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Bacteriophages and their microbial hosts in terrestrial biotopes of Antarctica

Published online by Cambridge University Press:  16 December 2021

Viktoriia Holovan Open the ORCID record for Viktoriia Holovan [Opens in a new window] ,
Olena Andriichuk ,
Irena Budzanivska ,
Pavlina Zelena ,
Tetiana Kondratiuk  and
Oleksiy Shevchenko
Viktoriia Holovan*
Affiliation:
Educational and Scientific Center ‘Institute of Biology and Medicine’, Taras Shevchenko National University of Kyiv, Volodymyrska str., 64/13, Kyiv 01601, Ukraine
Olena Andriichuk
Affiliation:
Educational and Scientific Center ‘Institute of Biology and Medicine’, Taras Shevchenko National University of Kyiv, Volodymyrska str., 64/13, Kyiv 01601, Ukraine
Irena Budzanivska
Affiliation:
Educational and Scientific Center ‘Institute of Biology and Medicine’, Taras Shevchenko National University of Kyiv, Volodymyrska str., 64/13, Kyiv 01601, Ukraine
Pavlina Zelena
Affiliation:
Educational and Scientific Center ‘Institute of Biology and Medicine’, Taras Shevchenko National University of Kyiv, Volodymyrska str., 64/13, Kyiv 01601, Ukraine
Tetiana Kondratiuk
Affiliation:
Educational and Scientific Center ‘Institute of Biology and Medicine’, Taras Shevchenko National University of Kyiv, Volodymyrska str., 64/13, Kyiv 01601, Ukraine
Oleksiy Shevchenko
Affiliation:
Educational and Scientific Center ‘Institute of Biology and Medicine’, Taras Shevchenko National University of Kyiv, Volodymyrska str., 64/13, Kyiv 01601, Ukraine
*
[email protected]
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Abstract

Virus diversity in Antarctic biotopes remains understudied. Here, we describe bacteriophages isolated from terrestrial environments, provide data on their natural bacterial hosts and study phage-host systems. Six bacterial isolates (FCKU 539, FCKU 533, FCKU 534, FCKU 538, FCKU 542 and FCKU 540) were recovered and characterized. Isolated bacteria belonged to Pseudomonas genus (Pseudomonas sp., Pseudomonas fluorescens, Pseudomonas putida) with optimal cultivation temperatures of 16–28°C. These bacteria and previously described Bacillus subtilis FCKU 537 were used for analysing virus-host interactions. Six lytic phages were isolated and named P. fluorescens Antarctic virus 1 (PFAV1), P. fluorescens Antarctic virus 2 (PFAV2), P. fluorescens Antarctic virus 3 (PFAV3), P. putida Antarctic virus 4 (PPAV4), Pseudomonas sp. Antarctic virus 5 (PSAV5) and B. subtilis Antarctic virus 6 (BSAV6) in relation to their natural hosts. According to electron microscopy data, these phages belonged to Caudovirales order. Cross-inoculation demonstrated high specificity of all Antarctic phages, which infected only their initial hosts at moderate temperatures. PFAV2 and PFAV3 phages also infected laboratory Pseudomonas savastanoi and P. fluorescens isolates. This paper adds new data on the occurrence and diversity of viruses and their respective bacterial hosts in soil biotopes of Antarctica.

