Evidence for shared ancestry between Actinobacteria and Firmicutes bacteriophages

10.24072/pcjournal.25 - Peer Community Journal, Volume 1 (2021), article no. e16.

Get full text PDF Peer reviewed and recommended by PCI

Bacteriophages typically infect a small set of related bacterial strains. The transfer of bacteriophages between more distant clades of bacteria has often been postulated, but remains mostly unaddressed. In this work we leverage the sequencing of a novel cluster of phages infecting Streptomyces bacteria and the availability of large numbers of complete phage genomes in public repositories to address this question. Using phylogenetic and comparative genomics methods, we show that several clusters of Actinobacteria-infecting phages are more closely related between them, and with a small group of Firmicutes phages, than with any other actinobacteriophage lineage. These data indicate that this heterogeneous group of phages shares a common ancestor with well-defined genome structure. Analysis of genomic %GC content and codon usage bias shows that these actinobacteriophages are poorly adapted to their Actinobacteria hosts, suggesting that this phage lineage could have originated in an ancestor of the Firmicutes, adapted to the low %GC content members of this phylum, and later migrated to the Actinobacteria, or that selective pressure for enhanced translational throughput is significantly lower for phages infecting Actinobacteria hosts.

Published online:
DOI: 10.24072/pcjournal.25
Koert, Matthew 1; López-Pérez, Júlia 2; Mattson, Courtney 1; Caruso, Steven 1; Erill, Ivan 2, 1

1 Department of Biological Sciences, University of Maryland Baltimore County (UMBC), Baltimore, MD (USA)
2 Departament de Genètica i Microbiologia, Universitat Autònoma de Barcelona, Bellaterra, Spain
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Koert, Matthew and L\'opez-P\'erez, J\'ulia and Mattson, Courtney and Caruso, Steven and Erill, Ivan},
     title = {Evidence for shared ancestry between {Actinobacteria} and {Firmicutes} bacteriophages},
     journal = {Peer Community Journal},
     eid = {e16},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.25},
     url = {}
AU  - Koert, Matthew
AU  - López-Pérez, Júlia
AU  - Mattson, Courtney
AU  - Caruso, Steven
AU  - Erill, Ivan
TI  - Evidence for shared ancestry between Actinobacteria and Firmicutes bacteriophages
JO  - Peer Community Journal
PY  - 2021
DA  - 2021///
VL  - 1
PB  - Peer Community In
UR  -
UR  -
DO  - 10.24072/pcjournal.25
ID  - 10_24072_pcjournal_25
ER  - 
%0 Journal Article
%A Koert, Matthew
%A López-Pérez, Júlia
%A Mattson, Courtney
%A Caruso, Steven
%A Erill, Ivan
%T Evidence for shared ancestry between Actinobacteria and Firmicutes bacteriophages
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%R 10.24072/pcjournal.25
%F 10_24072_pcjournal_25
Koert, Matthew; López-Pérez, Júlia; Mattson, Courtney; Caruso, Steven; Erill, Ivan. Evidence for shared ancestry between Actinobacteria and Firmicutes bacteriophages. Peer Community Journal, Volume 1 (2021), article  no. e16. doi : 10.24072/pcjournal.25.

Peer reviewed and recommended by PCI : 10.24072/pci.genomics.100003

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Bardina, C.; Colom, J.; Spricigo, D. A.; Otero, J.; Sánchez-Osuna, M.; Cortés, P.; Llagostera, M. Genomics of Three New Bacteriophages Useful in the Biocontrol of Salmonella, Frontiers in Microbiology, Volume 7 (2016) | DOI

[2] Benson, D. A.; Cavanaugh, M.; Clark, K.; Karsch-Mizrachi, I.; Lipman, D. J.; Ostell, J.; Sayers, E. W. GenBank, Nucleic Acids Research, Volume 45 (2016) no. D1 | DOI

[3] Bin Jang, H.; Bolduc, B.; Zablocki, O.; Kuhn, J. H.; Roux, S.; Adriaenssens, E. M.; Brister, J. R.; Kropinski, A. M.; Krupovic, M.; Lavigne, R.; Turner, D.; Sullivan, M. B. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks, Nature Biotechnology, Volume 37 (2019) no. 6, pp. 632-639 | DOI

