Skip to main content
SpringerLink
Log in

Exploring the Viral Ecology of High Latitude Aquatic Systems

  • Chapter
  • First Online:
Microbial Ecology of Extreme Environments

Abstract

Viruses are abundant and ubiquitous in aquatic systems. While most of our knowledge in the field of aquatic viral ecology comes from the study of temperate environments, new insights are starting to emerge from polar systems. It is becoming increasingly evident that viruses play a pivotal role in structuring high latitude aquatic systems where microbes are important players and major drivers of biogeochemical cycles. In this chapter, we summarize the latest findings about the abundance, distribution and production of viruses from polar regions. We also review viral-mediated bacterial mortality and phage-host dynamics in freshwater and marine polar waters. For example, we summarize temporal studies performed in polar freshwater systems, showing a seasonal trend with a high percent of lysogenic bacteria in the winter and an undetectable rate in the summer. These findings suggest that lysogeny represents an important life strategy in polar regions. We conclude with the latest analysis of large scale meta-omics datasets, which suggest that polar viral assemblages might be a reservoir of new lineages of viruses and unknown viral diversity.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aguirre de Cárcer D, López-Bueno A, Pearce DA, Alcamí A (2015) Biodiversity and distribution of polar freshwater DNA viruses. Sci Adv 1(5):e1400127

    Article  PubMed  PubMed Central  Google Scholar 

  • Anesio AM, Bellas CM (2011) Are low temperature habitats hot spots of microbial evolution driven by viruses? Trends Microbiol 19(2):52–57

    Google Scholar 

  • Anesio AM, Mindl B, Laybourn-Parry J, Hodson AJ, Sattler B (2007) Viral dynamics in cryoconite holes on a high Arctic glacier (Svalbard). J Geophys Res: Biogeosci 112:G04531

    Google Scholar 

  • Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C, Chan AM et al (2006) The marine viromes of four oceanic regions. PLoS Biol 4(11):2121–2131

    Google Scholar 

  • Bergh O, Borsheim KY (1989) High abundance of viruses found in aquatic environments. Nature 340:467–468

    Article  CAS  PubMed  Google Scholar 

  • Bettarel Y, Sime-Ngando T, Amblard C, Dolan J (2004) Viral activity in two contrasting lake ecosystems. Appl Environ Microbiol 70(5):2941–2951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bettarel Y, Bouvy M, Dumont C, Sime-Ngando T (2006) Virus-bacterium interactions in water and sediment of West African inland aquatic systems. Appl Environ Microbiol 72(8):5274–5282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boras JA, Sala MM, Arrieta JM, Sà EL, Felipe J, Agusti S, Duarte CM, Vaqué D (2010) Effect of ice melting on bacterial carbon fluxes channelled by viruses and protists in the Arctic Ocean. Polar Biol 33(12):1695–1707

    Article  Google Scholar 

  • Borriss M, Lombardot T, Glockner FO, Becher D, Albrecht D, Schweder T (2007) Genome and proteome characterization of the psychrophilic Flavobacterium bacteriophage 11b. Extremophiles 11:95–104

    Article  CAS  PubMed  Google Scholar 

  • Brum, JR, Hurwitz BL, Schofield O, Ducklow HW, Sullivan MB (2016) Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics. ISME J 10:437–449

    Google Scholar 

  • Brussaard CPD, Timmermans KR, Uitz J, Veldhuis MJW (2008) Virioplankton dynamics and virally induced phytoplankton lysis versus microzooplankton grazing southeast of the Kerguelen (Southern Ocean). Deep-Sea Res Part II: Topical Stud Oceanogr 55(5–7):752–765

    Article  Google Scholar 

  • Chénard C, Suttle CA (2008) Phylogenetic diversity of sequences of cyanophage photosynthetic gene psbA in marine and freshwaters. Appl Environ Microbiol 74(17):5317–5324

    Article  PubMed  PubMed Central  Google Scholar 

  • Chénard C, Chan AM, Vincent WF, Suttle CA (2015) Polar freshwater cyanophage S-EIV1 represents a new widespread evolutionary lineage of phages. ISME J 9:2046–2058

    Google Scholar 

  • Colangelo-Lillis JR, Deming JW (2013) Genomic analysis of cold-active Colwelliaphage 9A and psychrophilic phage-host interactions. Extremophiles: Life Under Extreme Conditions 17(1):99–114

    Article  CAS  Google Scholar 

  • Cottrell MT, Kirchman DL (2012) Virus genes in arctic marine bacteria identified by metagenomic analysis. Aquat Microb Ecol 66(2):107–116

    Article  Google Scholar 

  • DeMaere MZ, Williams TJ, Allen MA, Brown MV, Gibson JAE, Rich J, Lauro FM et al (2013) High level of intergenera gene exchange shapes the evolution of haloarchaea in an isolated Antarctic lake. Proc Natl Acad Sci U S A 110(42):16939–16944

    Google Scholar 

  • Derelle E, Ferraz C, Escande ML, Eychenié S, Cooke R, Piganeau G, Desdevises Y, Bellec L, Moreau H, Grimsley N (2008) Life-cycle and genome of OtV5, a large DNA virus of the pelagic marine unicellular green alga Ostreococcus tauri. PLoS ONE 3(5)

    Google Scholar 

  • Desnues C, La Scola B, Yutin N, Fournous G, Robert C, Azza S, Jardot P et al (2012) Provirophages and transpovirons as the diverse mobilome of giant viruses. Proc Natl Acad Sci U S A 109(44):18078–18083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dore JE, Priscu JC (2001) Phytoplankton phosphorus deficiency and alkaline phosphatase activity in the McMurdo Dry Valley lakes, Antarctica. Limnol Oceanogr 46(6):1331–1346

