The first known virus isolates from Antarctic sea ice have complex infection patterns

Sea ice microbiology; Virus isolation; Virus-host interactions; VLP in sea ice; Antarctica; Southern Ocean; Weddell Sea; Bacteria (microorganisms); Octadecabacter

Abstract :

[en] Viruses are recognized as important actors in ocean ecology and biogeochemical cycles, but many details are not yet understood. We participated in a winter expedition to the Weddell Sea, Antarctica, to isolate viruses and to measure virus-like particle abundance (flow cytometry) in sea ice. We isolated 59 bacterial strains and the first four Antarctic sea-ice viruses known (PANV1, PANV2, OANV1 and OANV2), which grow in bacterial hosts belonging to the typical sea-ice genera Paraglaciecola and Octadecabacter. The viruses were specific for bacteria at the strain level, although OANV1 was able to infect strains from two different classes. Both PANV1 and PANV2 infected 11/15 isolated Paraglaciecola strains that had almost identical 16S rRNA gene sequences, but the plating efficiencies differed among the strains, whereas OANV1 infected 3/7 Octadecabacter and 1/15 Paraglaciecola strains and OANV2 1/7 Octadecabacter strains. All the phages were cold-active and able to infect their original host at 0°C and 4°C, but not at higher temperatures. The results showed that virus-host interactions can be very complex and that the viral community can also be dynamic in the winter-sea ice. © FEMS 2018. All rights reserved.

Research Center/Unit :

FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège

Disciplines :

Microbiology

Author, co-author :

Luhtanen, A.-M.; Marine Research Centre, Finnish Environment Institute, Helsinki, Finland, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland, Tvärminne Zoological Station, University of Helsinki, Hanko, Finland

Eronen-Rasimus, E.; Marine Research Centre, Finnish Environment Institute, Helsinki, Finland

Oksanen, H. M.; Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland

Tison, Jean-Louis; Laboratoire de Glaciologie, DGES, Université Libre de Bruxelles, Belgium

Delille, Bruno ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Département d'astrophys., géophysique et océanographie (AGO)

Dieckmann, G. S.; Alfred Wegener Institute Helmholtz Center for Polar and Marine Research, Bremerhaven, Germany

Rintala, J.-M.; Tvärminne Zoological Station, University of Helsinki, Hanko, Finland, Department of Environmental Sciences, University of Helsinki, Helsinki, Finland, Institute for Atmospheric and Earth System Research (INAR), Faculty of Science, University of Helsinki, Helsinki, Finland

Bamford, D. H.; Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland

Language :

English

Title :

The first known virus isolates from Antarctic sea ice have complex infection patterns

Publication date :

2018

Journal title :

FEMS Microbiology Ecology

ISSN :

0168-6496

eISSN :

1574-6941

Publisher :

Oxford University Press

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

Nottbeck Foundation
F.R.S.-FNRS - Fonds de la Recherche Scientifique
Onni Talas Foundation
Finlands Akademi
BELSPO - Politique scientifique fédérale

Available on ORBi :

since 28 January 2019

Statistics

Number of views

62 (5 by ULiège)