Keywords

bacteriaelectron microscopysoilvirus particles
Type
Biological Sciences
Information
Antarctic Science , Volume 34 , Issue 2 , April 2022 , pp. 120 - 136
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Copyright
Copyright © Antarctic Science Ltd 2021

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References

Ackermann, H.W. 2009. Phage classification and characterization. Methods in Molecular Biology, 501, 127–140.10.1007/978-1-60327-164-6_13CrossRefGoogle ScholarPubMed
Adams, M.H. 1959. Bacteriophages. London: Interscience Publishers, 592 pp.CrossRefGoogle Scholar
Adriaenssens, E.M., Kramer, R., Van Goethem, M.W., Makhalanyane, T.P., Hogg, I. & Cowan, D.A. 2017. Environmental drivers of viral community composition in Antarctic soils identified by viromics. Microbiome, 5, 83.10.1186/s40168-017-0301-7CrossRefGoogle ScholarPubMed
Adriaenssens, E.M., Van Zyl, L., De Maayer, P., Rubagotti, E., Rybicki, E., Tuffin, M. & Cowan, D.A. 2015. Metagenomic analysis of the viral community in Namib Desert hypoliths. Environmental Microbiology, 17, 480–495.CrossRefGoogle ScholarPubMed
Anesio, A.M. & Bellas, C.M. 2011. Are low temperature habitats hot spots of microbial evolution driven by viruses? Trends in Microbiology, 19, 52–57.CrossRefGoogle ScholarPubMed
Angly, F.E., Felts, B., Breitbart, M., Salamon, P., Edwards, R.A. & Carlson, C. 2006. The marine viromes of four oceanic regions. PLoS Biology, 4, e368.10.1371/journal.pbio.0040368CrossRefGoogle ScholarPubMed
Antibus, D.E., Leff, L.G., Hall, B.L., Baeseman, J.L. & Blackwood, C.B. 2012. Cultivable bacteria from ancient algal mats from the McMurdo Dry Valleys, Antarctica. Extremophiles, 16, 105–114.10.1007/s00792-011-0410-3CrossRefGoogle ScholarPubMed
Bakermans, C., Skidmore, M.L., Douglas, S. & McKay, C.P. 2014. Molecular characterization of bacteria from permafrost of the Taylor Valley, Antarctica. FEMS Microbiology Ecology, 89, 331–346.10.1111/1574-6941.12310CrossRefGoogle ScholarPubMed
Bauman, R.W. 2017. Microbiology with diseases by body system, 5th ed. Upper Saddle River, NJ: Pearson, 944 pp.Google Scholar
Borriss, M., Helmke, E., Hanschke, R. & Schweder, T. 2003. Isolation and characterization of marine psychrophilic phage-host systems from Arctic sea ice. Extremophiles, 7, 377–384.10.1007/s00792-003-0334-7CrossRefGoogle ScholarPubMed
Bottos, E.M., Scarrow, J.W., Archer, S.D.J., McDonald, I.R. & Cary, S.C. 2014. Bacterial community structures of Antarctic soils. In Cowan, D.A., ed. Antarctic terrestrial microbiology. Berlin: Springer, 9–33.10.1007/978-3-642-45213-0_2CrossRefGoogle Scholar
Bowman, J.P. 2017. Genomics of psychrophilic bacteria and archaea. In Margesin, R., ed. Psychrophiles: from biodiversity to biotechnology. Cham: Springer, 345–387.10.1007/978-3-319-57057-0_15CrossRefGoogle Scholar
Breitbart, M. & Rohwer, F. 2005. Here a virus, there a virus, everywhere the same virus? Trends in Microbiology, 13, 278–284.10.1016/j.tim.2005.04.003CrossRefGoogle Scholar
Brum, J.R., Hurwitz, B.L., Schofield, O., Ducklow, H.W. & Sullivan, M.B. 2016. Seasonal time bombs: dominant temperate viruses affect southern ocean microbial dynamics. ISME Journal, 10, 437–449.10.1038/ismej.2015.125CrossRefGoogle ScholarPubMed