[4] Blocker, D.; Koert, M.; Mattson, C.; Patel, H.; Patel, P.; Patel, R.; Paudel, H.; Erill, I.; Caruso, S. M. Complete Genome Sequences of Six BI Cluster Streptomyces Bacteriophages, HotFries, Moozy, Rainydai, RavenPuff, Scap1, and SenditCS, Microbiology Resource Announcements, Volume 7 (2017) no. 12 | DOI

[5] Brown, C. T.; Olm, M. R.; Thomas, B. C.; Banfield, J. F. Measurement of bacterial replication rates in microbial communities, Nature Biotechnology, Volume 34 (2016) no. 12, pp. 1256-1263 | DOI

[6] Caruso, S. M.; deCarvalho, T. N.; Huynh, A.; Morcos, G.; Kuo, N.; Parsa, S.; Erill, I. A Novel Genus of Actinobacterial Tectiviridae, Viruses, Volume 11 (2019) no. 12 | DOI

[7] Casjens, S. R. Comparative genomics and evolution of the tailed-bacteriophages, Current Opinion in Microbiology, Volume 8 (2005) no. 4, pp. 451-458 | DOI

[8] Casjens, S. R.; Gilcrease, E. B.; Winn-Stapley, D. A.; Schicklmaier, P.; Schmieger, H.; Pedulla, M. L.; Ford, M. E.; Houtz, J. M.; Hatfull, G. F.; Hendrix, R. W. The Generalized Transducing Salmonella Bacteriophage ES18: Complete Genome Sequence and DNA Packaging Strategy, Journal of Bacteriology, Volume 187 (2005) no. 3, pp. 1091-1104 | DOI

[9] Castresana, J. Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis, Molecular Biology and Evolution, Volume 17 (2000) no. 4, pp. 540-552 | DOI

[10] Chiura, H. Generalized gene transfer by virus-like particles from marine bacteria, Aquatic Microbial Ecology, Volume 13 (1997), pp. 75-83 | DOI

[11] Cornuault, J. K.; Petit, M.-A.; Mariadassou, M.; Benevides, L.; Moncaut, E.; Langella, P.; Sokol, H.; De Paepe, M. Phages infecting Faecalibacterium prausnitzii belong to novel viral genera that help to decipher intestinal viromes, Microbiome, Volume 6 (2018) | DOI

[12] Cresawn, S. G.; Bogel, M.; Day, N.; Jacobs-Sera, D.; Hendrix, R. W.; Hatfull, G. F. Phamerator: a bioinformatic tool for comparative bacteriophage genomics, BMC Bioinformatics, Volume 12 (2011) | DOI

[13] Dodd, I. B.; Egan, J. Improved detection of helix-turn-helix DNA-binding motifs in protein sequences, Nucleic Acids Research, Volume 18 (1990) no. 17, pp. 5019-5026 | DOI

[14] Eddy, S. R. Accelerated Profile HMM Searches, PLoS Computational Biology, Volume 7 (2011) no. 10 | DOI

[15] Erill, I.; Caruso, S. M. Genome Sequence of Bacillus cereus Group Phage SalinJah, Genome Announcements, Volume 4 (2016) no. 5 | DOI

[16] Flores, C. O.; Meyer, J. R.; Valverde, S.; Farr, L.; Weitz, J. S. Statistical structure of host-phage interactions, Proceedings of the National Academy of Sciences, Volume 108 (2011) no. 28 | DOI

[17] Fokine, A.; Rossmann, M. G. Molecular architecture of tailed double-stranded DNA phages, Bacteriophage, Volume 4 (2014) no. 2 | DOI

[18] Garneau, J. E.; Tremblay, D. M.; Moineau, S. Characterization of 1706, a virulent phage from Lactococcus lactis with similarities to prophages from other Firmicutes, Virology, Volume 373 (2008) no. 2, pp. 298-309 | DOI

[19] Gascuel, O. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data, Molecular Biology and Evolution, Volume 14 (1997) no. 7, pp. 685-695 | DOI

[20] Gibson, B.; Wilson, D. J.; Feil, E.; Eyre-Walker, A. The distribution of bacterial doubling times in the wild, Proceedings of the Royal Society B: Biological Sciences, Volume 285 (2018) no. 1880 | DOI

[21] Iyer, L. M.; Koonin, E. V.; Aravind, L. Evolutionary connection between the catalytic subunits of DNA- dependent RNA polymerases and eukaryotic RNA-dependent RNA polymerases and the origin of RNA polymerases, BMC Structural Biology, Volume 3 (2003) no. 1 | DOI