Number of downloads

5 (4 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Anderson NG, Harris WW, Barber AA, et al. Separation of subcellular components and viruses by combined rate- and isopycnic-zonal centrifugation. J Natl Cancer Inst Monogr 1966;21:253-83.
Arrigo KR, Dieckmann G, Gosselin M, et al. High resolution study of the platelet ice ecosystem in McMurdo Sound, Antarctica: biomass, nutrient, and production profiles within a dense microalgal bloom. Mar Ecol Prog Ser 1995;127:255-68.
Arrigo KR,Mock T, Lizotte MP. Primary producers and sea ice. In: Thomas DN Dieckmann GS (ed). Sea Ice. 2nd ed. Oxford: John Wiley & Sons, Ltd, 2010, 283-325.
Arrigo KR, Thomas DN. Large scale importance of sea ice biology in the Southern Ocean. Antarct Sci 2004;16:471-86.
Bamford JK, Bamford DH. Large-scale purification of membranecontaining bacteriophage PRD1 and its subviral particles. Virology 1991;181:348-52.
Beckett SJ, Williams HTP. Coevolutionary diversification creates nested-modular structure in phage-bacteria interaction networks. Interface Focus 2013;3:20130033.
Bischof JC, He X. Thermal stability of proteins. Ann NY Acad Sci 2005;1066:12-33.
Boetius A, Anesio AM, Deming JW, et al. Microbial ecology of the cryosphere: sea ice and glacial habitats. Nat Rev Microbiol 2015;13:677-90.
Borriss M, Helmke E, Hanschke R, et al. Isolation and characterization of marine psychrophilic phage-host systems from Arctic sea ice. Extremophiles 2003;7:377-84.
Borriss M, Lombardot T, Glöckner FO, et al. Genome and proteome characterization of the psychrophilic Flavobacterium bacteriophage 11b. Extremophiles 2007;11:95-104.
Boulanger PA, Puvion F. Large-scale preparation of soluble adenovirus hexon, penton and fiber antigens in highly purified form. Eur J Biochem 1973;39:37-42.
Bowman JP, McCammon SA, Brown MV, et al. Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl Environ Microb 1997;63:3068-78.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54.
Brinkmeyer R, Knittel K, Jurgens J, et al. Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl Environ Microb 2003;69:6610-9.
Brussaard CPD, Payet JP,Winter C, et al. Quantification of aquatic viruses by flowcytometry. In:Wilhelm SWeinbauerM, Suttle C (eds). Manual of Aquatic Viral Ecology. Association for the Sciences of Limnology and Oceanography, Inc, 2010:102-9.
Burgess RR. Chapter 20 - Protein Precipitation Techniques. Method Enzymol. Vol 463. 1st ed. Elsevier Inc., 2009, 331-42.
Colangelo-Lillis JR, Deming JW. Genomic analysis of cold-active Colwelliaphage 9A and psychrophilic phage-host interactions. Extremophiles 2013;17:99-114.
Collins RE, Deming JW. Abundant dissolved genetic material in Arctic sea ice part ii: viral dynamics during autumn freezeup. Polar Biol 2011;34:1831-41.
Deming JW, Collins RE. Sea ice as a habitat for bacteria, archaea and viruses. In: Thomas DN (ed). Sea Ice. 3rd ed. Oxford: John Wiley & Sons, Ltd., 2017, 326-51.
Dieckmann GS, Hellmer H. The importance of sea ice: an overview. In: Thomas DN, Dieckmann GS (eds). Sea Ice. 2nd ed. Oxford: John Wiley & Sons, Ltd., 2010, 1-22.
Edwards U, Rogall T, Blöcker H, et al. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 1989;17:7843-53.
Eronen-Rasimus E, Luhtanen A-M, Rintala J-M, et al. An active bacterial community linked to high chl-a concentrations in Antarctic winter-pack ice and evidence for the development of an anaerobic sea-ice bacterial community. ISME J 2017;63:3068.
Eronen-Rasimus E, Lyra C, Rintala J-M, et al. Ice formation and growth shape bacterial community structure in Baltic Sea drift ice. FEMS Microbiol Ecol 2015;91:1-13.
Flores CO, Meyer JR, Valverde S, et al. Statistical structure of hostphage interactions. P Natl Acad Sci USA 2011;108:E288-97.
Forterre P, Soler N, Krupovic M, et al. Fake virus particles generated by fluorescence microscopy. Trends Microbiol 2013;21:1-5.
Fuhrman JA. Marine viruses and their biogeochemical and ecological effects. Nature 1999;399:541-8.
Gowing MM, Garrison DL, Gibson AH, et al. Bacterial and viral abundance in Ross Sea summer pack ice communities. Mar Ecol Prog Ser 2004;279:3-12.