Cameron, K.A., Hodson, A.J. & Osborn, A.M. 2012. Structure and diversity of bacterial, eukaryotic and archaeal communities in glacial cryoconite holes from the Arctic and the Antarctic. FEMS Microbiology Ecology, 82, 254–267.CrossRefGoogle ScholarPubMed
Cary, S.C., McDonald, I.R., Barrett, J.E. & Cowan, D.A. 2010. On the rocks: the microbiology of Antarctic Dry Valley soils. Nature Reviews Microbiology, 8, 129–138.CrossRefGoogle ScholarPubMed
Cavicchioli, R., Charlton, T., Ertan, H., Mohd Omar, S., Siddiqui, K.S. & Williams, T.J. 2011. Biotechnological uses of enzymes from psychrophiles. Microbial Biotechnology, 4, 449–460.CrossRefGoogle ScholarPubMed
Chauhan, A., Bharti, P.K., Goyal, P., Varma, A. & Jindal, T. 2015. Psychrophilic pseudomonas in Antarctic freshwater lake at Stornes Peninsula, Larsemann Hills over East Antarctica. SpringerPlus, 4, 582.CrossRefGoogle ScholarPubMed
Cho, J.C. & Giovannoni, S.J. 2004. Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria. Applied and Environmental Microbiology, 70, 432–440.10.1128/AEM.70.1.432-440.2004CrossRefGoogle ScholarPubMed
Connon, S.A. & Giovannoni, S.J. 2002. High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates. Applied and Environmental Microbiology, 68, 3878–3885.10.1128/AEM.68.8.3878-3885.2002CrossRefGoogle ScholarPubMed
Cook, G.T. 1950. A plate test for nitrate reduction. Journal of Clinical Pathology, 3, 359–362.10.1136/jcp.3.4.359CrossRefGoogle ScholarPubMed
Cowan, D.A. & Tow, L.A. 2004. Endangered Antarctic environments. Annual Review of Microbiology, 58, 649–690.10.1146/annurev.micro.57.030502.090811CrossRefGoogle ScholarPubMed
Cowan, S.T. & Steel, K.J. 1973. Manual for the identification of medical bacteria. Cambridge: Cambridge University Press, 217 pp.Google Scholar
Culley, A.I., Lang, A.S. & Suttle, C.A. 2006. Metagenomic analysis of coastal RNA virus communities. Science, 312, 1795–1798.10.1126/science.1127404CrossRefGoogle ScholarPubMed
Fierer, N. & Jackson, R.B. 2006. The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America, 17, 626–631.10.1073/pnas.0507535103CrossRefGoogle Scholar
Foreman, C.M., Sattler, B., Mikucki, J.A., Porazinska, D.L. & Priscu, J.C. 2007. Metabolic activity and diversity of cryoconites in the Taylor Valley, Antarctica. Journal of Geophysical Research - Biogeosciences, 112, G04S32.CrossRefGoogle Scholar
Gong, Z., Liang, Y., Wang, M., Jiang, Y., Yang, Q., Xia, J., et al. 2018. Viral diversity and its relationship with environmental factors at the surface and deep sea of Prydz Bay, Antarctica. Frontiers in Microbiology, 9, 2981.CrossRefGoogle ScholarPubMed
Gowing, M.M., Riggs, B., Garrison, D.L., Gibson, A.H. & Jeffries, M.O. 2002. Large viruses in Ross Sea late autumn pack ice habitats. Marine Ecology Progress Series, 241, 1–11.10.3354/meps241001CrossRefGoogle Scholar
Gregersen, T. 1978. Rapid method for distinction of Gram-negative from Gram-positive bacteria. European Journal of Applied Microbiology and Biotechnology, 5, 123–127.CrossRefGoogle Scholar
Gregory, A.C., Zayed, A.A., Conceição-Neto, N., Temperton, B., Bolduc, B., Alberti, A., et al. 2019. Marine DNA viral macro- and micro-diversity from pole to pole. Cell, 177, 1109–1123.e14.CrossRefGoogle Scholar
