Biogeography and taxonomic overview of terrestrial hot spring thermophilic phages
Bacterial viruses (“phages”) play important roles in the regulation and evolution of microbial communities in most ecosystems. Terrestrial hot springs typically contain thermophilic bacterial communities, but the diversity and impacts of its associated viruses (“thermophilic phages”) are largely unexplored. Here, we provide a taxonomic overview of phages that have been isolated strictly from terrestrial hot springs around the world. In addition, we placed 17 thermophilic phage genomes in a global phylogenomic context to detect evolutionary patterns. Thermophilic phages have diverse morphologies (e.g., tailed, filamentous), unique virion structures (e.g., extremely long tailed siphoviruses), and span five taxonomic families encompassing strictly thermophilic phage genera. Within the phage proteomic tree, six thermophilic phage-related clades were identified, with evident genomic relatedness between thermophilic phages and archaeal viruses. Moreover, whole proteome analyses showed clustering between phages that infect distinct host phyla, such as Firmicutes and Deinococcus–Thermus. The potential for discovery of novel phage-host systems in terrestrial hot springs remain mostly untapped, thus additional emphasis on thermophilic phages in ecological prospecting is encouraged to gain insights into the microbial population dynamics of these environments.
KeywordsThermophilic phage Hot spring Viral metagenomics Thermus Gammasphaerolipovirus
This work was supported by the DST/NRF SARChI programme (UID87326) and the Claude Leon Foundation.
- Currie DH, Guss AM, Herring CD et al (2014) Profile of secreted hydrolases, associated proteins, and SlpA in Thermoanaerobacterium saccharolyticum during the degradation of hemicellulose. Appl Environ Microbiol 80:5001–5011. https://doi.org/10.1128/aem.00998-14 CrossRefPubMedPubMedCentralGoogle Scholar
- Dellas N, Snyder JC, Bolduc B, Young MJ (2014) Archaeal viruses: diversity, replication, and structure. Annu Rev Virol 1:399–426. https://doi.org/10.1146/annurev-virology-031413-085357 CrossRefPubMedGoogle Scholar
- Doi K, Mori K, Martono H et al (2013) Draft genome sequence of geobacillus kaustophilus GBlys, a lysogenic strain with bacteriophage phiOH2. GenomeA 1:4–5. https://doi.org/10.1128/genomea.00634-13.copyright CrossRefGoogle Scholar
- Gudbergsdóttir SR, Menzel P, Krogh A, Young M, Peng X (2016) Novel viral genomes identified from six metagenomes reveal wide distribution of archaeal viruses and high viral diversity in terrestrial hot springs. Environ Microbiol 18:863–874. https://doi.org/10.1111/1462-2920.13079 CrossRefPubMedGoogle Scholar
- Jalasvuori M, Pawlowski A, Bamford JKH (2010) A unique group of virus-related, genome-integrating elements found solely in the bacterial family Thermaceae and the archaeal family Halobacteriaceae. J Bacteriol 192:3231–3234. https://doi.org/10.1128/jb.00124-10 CrossRefPubMedPubMedCentralGoogle Scholar
- Matsushita I, Yamashita N, Yokota A (1995) Isolation and characterization of bacteriophage induced from a new isolate of Thermus aquaticus. Microbiol Cult Collect Off Publ Japan Soc Cult Collect 11:133–138Google Scholar
- Minakhin L, Goel M, Berdygulova Z et al (2008) Genome comparison and proteomic characterization of Thermus thermophilus bacteriophages P23-45 and P74-26: siphoviruses with triplex-forming sequences and the longest known tails. J Mol Biol 378:468–480. https://doi.org/10.1016/j.jmb.2008.02.018 CrossRefPubMedPubMedCentralGoogle Scholar
- Pawlowski A, Rissanen I, Bamford JKH, Krupovic M, Jalasvuori M (2014) Gammasphaerolipovirus, a newly proposed bacteriophage genus, unifies viruses of halophilic archaea and thermophilic bacteria within the novel family Sphaerolipoviridae. Arch Virol 159:1541–1554. https://doi.org/10.1007/s00705-013-1970-6 CrossRefPubMedGoogle Scholar
- Pentecost A (1996) High temperature ecosystems and their chemical interactions with their environment. In: Ciba foundation symposium 202-evolution of hydrothermal ecosystems on earth (and mars?). Wiley, New York, pp 99–111Google Scholar
- Prangishvili D (2013) The wonderful world of archaeal viruses. Annu Rev Microbiol 67:565–585. https://doi.org/10.1146/annurev-micro-092412-155633 CrossRefPubMedGoogle Scholar
- Tripathi C, Mishra H, Khurana H et al (2017) Complete genome analysis of Thermus parvatiensis and comparative genomics of Thermus spp. provide insights into genetic variability and evolution of natural competence as strategic survival attributes. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01410 CrossRefPubMedPubMedCentralGoogle Scholar
- Williamson KE, Fuhrmann JJ, Wommack KE, Radosevich M (2017) Viruses in soil ecosystems: an unknown quantity within an unexplored territory. Annu Rev Virol 4:201–219. https://doi.org/10.1146/annurev-virology-101416-041639 CrossRefPubMedGoogle Scholar