Gowing MM, Riggs BE, Garrison DL, et al. Large viruses in Ross Sea late autumn pack ice habitats. Mar Ecol Prog Ser 2002;241:1-11.
Helmke E, Weyland H. Bacteria in sea ice and underlying water of the eastern Weddell Sea in midwinter. Mar Ecol Prog Ser 1995;117:269-87.
Holmfeldt K, Middelboe M, Nybroe O, et al. Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts. Appl Environ Microbiol 2007;73:6730-39.
Huston AL, Krieger-Brockett BB, Deming JW. Remarkably low temperature optima for extracellular enzyme activity from Arctic bacteria and sea ice. Environ Microbiol 2000;2:383-8.
Jaenicke R. Protein stability and molecular adaptation to extreme conditions. Eur J Biochem 1991;202:715-28.
Junge K, Eicken H, Deming JW. Bacterial activity at -2 to -20°C in ArcticWintertime sea ice. Appl Environ Microbiol 2004;70:550-7.
Knowles B, Silveira CB, Bailey BA, et al. Lytic to temperate swithching of viral communities. Nature 2016;531:1-15.
Koskella B, Brockhurst MA. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev 2014;38:916-31.
Krupovic M, Dutilh BE, Adriaenssens EM, et al. Taxonomy of prokaryotic viruses: update from the ICTV bacterial and archaeal viruses subcommittee. Arch Virol 2016;161:1095-9.
Labrie SJ, Samson JE,Moineau S. Bacteriophage resistance mechanisms. Nat Rev Microbiol 2010;8:317-27.
Lane DJ, Pace B, Olsen GJ, et al. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. P Natl Acad Sci USA 1985;82:6955-9.
Lannuzel D, De Jong J, Schoemann V, et al. Development of a sampling and flow injection analysis technique for iron determination in the sea ice environment. Anal Chim Acta 2006;556:476-83.
Lawrence JE, Steward GF. Purification of viruses by centrifugation. In: Wilhelm S, Weinbauer M, Suttle C (eds). Manual of Aquatic Viral Ecology. Association for the Sciences of Limnology and Oceanography, Inc, 2010:166-81, doi: 10.4319/mave.2010.978-0-9845591-0-7.
Leon-Velarde CG, Happonen L, Pajunen M, et al. Yersinia enterocolitica-specific infection by bacteriophages TG1 and fR1-RT is dependent on temperature-regulated expression of the phage host receptor OmpF. Appl Environ Microb 2016;82:5340-53.
Leturnic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 2007;23:127-8.
Louhi K-R, Sundberg L-R, Jokela J, et al. Interactions among bacterial strains and fluke genotypes shape virulence of coinfection. Proc R Soc B 2016;282:20152097.
Luhtanen A-M, Eronen-Rasimus E, Kaartokallio H, et al. Isolation and characterization of phage-host systems from the Baltic Sea ice. Extremophiles 2014;18:121-30.
Maranger R, Bird DF. Viral abundance in aquatic systems: a comparison between marine and fresh waters. Mar Ecol Prog Ser 1995;121: 217-26.
Maranger R, Bird D, Juniper S. Viral and bacterial dynamics in Arctic sea ice during the spring algal bloom near Resolute, N. W. T., Canada. Mar Ecol Prog Ser 1994;111:121-7.
Marchant H, Davidson A, Wright S, et al. The distribution and abundance of viruses in the Southern Ocean during spring. Antarct Sci 2000;12:414-7.
Meiners K, Krembs C, Gradinger R. Exopolymer particles: microbial hotspots of enhanced bacterial activity in Arctic fast ice (Chukchi Sea). Aquat Microb Ecol 2008;52:195-207.
Middelboe M. Bacterial growth rate and marine virus-host dynamics. Microb Ecol 2000;40:114-24.
Middelboe M, Hagström A, Blackburn N, et al. Effects of bacteriophages on the population dynamics of four strains of pelagic marine bacteria. Microb Ecol 2001;42:395-406.
Middelboe M, Riemann L, Steward GF, et al. Virus-induced transfer of organic carbon between marine bacteria in a model community. Aquat Microb Ecol 2003;33:1-10.
Mock T, Thomas DN. Recent advances in sea-ice microbiology. Environ Microbiol 2005;7:605-19.
Morita RY. Psychrophilic bacteria. Bacteriol Rev 1975;39:144-67.
Olkkonen VM, Bamford DH. Quantitation of the adsorption and penetration stages of bacteriophage f6 infection. Virology 1989;171:229-38.
Paterson H, Laybourn-Parry J. Antarctic sea ice viral dynamics over an annual cycle. Polar Biol 2012;35:491-7.
Proctor LM, Fuhrman JA. Viral mortality of marine bacteria and cyanobacteria. Nature 1990;343:60-2.