Hansen, M.C., Tolker-Nielsen, T., Givskov, M. & Molin, S. 1998. Biased 16S rDNA PCR amplification caused by interference from DNA flanking the template region. FEMS Microbiology Ecology, 26, 141–149.10.1111/j.1574-6941.1998.tb00500.xCrossRefGoogle Scholar
Hemraj, V., Sharma, D. & Gupta, A. 2013. A review on commonly used biochemical test for bacteria. Innovare Journal of Life Science, 1, 1–7.Google Scholar
Junge, K., Eicken, H. & Deming, J.W. 2004. Bacterial activity at -2 to -20 degrees C in Arctic wintertime sea ice. Applied Environmental Microbiology, 70, 550–557.10.1128/AEM.70.1.550-557.2004CrossRefGoogle ScholarPubMed
Kimble, J.M., ed. 2004. Cryosols: permafrost-affected soils. New York: Springer, 744 pp.CrossRefGoogle Scholar
Kondratiuk, T.O., Beregova, T.V. & Ostapchenko, L.I. 2016. Diversity of Antarctic microorganisms - potential producers of biologically active substances. Ukrainian Antarctic Journal, 15, 176–182.CrossRefGoogle Scholar
Koskella, B. & Brockhurst, M.A. 2014. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiology Reviews, 38, 916–931.10.1111/1574-6976.12072CrossRefGoogle ScholarPubMed
Kutter, E. 2009. Phage host range and efficiency of plating. Methods in Molecular Biology, 501, 141–149.10.1007/978-1-60327-164-6_14CrossRefGoogle ScholarPubMed
Lauro, F.M., DeMaere, M.Z., Yau, S., Brown, M.V., Ng, C., Wilkins, D., Raftery, M.J., et al. 2010. An integrative study of a meromictic lake ecosystem in Antarctica. ISME Journal, 5, 879.10.1038/ismej.2010.185CrossRefGoogle ScholarPubMed
Lavysh, D., Sokolova, M., Minakhin, L., Yakunina, M., Artamonova, T., Kozyavkin, S., et al. 2016. The genome of AR9, a giant transducing Bacillus phage encoding two multisubunit RNA polymerases. Virology, 495, 185–196.CrossRefGoogle ScholarPubMed
Lee, J., Cho, Y.J., Yang, J.Y., Jung, Y.J., Hong, S.G. & Kim, O.S. 2017. Complete genome sequence of Pseudomonas antarctica PAMC 27494, a bacteriocin-producing psychrophile isolated from Antarctica. Journal of Biotechnology, 259, 15–18.CrossRefGoogle ScholarPubMed
Leijh, P.C., van Zwet, T.L., ter Kuile, M.N. & van Furth, R. 1984. Effect of thioglycolate on phagocytic and microbicidal activities of peritoneal macrophages. Infection and Immunity, 46, 448–452.CrossRefGoogle ScholarPubMed
López-Bueno, A., Rastrojo, A., Peiró, R., Arenas, M. & Alcamí, A. 2015. Ecological connectivity shapes quasispecies structure of RNA viruses in an Antarctic lake. Molecular Ecology, 24, 4812–4825.CrossRefGoogle Scholar
López-Bueno, A., Tamames, J., Velázquez, D., Moya, A., Quesada, A. & Alcamí, A. 2009. High diversity of the viral community from an Antarctic lake. Science, 326, 858–861.10.1126/science.1179287CrossRefGoogle ScholarPubMed
Luhtanen, A.M., Eronen-Rasimus, E., Kaartokallio, H., Rintala, J.M., Autio, R. & Roine, E. 2014. Isolation and characterization of phage-host systems from the Baltic Sea ice. Extremophiles, 18, 121–130.CrossRefGoogle ScholarPubMed
Luhtanen, A.M., Eronen-Rasimus, E., Oksanen, H.M., Tison, J.L., Delille, B., Dieckmann, G.S., et al. 2018. The first known virus isolates from Antarctic sea ice have complex infection patterns. FEMS Microbiology Ecology, 94, fiy028.CrossRefGoogle ScholarPubMed
MacFaddin, J.F. 1985. Media for isolation-cultivation-identification-maintenance of medical bacteria. London: Williams and Wilkins, 929 pp.Google Scholar