[22] Kloepper, T. H.; Huson, D. H. Drawing explicit phylogenetic networks and their integration into SplitsTree, BMC Evolutionary Biology, Volume 8 (2008) no. 1 | DOI

[23] Kot, W.; Neve, H.; Vogensen, F. K.; Heller, K. J.; Sørensen, S. J.; Hansen, L. H. Complete Genome Sequences of Four Novel Lactococcus lactis Phages Distantly Related to the Rare 1706 Phage Species, Genome Announcements, Volume 2 (2014) no. 4 | DOI

[24] Lamine, J. G.; DeJong, R. J.; Nelesen, S. M. PhamDB: a web-based application for building Phamerator databases, Bioinformatics, Volume 32 (2016) no. 13, pp. 2026-2028 | DOI

[25] Le, S. Q.; Dang, C. C.; Gascuel, O. Modeling Protein Evolution with Several Amino Acid Replacement Matrices Depending on Site Rates, Molecular Biology and Evolution, Volume 29 (2012) no. 10, pp. 2921-2936 | DOI

[26] Lefort, V.; Desper, R.; Gascuel, O. FastME 2.0: A Comprehensive, Accurate, and Fast Distance-Based Phylogeny Inference Program: Table 1., Molecular Biology and Evolution, Volume 32 (2015) no. 10, pp. 2798-2800 | DOI

[27] Lopes, A.; Tavares, P.; Petit, M.-A.; Guérois, R.; Zinn-Justin, S. Automated classification of tailed bacteriophages according to their neck organization, BMC Genomics, Volume 15 (2014) no. 1 | DOI

[28] Low, S. J.; Džunková, M.; Chaumeil, P.-A.; Parks, D. H.; Hugenholtz, P. Evaluation of a concatenated protein phylogeny for classification of tailed double-stranded DNA viruses belonging to the order Caudovirales, Nature Microbiology, Volume 4 (2019) no. 8, pp. 1306-1315 | DOI

[29] Meier-Kolthoff, J. P.; Auch, A. F.; Klenk, H.-P.; Göker, M. Genome sequence-based species delimitation with confidence intervals and improved distance functions, BMC Bioinformatics, Volume 14 (2013) no. 1 | DOI

[30] Meier-Kolthoff, J. P.; Göker, M. VICTOR: genome-based phylogeny and classification of prokaryotic viruses, Bioinformatics, Volume 33 (2017) no. 21, pp. 3396-3404 | DOI

[31] Merrill, B. D.; Ward, A. T.; Grose, J. H.; Hope, S. Software-based analysis of bacteriophage genomes, physical ends, and packaging strategies, BMC Genomics, Volume 17 (2016) no. 1 | DOI

[32] Minh, B. Q.; Nguyen, M. A. T.; von Haeseler, A. Ultrafast Approximation for Phylogenetic Bootstrap, Molecular Biology and Evolution, Volume 30 (2013) no. 5, pp. 1188-1195 | DOI

[33] Minh, B. Q.; Schmidt, H. A.; Chernomor, O.; Schrempf, D.; Woodhams, M. D.; von Haeseler, A.; Lanfear, R. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era, Molecular Biology and Evolution, Volume 37 (2020) no. 5, pp. 1530-1534 | DOI

[34] Müller, T.; Vingron, M. Modeling Amino Acid Replacement, Journal of Computational Biology, Volume 7 (2000) no. 6, pp. 761-776 | DOI

[35] Murooka, Y.; Takizawa, N.; Harada, T. Introduction of bacteriophage Mu into bacteria of various genera and intergeneric gene transfer by RP4::Mu., Journal of Bacteriology, Volume 145 (1981) no. 1, pp. 358-368 | DOI

[36] Narasimhan, G.; Bu, C.; Gao, Y.; Wang, X.; Xu, N.; Mathee, K. Mining Protein Sequences for Motifs, Journal of Computational Biology, Volume 9 (2002) no. 5, pp. 707-720 | DOI

[37] Nishimura, Y.; Yoshida, T.; Kuronishi, M.; Uehara, H.; Ogata, H.; Goto, S. ViPTree: the viral proteomic tree server, Bioinformatics, Volume 33 (2017) no. 15, pp. 2379-2380 | DOI

[38] O'Neill, P. K.; Or, M.; Erill, I. scnRCA: A Novel Method to Detect Consistent Patterns of Translational Selection in Mutationally-Biased Genomes, PLoS ONE, Volume 8 (2013) no. 10 | DOI