Pruesse E, Peplies J, Glockner FO. SINA: Accurate highthroughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012;28:1823-9.
Reed CJ, Lewis H, Trejo E, et al. Protein adaptations in archaeal extremophiles. Archaea 2013;2013:14.
Rintala J-M, Piiparinen J, Blomster J, et al. Fast direct melting of brackish sea-ice samples results in biologically more accurate results than slow buffered melting. Polar Biol 2014;37:1811-22.
Sait L, Galic M, Strugnell RA, et al. Secretory Antibodies Do Not Affect the Composition of the Bacterial Microbiota in the Terminal Ileum of 10-Week-Old Mice. Appl Environ Microb 2003;69:2100-9.
Senčilo A, Luhtanen A-M, Saarijärvi M, et al. Cold-active bacteriophages from the Baltic Sea ice have diverse genomes and virus-host interactions. Environ Microbiol 2015;17:3628-41.
Shivaji S, Reddy GS. Phylogenetic analyses of the genus Glaciecola: emended description of the genus Glaciecola, transfer of Glaciecola mesophila, G. agarilytica, G. aquimarina, G. arctica, G. chathamensis, G. polaris and G. psychrophila to the genus Paraglaciecola gen. nov. as Paraglaciecola mesophila comb. nov., P. agarilytica comb. nov., P. aquimarina comb. nov., P. arctica comb. nov., P. chathamensis comb. nov., P. polaris comb. nov. and P. psychrophila comb. nov., and description of Paraglaciecola oceanifecundans sp. nov., isolated from the Southern Ocean. Int J Syst Evol Micr 2014;64:3264-75.
Soler N, Krupovic M, Marguet E, et al. Membrane vesicles in natural environments: a major challenge in viral ecology. ISME J 2015;9:793-6.
Stamatakis A. RaxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30:1312-3.
Suttle C. Viruses in the sea. Nature 2005;437:356-61.
Suttle CA. Marine viruses - major players in the global ecosystem. Nat Rev Microbiol 2007;5:801-12.
Thingstad T, Lignell R. Theoreticalmodels for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 1997;13:19-27.
Thingstad TF, Vage S, Storesund JE, et al. A theoretical analysis of how strain-specific viruses can control microbial species diversity. P Natl Acad Sci USA 2014;111:7813-8.
Thomas DN, Dieckmann GS. Antarctic sea ice - a habitat for extremophiles. Science 2002;295:641-4.
Tison J-L, Schwegmann S, Dieckmann G, et al. Biogeochemical impact of snow cover and cyclonic intrusions on the winter Weddell Sea ice pack. J Geophys Res Oceans 2017;122:9548-71.
Tokman JI, Kent DJ,WiedmannMet al. Temperature significantly affects the plaquing and adsorption efficiencies of Listeria phages. Front Microbiol 2016;7:631-40.
Våge S, Storesund JE, Thingstad TF. Adding a cost of resistance description extends the ability of virus-hostmodel to explain observed patterns in structure and function of pelagic microbial communities. Environ Microbiol 2013;15:1842-52.
Weinbauer MG. Ecology of prokaryotic viruses. FEMS Microbiol Rev 2004;28:127-81.
Weitz JS, Poisot T, Meyer JR, et al. Phage-bacteria infection networks. Trends Microbiol 2013;21:82-91.
Wells L, Deming J. Modelled and measured dynamics of viruses in Arctic winter sea-ice brines. Environ Microbiol 2006a;8:1115-21.
Wells LE, Deming JW. Characterization of a cold-active bacteriophage on two psychrophilic marine hosts. Aquat Microb Ecol 2006b;45:15-29.
Wells LE, Deming JW. Effects of temperature, salinity and clay particles on inactivation and decay of cold-active marine Bacteriophage 9A. Aquat Microb Ecol 2006c;45:31-9.
Wigington CH, Sonderegger D, Brussaard CPD, et al. Reexamination of the relationship between marine virus and microbial cell abundances. Nat Rev Microbiol 2016;1:1-8.
Wommack KE, Colwell RR. Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol R 2000;64:69-114.
Yoon SH, Ha S-M, Kwon S, et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017;67:1613-7.
Yu Z-C, Chen X-L, Shen Q-T, et al. Filamentous phages prevalent in Pseudoalteromonas spp. confer properties advantageous to host survival in Arctic sea ice. ISME J 2015;9:871-81.
Zablocki O, van Zyl LJ, Kirby B, et al. Diversity of dsDNA viruses in a South African hot spring assessed by metagenomics and microscopy. Viruses 2017;9:348-61.