Margesin, R. 2000. Potential of cold-adapted microorganisms for bioremediation of oil-polluted Alpine soils. International Biodeterioration and Biodegradation, 46, 3–10.CrossRefGoogle Scholar
Massalski, A., Kostikov, I., Olech, M. & Hoffmann, L. 2009. Mitosis, cytokinesis and multinuclearity in a Xanthonema (Xanthophyta) isolated from Antarctica. European Journal of Phycology, 44, 263–275.CrossRefGoogle Scholar
Miller, J.H. 1972. Experiments in molecular genetics. New York: Cold Spring Harbor Laboratory Press, 466 pp.Google Scholar
Miranda, J.A., Culley, A.I., Schvarcz, C.R. & Steward, G.F. 2016. RNA viruses as major contributors to Antarctic virioplankton. Environmental Microbiology, 18, 3714–3727.CrossRefGoogle ScholarPubMed
Murray, A.G. & Eldridge, P.M. 1994. Marine viral ecology: incorporation of bacteriophage into the microbial planktonic food web paradigm. Journal of Plankton Research, 16, 627–641.CrossRefGoogle Scholar
O'Brien, A., Sharp, R., Russell, N. & Roller, S. 2004. Antarctic bacteria inhibit growth of food-borne microorganisms at low temperatures. FEMS Microbiology Ecology, 48, 157–167.CrossRefGoogle ScholarPubMed
Orellana-Saez, M., Pacheco, N., Costa, J.I., Mendez, K.N., Miossec, M.J., Meneses, C., et al. 2019. In-depth genomic and phenotypic characterization of the Antarctic psychrotolerant strain Pseudomonas sp. MPC6 reveals unique metabolic features, plasticity, and biotechnological potential. Frontiers in Microbiology, 10, 1154.10.3389/fmicb.2019.01154CrossRefGoogle ScholarPubMed
Ozen, A.I. & Ussery, D.W. 2012. Defining the Pseudomonas genus: where do we draw the line with Azotobacter? Microbial Ecology, 63, 239–248.CrossRefGoogle ScholarPubMed
Pacheco, N., Orellana-Saez, M., Pepczynska, M., Enrione, J., Bassas-Galia, M., Borrero-de Acuña, J.M., et al. 2019. Exploiting the natural poly(3-hydroxyalkanoates) production capacity of Antarctic Pseudomonas strains: from unique phenotypes to novel biopolymers. Journal of Industrial Microbiology and Biotechnology, 46, 1139–1153.10.1007/s10295-019-02186-2CrossRefGoogle ScholarPubMed
Paterson, H. & Laybourn-Parry, J. 2012. Antarctic sea ice viral dynamics over an annual cycle. Polar Biology, 35, 491–497.10.1007/s00300-011-1093-zCrossRefGoogle Scholar
Pearce, D. & Wilson, W. 2003. Viruses in Antarctic ecosystems. Antarctic Science, 15, 319–331.10.1017/S0954102003001330CrossRefGoogle Scholar
Poblete-Castro, I., Becker, J., Dohnt, K., dos Santos, V.M. & Wittmann, C. 2012. Industrial biotechnology of Pseudomonas putida and related species. Applied Microbiology and Biotechnology, 93, 2279–2290.CrossRefGoogle ScholarPubMed
Polischuk, V., Budzanivska, I., Shevchenko, T. & Oliynik, S. 2007. Evidence for plant viruses in the region of Argentina Islands, Antarctica. FEMS Microbiology Ecology, 59, 409–417.CrossRefGoogle ScholarPubMed
Pulschen, A.A., Bendia, A.G., Fricker, A.D., Pellizari, V.H., Galante, D. & Rodrigues, F. 2017. Isolation of uncultured bacteria from Antarctica using long incubation periods and low nutritional media. Frontiers in Microbiology, 8, 1346.10.3389/fmicb.2017.01346CrossRefGoogle ScholarPubMed
Rastrojo, A. & Alcamí, A. 2018. Viruses in polar lake and soil ecosystems. Advances in Virus Research, 101, 39–54.CrossRefGoogle ScholarPubMed