[39] Pedulla, M. L.; Ford, M. E.; Houtz, J. M.; Karthikeyan, T.; Wadsworth, C.; Lewis, J. A.; Jacobs-Sera, D.; Falbo, J.; Gross, J.; Pannunzio, N. R.; Brucker, W.; Kumar, V.; Kandasamy, J.; Keenan, L.; Bardarov, S.; Kriakov, J.; Lawrence, J. G.; Jacobs, W. R.; Hendrix, R. W.; Hatfull, G. F. Origins of Highly Mosaic Mycobacteriophage Genomes, Cell, Volume 113 (2003) no. 2, pp. 171-182 | DOI

[40] Pope, W. H.; Bowman, C. A.; Russell, D. A.; Jacobs-Sera, D.; Asai, D. J.; Cresawn, S. G.; Jacobs, W. R.; Hendrix, R. W.; Lawrence, J. G.; Hatfull, G. F. Whole genome comparison of a large collection of mycobacteriophages reveals a continuum of phage genetic diversity, eLife, Volume 4 (2015) | DOI

[41] Pope, W. H.; Jacobs-Sera, D. Annotation of Bacteriophage Genome Sequences Using DNA Master: An Overview, Methods in Molecular Biology, Springer New York, New York, NY, 2017, pp. 217-229 | DOI

[42] Pope, W. H.; Jacobs-Sera, D.; Best, A. A.; Broussard, G. W.; Connerly, P. L.; Dedrick, R. M.; Kremer, T. A.; Offner, S.; Ogiefo, A. H.; Pizzorno, M. C.; Rockenbach, K.; Russell, D. A.; Stowe, E. L.; Stukey, J.; Thibault, S. A.; Conway, J. F.; Hendrix, R. W.; Hatfull, G. F. Cluster J Mycobacteriophages: Intron Splicing in Capsid and Tail Genes, PLoS ONE, Volume 8 (2013) no. 7 | DOI

[43] Pope, W. H.; Mavrich, T. N.; Garlena, R. A.; Guerrero-Bustamante, C. A.; Jacobs-Sera, D.; Montgomery, M. T.; Russell, D. A.; Warner, M. H.; Hatfull, G. F. Bacteriophages of Gordonia spp. Display a Spectrum of Diversity and Genetic Relationships, mBio, Volume 8 (2017) no. 4 | DOI

[44] Ross, A.; Ward, S.; Hyman, P. More Is Better: Selecting for Broad Host Range Bacteriophages, Frontiers in Microbiology, Volume 7 (2016) | DOI

[45] Russell, D. A.; Hatfull, G. F. PhagesDB: the actinobacteriophage database, Bioinformatics, Volume 33 (2017) no. 5, pp. 784-786 | DOI

[46] Sharaf, A.; Oborník, M.; Hammad, A.; El-Afifi, S.; Marei, E. Characterization and comparative genomic analysis of virulent and temperateBacillus megateriumbacteriophages, PeerJ, Volume 6 (2018) | DOI

[47] Sievers, F.; Wilm, A.; Dineen, D.; Gibson, T. J.; Karplus, K.; Li, W.; Lopez, R.; McWilliam, H.; Remmert, M.; Söding, J.; Thompson, J. D.; Higgins, D. G. Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega, Molecular Systems Biology, Volume 7 (2011) no. 1 | DOI

[48] Snel, B.; Bork, P.; Huynen, M. A. Genome phylogeny based on gene content, Nature Genetics, Volume 21 (1999) no. 1, pp. 108-110 | DOI

[49] Soding, J.; Biegert, A.; Lupas, A. N. The HHpred interactive server for protein homology detection and structure prediction, Nucleic Acids Research, Volume 33 (2005) | DOI

[50] Vieira-Silva, S.; Rocha, E. P. C. The Systemic Imprint of Growth and Its Uses in Ecological (Meta)Genomics, PLoS Genetics, Volume 6 (2010) no. 1 | DOI

[51] Yutin, N.; Makarova, K. S.; Gussow, A. B.; Krupovic, M.; Segall, A.; Edwards, R. A.; Koonin, E. V. Discovery of an expansive bacteriophage family that includes the most abundant viruses from the human gut, Nature Microbiology, Volume 3 (2018), pp. 38-46 | DOI

Cited by Sources: