puig, M.; Girones, R. Microbiology, Vol. 145, Issue 7 https://doi.org/10.1099/13500872-145-7-1661	journal	July 1999
Isolation and Characterization of Soil Bacteria That Define Terriglobus gen. nov., in the Phylum Acidobacteria Eichorst, S. A.; Breznak, J. A.; Schmidt, T. M. Applied and Environmental Microbiology, Vol. 73, Issue 8 https://doi.org/10.1128/AEM.02140-06	journal	February 2007
The other face of restriction: modification-dependent enzymes Loenen, Wil A. M.; Raleigh, Elisabeth A. Nucleic Acids Research, Vol. 42, Issue 1 https://doi.org/10.1093/nar/gkt747	journal	August 2013
Metagenomics of rumen bacteriophage from thirteen lactating dairy cattle Ross, Elizabeth M.; Petrovski, Steve; Moate, Peter J. BMC Microbiology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2180-13-242	journal	January 2013
CRISPR-Cas systems and RNA-guided interference: CRISPR-Cas systems and RNA-guided interference Barrangou, Rodolphe Wiley Interdisciplinary Reviews: RNA, Vol. 4, Issue 3 https://doi.org/10.1002/wrna.1159	journal	March 2013
Phage resistance and altered growth habit in a strain of Streptococcus bovis Klieve, Athol V.; Bauchop, Tom FEMS Microbiology Letters, Vol. 80, Issue 2-3 https://doi.org/10.1111/j.1574-6968.1991.tb04653.x	journal	May 1991
PHAST: A Fast Phage Search Tool Zhou, Y.; Liang, Y.; Lynch, K. H. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr485	journal	June 2011
Differential functional behavior of viral phi29, Nf and GA-1 SSB proteins Gascon, I. Nucleic Acids Research, Vol. 28, Issue 10 https://doi.org/10.1093/nar/28.10.2034	journal	May 2000
Bacteriophages Klieve, Athol V. Methods in Gut Microbial Ecology for Ruminants https://doi.org/10.1007/1-4020-3791-0_3	book	January 2005
Molecular Characterization of Podoviral Bacteriophages Virulent for Clostridium perfringens and Their Comparison with Members of the Picovirinae Volozhantsev, Nikolay V.; Oakley, Brian B.; Morales, Cesar A. PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0038283	journal	May 2012
Isolation of bacteriophages from the bovine rumen Adams, J. C.; Gazaway, J. A.; Brailsford, M. D. Experientia, Vol. 22, Issue 11 https://doi.org/10.1007/BF01901335	journal	November 1966
Some Morphological Types of Bacteriophages in Bovine Rumen Contents1 Paynter, M. J. B.; Ewert, D. L.; Chalupa, W. Applied Microbiology, Vol. 18, Issue 5 https://doi.org/10.1128/AEM.18.5.942-943.1969	journal	January 1969
REBASE—a database for DNA restriction and modification: enzymes, genes and genomes Roberts, Richard J.; Vincze, Tamas; Posfai, Janos Nucleic Acids Research, Vol. 38, Issue suppl_1 https://doi.org/10.1093/nar/gkp874	journal	October 2009
Molecular profiling of microbial community structure and their CAZymes via metagenomics, from Tsomgo lake in the Eastern Himalayas Rai, Aditi; Bhattacharjee, Arindam Archives of Microbiology, Vol. 203, Issue 6 https://doi.org/10.1007/s00203-021-02278-7	journal	April 2021
Coriander Genomics Database: a genomic, transcriptomic, and metabolic database for coriander Song, Xiaoming; Nie, Fulei; Chen, Wei Horticulture Research, Vol. 7, Issue 1 https://doi.org/10.1038/s41438-020-0261-0	journal	April 2020
An SHR–SCR module specifies legume cortical cell fate to enable nodulation Dong, Wentao; Zhu, Yayun; Chang, Huizhong Nature, Vol. 589, Issue 7843 https://doi.org/10.1038/s41586-020-3016-z	journal	December 2020
Draft Genome Sequence of Comamonas aquatilis Strain LK (= CSUR P6418 = CECT 9772), Isolated from the Planarian Schmidtea mediterranea Kangale, Luis Johnson; Levasseur, Anthony; Raoult, Didier Microbiology Resource Announcements, Vol. 10, Issue 5 https://doi.org/10.1128/mra.00297-20	journal	February 2021
Fine-scale population structure and evidence for local adaptation in Australian giant black tiger shrimp (Penaeus monodon) using SNP analysis Vu, Nga T. T.; Zenger, Kyall R.; Guppy, Jarrod L. BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-07084-x	journal	September 2020
Comparative genome analysis of Streptococcus infantarius subsp. infantarius CJ18, an African fermented camel milk isolate with adaptations to dairy environment Jans, Christoph; Follador, Rainer; Hochstrasser, Mira ETH Zurich https://doi.org/10.3929/ethz-b-000066780	text	January 2013
The complete sequence of Bacillus phage φ 29 gene 16: a protein required for the genome encapsidation reaction Garvey, Kevin J.; Saedi, Mohammad S.; Ito, Junetsu Gene, Vol. 40, Issue 2-3 https://doi.org/10.1016/0378-1119(85)90054-x	journal	January 1985
Commensal Pseudomonas protect Arabidopsis thaliana from a coexisting pathogen via multiple lineage-dependent mechanisms Shalev, Or; Ashkenazy, Haim; Neumann, Manuela The ISME Journal, Vol. 16, Issue 5 https://doi.org/10.1038/s41396-021-01168-6	journal	December 2021
Characterization and phylogenetic analysis of the complete mitochondrial genome of the pathogenic fungus Ilyonectria destructans Androsiuk, Piotr; Okorski, Adam; Paukszto, Łukasz Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-05428-z	journal	February 2022
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence Lowe, Todd M.; Eddy, Sean R. Nucleic Acids Research, Vol. 25, Issue 5 https://doi.org/10.1093/nar/25.5.955	journal	March 1997
Type II restriction endonucleases — a historical perspective and more Pingoud, Alfred; Wilson, Geoffrey G.; Wende, Wolfgang Nucleic Acids Research, Vol. 44, Issue 16 https://doi.org/10.1093/nar/gkw513	journal	June 2016
Bacteriophages that infect the cellulolytic ruminal bacterium Ruminococcus albus AR67 Klieve, A. V.; Bain, P. A.; Yokoyama, M. T. Letters in Applied Microbiology, Vol. 38, Issue 4 https://doi.org/10.1111/j.1472-765x.2004.01493.x	journal	April 2004
Morphological diversity of ruminal bacteriophages from sheep and cattle. Klieve, A. V.; Bauchop, T. Applied and Environmental Microbiology, Vol. 54, Issue 6 https://doi.org/10.1128/aem.54.6.1637-1641.1988	journal	January 1988
Inducible bacteriophages from ruminal bacteria. Klieve, A. V.; Hudman, J. F.; Bauchop, T. Applied and Environmental Microbiology, Vol. 55, Issue 6 https://doi.org/10.1128/aem.55.6.1630-1634.1989	journal	January 1989
Estimation of ruminal bacteriophage numbers by pulsed-field gel electrophoresis and laser densitometry. Klieve, A. V.; Swain, R. A. Applied and Environmental Microbiology, Vol. 59, Issue 7 https://doi.org/10.1128/aem.59.7.2299-2303.1993	journal	January 1993
Diversity of Bacteroides fragilisStrains in Their Capacity To Recover Phages from Human and Animal Wastes and from Fecally Polluted Wastewater Puig, Anna; Queralt, Nuria; Jofre, Juan Applied and Environmental Microbiology, Vol. 65, Issue 4 https://doi.org/10.1128/aem.65.4.1772-1776.1999	journal	April 1999
Some Morphological Types of Bacteriophages in Bovine Rumen Contents Paynter, M. J. B.; Ewert, D. L.; Chalupa, W. Applied Microbiology, Vol. 18, Issue 5 https://doi.org/10.1128/am.18.5.942-943.1969	journal	November 1969
Draft Genomes of Two Strains of Flavobacterium Isolated from Lake Washington Sediment McTaggart, Tami L.; Shapiro, Nicole; Woyke, Tanja Genome Announcements, Vol. 3, Issue 1 https://doi.org/10.1128/genomea.01597-14	journal	February 2015

Cited By (5)

Review: Ruminal microbiome and microbial metabolome: effects of diet and ruminant host Newbold, C. J.; Ramos-Morales, E. animal, Vol. 14, Issue S1 https://doi.org/10.1017/s1751731119003252	journal	February 2020
Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem Solden, Lindsey M.; Naas, Adrian E.; Roux, Simon Nature Microbiology, Vol. 3, Issue 11 https://doi.org/10.1038/s41564-018-0225-4	journal	October 2018
Addressing Global Ruminant Agricultural Challenges Through Understanding the Rumen Microbiome: Past, Present, and Future Huws, Sharon A.; Creevey, Christopher J.; Oyama, Linda B. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02161	journal	September 2018
Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber Hagen, Live H.; Brooke, Charles G.; Shaw, Claire A. The ISME Journal, Vol. 15, Issue 2 https://doi.org/10.1038/s41396-020-00769-x	journal	September 2020
1st German Phage Symposium—Conference Report Huber, Irene; Potapova, Katerina; Kuhn, Andreas Viruses, Vol. 10, Issue 4 https://doi.org/10.3390/v10040158	journal	March 2018