Romaniuk, K., Ciok, A., Decewicz, P., Uhrynowski, W., Budzik, K., Nieckarz, M., et al. 2018. Insight into heavy metal resistome of soil psychrotolerant bacteria originating from King George Island (Antarctica). Polar Biology, 41, 1319–1333.CrossRefGoogle Scholar
Rybalka, N., Andersen, R.A., Kostikov, I., Mohr, K.I., Massalski, A., Olech, M. & Friedl, T. 2009. Testing for endemism, genotypic diversity and species concepts in Antarctic terrestrial microalgae of the Tribonemataceae (Stramenopiles, Xanthophyceae). Environmental Microbiology, 11, 554–565.CrossRefGoogle ScholarPubMed
Sambrook, J. & Russell, D. 2001. Molecular cloning: a laboratory manual. New York: Cold Spring Harbor Laboratory Press, 2100 pp.Google Scholar
Säwström, C., Lisle, J., Anesio, A.M., Priscu, J.C. & Laybourn-Parry, J. 2008. Bacteriophage in polar inland waters. Extremophiles, 12, 167–175.CrossRefGoogle ScholarPubMed
Siddharth, R. & Krishnamurthy, W.D. 2017. Origins and challenges of viral dark matter. Virus Research, 239, 136–142.Google Scholar
Silhavy, T.J., Kahne, D. & Walker, S. 2010. The bacterial cell envelope. Cold Spring Harbor Perspectives in Biology, 2, a000414.CrossRefGoogle ScholarPubMed
Smeele, Z.E., Ainley, D.G. & Varsani, A. 2018. Viruses associated with Antarctic wildlife: from serology based detection to identification of genomes using high throughput sequencing. Virus Research, 243, 91–105.CrossRefGoogle ScholarPubMed
Sommers, P., Fontenele, R.S., Kringen, T., Kraberger, S., Porazinska, D.L., Darcy, J.L., et al. 2019. Single-stranded DNA viruses in Antarctic cryoconite holes. Viruses, 11, 1022.CrossRefGoogle ScholarPubMed
Spain, A., Krumholz, L. & Elshahed, M. 2009. Abundance, composition, diversity and novelty of soil Proteobacteria. ISME Journal, 3, 992–1000.CrossRefGoogle ScholarPubMed
Spanu, T., Sanguinetti, M., Ciccaglione, D., D'Inzeo, T., Romano, L., Leone, F. & Fadda, G. 2003. Use of the VITEK 2 system for rapid identification of clinical isolates of Staphylococci from bloodstream infections. Journal of Clinical Microbiology, 41, 4259–4263.10.1128/JCM.41.9.4259-4263.2003CrossRefGoogle ScholarPubMed
Spencer, R. 1960. Indigenous marine bacteriophages. Journal of Bacteriology, 79, 614.10.1128/jb.79.4.614-614.1960CrossRefGoogle ScholarPubMed
Straka, R.P. & Stokes, J.L. 1960. Psychrophilic bacteria from Antarctica. Journal of Bacteriology, 80, 622–625.CrossRefGoogle ScholarPubMed
Suttle, C. 2007. Marine viruses - major players in the global ecosystem. Nature Reviews Microbiology, 5, 801–812.CrossRefGoogle ScholarPubMed
Swanson, M.M., Reavy, B., Makarova, K.S., Cock, P.J., Hopkins, D.W., Torranceet, L., et al. 2012. Novel bacteriophages containing a genome of another bacteriophage within their genomes. PLoS ONE, 7, e40683.10.1371/journal.pone.0040683CrossRefGoogle ScholarPubMed
Taylor, W.I. & Achanzar, D. 1972. Catalase test as an aid to the identification of Enterobacteriaceae. Journal of Applied Microbiology, 24, 58–61.CrossRefGoogle Scholar
Teixeira, L.C., Peixoto, R.S., Cury, J.C., Sul, W.J., Pellizari, V.H., Tiedje, J. & Rosado, A.S. 2010. Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, Maritime Antarctica. ISME Journal, 4, 989–1001.10.1038/ismej.2010.35CrossRefGoogle ScholarPubMed
Thingstad, T.F. & Lignell, R. 1997. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquatic Microbial Ecology, 13, 19–27.10.3354/ame013019CrossRefGoogle Scholar
Van Horn, D.J., Van Horn, M.L., Barrett, J.E., Gooseff, M.N., Altrichter, A.E., Geyer, K.M., et al. 2013. Factors controlling soil microbial biomass and bacterial diversity and community composition in a cold desert ecosystem: role of geographic scale. PLoS ONE, 8, e66103.CrossRefGoogle Scholar
Vos, P.D., Garrity, G.M., Dorothy, J., Krieg, N.R., Ludwig, W., Rainey, F.A., et al. 2009. Bergey's manual of systematic bacteriology. The Firmicutes. New York: Springer, 1450 pp.Google Scholar
Wasserman, А.Е. 1965. Absorption and fluorescence of water-soluble pigments produced by four species of Pseudomonas. Applied Microbiology, 13, 175–180.CrossRefGoogle ScholarPubMed
Wei, S.T., Lacap-Bugler, D.C., Lau, M.C., Caruso, T., Rao, S., de Los Rios, A., et al. 2016. Taxonomic and functional diversity of soil and hypolithic microbial communities in Miers Valley, McMurdo Dry Valleys, Antarctica. Frontiers in Microbiology, 7, 1642.CrossRefGoogle ScholarPubMed
Weinbauer, M.G. 2004. Ecology of prokaryotic viruses. FEMS Microbiology Reviews, 28, 127–121.10.1016/j.femsre.2003.08.001CrossRefGoogle ScholarPubMed
Williamson, K.E., Radosevich, M., Smith, D.W. & Wommack, K.E. 2007. Incidence of lysogeny within temperate and extreme soil environments. Environmental Microbiology, 9, 2563–2574.CrossRefGoogle ScholarPubMed
Wommack, K.E., Ravel, J., Hill, R.T. & Colwell, R.R. 1999a. Hybridization analysis of Chesapeake Bay virioplankton. Applied and Environmental Microbiology, 65, 241–225.CrossRefGoogle ScholarPubMed
Wommack, K.E., Ravel, J., Hill, R.T., Chun, J. & Colwell, R.R. 1999b. Population dynamics of Chesapeake Bay virioplankton: total community analysis by pulse-field gel electrophoresis. Applied and Environmental Microbiology, 65, 231–240.10.1128/AEM.65.1.231-240.1999CrossRefGoogle Scholar
Yau, S. & Seth-Pasricha, M. 2019. Viruses of polar aquatic environments. Viruses, 11, 189.10.3390/v11020189CrossRefGoogle ScholarPubMed
Yau, S., Lauro, F.M., DeMaere, M.Z., Brown, M.V., Thomas, T., Raftery, M.J., et al. 2011. Virophage control of Antarctic algal host-virus dynamics. Proceedings of the National Academy of Sciences of the United States of America, 108, 6163–6168.CrossRefGoogle ScholarPubMed
Yu, Z.C., Chen, X.L., Shen, Q.T., Zhao, D.L., Tang, B.L., Su, H.N., et al. 2015. Filamentous phages prevalent in Pseudoalteromonas spp. confer properties advantageous to host survival in Arctic sea ice. ISME Journal, 9, 871–881.CrossRefGoogle ScholarPubMed
Zablocki, O., Adriaenssens, E.M. & Cowan, D. 2016. Diversity and ecology of viruses in hyperarid desert soils. Applied and Environmental Microbiology, 82, 770–777.CrossRefGoogle ScholarPubMed
Zablocki, O., van Zyl, L., Adriaenssens, E.M., Rubagotti, E., Tuffin, M., Cary, S.C. & Cowan, D. 2014. High-level diversity of tailed phages, eukaryote-associated viruses, and virophage-like elements in the metaviromes of Antarctic soils. Applied and Environmental Microbiology, 80, 6888–6897.CrossRefGoogle ScholarPubMed
Zhang, X.F., Yao, T.D., Tian, L.D., Xu, S.J. & An, L.Z. 2008. Phylogenetic and physiological diversity of bacteria isolated from Puruogangri ice core. Microbial Ecology, 55, 476–488.CrossRefGoogle ScholarPubMed