    Article  CAS  Google Scholar 

  • Evans C, Brussaard CPD (2012) Regional variation in lytic and lysogenic viral infection in the Southern Ocean and its contribution to biogeochemical cycling. Appl Environ Microbiol 78(18):6741–6748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans C, Pearce I, Brussaard CPD (2009) Viral-mediated lysis of microbes and carbon release in the sub-Antarctic and Polar Frontal zones of the Australian Southern Ocean. Environ Microbiol 11(11):2924–2934

    Article  CAS  PubMed  Google Scholar 

  • Fischer MG, Suttle CA (2011) A virophage at the origin of large DNA transposons. Science 332:231–234

    Google Scholar 

  • Fischer UR, Velimirov B (2002) High control of bacterial production by viruses in a eutrophic oxbow lake. Aquat Microb Ecol 27(1):1–12

    Article  Google Scholar 

  • Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399(6736):541–548

    Article  CAS  PubMed  Google Scholar 

  • Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL, Brown JH (2008) A latitudinal diversity gradient in planktonic marine bacteria. Proc Natl Acad Sci U S A 105(22):7774–7778

    Google Scholar 

  • Gowing MM (2003) Large viruses and infected microeukaryotes in Ross Sea summer pack ice habitats. Mar Biol 142(5):1029–1040

    Article  Google Scholar 

  • Gowing MM, Riggs BE, Garrison DL, Gibson AH, Jeffries MO (2002) Large viruses in Ross Sea late autumn pack ice habitats. Mar Ecol Prog Ser 241:1–11

    Article  Google Scholar 

  • Granéli W, Bertilsson S, Philibert A (2004) Phosphorus limitation of bacterial growth in high Arctic lakes and ponds. Aquat Sci 66(4):430–439

    Article  Google Scholar 

  • Guixa-Boixereu N, Vaqué D, Gasol JM, Sánchez-Cámara J, Pedrós-Alió C (2002) Viral distribution and activity in Antarctic waters. Deep-Sea Res Part II: Topical Stud Oceanogr 49(4–5):827–845

    Article  Google Scholar 

  • Hennes KP, Simon M (1995) Significance of bacteriophage for controlling bacterioplankton in a mesotrophic lake. Appl Environ Microbiol 61(1):333–340

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hillebrand H (2004) Strength, slope and variability of marine latitudinal gradients. Mar Ecol Prog Ser 273(1992):251–267

    Article  Google Scholar 

  • Hofer JS, Sommaruga R (2001) seasonal dynamics of viruses in an alpine lake: importance of filamentous forms. Aquat Microb Ecol 26(1):1–11

    Article  Google Scholar 

  • Jain M, Fiddes IT, Miga KH, Olsen HE, Paten B, Akeson M (2015) Improved data analysis for the MinION nanopore sequencer. Nature Methods 12(4):351–356

    Google Scholar 

  • Jiang SC, Paul JH (1998) Significance of lysogeny in the marine environment: studies with isolates and a model of lysogenic phage production. Microb Ecol 35:235–243

    Article  CAS  PubMed  Google Scholar 

  • Kepner RL, Wharton RA, Suttle CA (1998) Viruses in Antarctic lakes. Limnol Oceanogr 43(7):1754–1761

    Article  PubMed  Google Scholar 

  • Knowles B, Silveira CB, Bailey BA, Barott K, Cantu VA, Cobián-Güemes AG, Coutinho FH et al (2016) Lytic to temperate switching of viral communities. Nature 531(7595):466–470

    Google Scholar 

  • La Scola B, Desnues C, Pagnier I, Robert C, Barrassi L, Fournous G, Merchat M et al (2008) The virophage as a unique parasite of the giant mimivirus. Nature 455(7209):100–104

    Article  CAS  PubMed  Google Scholar 

  • Lauro FM, DeMaere MZ, Yau S, Brown MV, Ng C, Wilkins D, Raftery MJ et al (2011) An integrative study of a meromictic lake ecosystem in Antarctica. ISME J 5(5):879–895

    Article  CAS  PubMed  Google Scholar 

  • Laybourn-Parry J, Marshall WA, Madan NJ (2007) Viral dynamics and patterns of lysogeny in saline Antarctic lakes. Polar Biol 30:351–358

    Google Scholar 

  • Lindell D, Jaffe JD, Coleman ML, Futschik ME, Axmann IM, Rector T, Kettler G et al (2007) Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449(7158):83–86

    Google Scholar 

  • Lisle JT, Priscu JC (2004) The occurrence of lysogenic bacteria and microbial aggregates in the lakes of the McMurdo Dry Valleys, Antarctica. Microb Ecol 47(1):427–439

    CAS  PubMed  Google Scholar 

  • Logares R, BrÃ¥te J, Bertilsson S, Clasen JL, Shalchian-Tabrizi K, Rengefors K (2009) Infrequent marine-freshwater transitions in the microbial world. Trends Microbiol 17(9):414–422

    Article  CAS  PubMed  Google 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(5954):858–861

    Google Scholar 

  • Lõpez-Bueno A, Rastrojo A, Peirõ R, Arenas M, Alcamí A (2015) Ecological connectivity shapes quasispecies structure of RNA viruses in an Antarctic lake. Mol Ecol 24(19):4812–4825

    Article  PubMed  Google Scholar 

  • Madan NJ, Marshall WA, Laybourn-Parry J (2005) Virus and microbial loop dynamics over an annual cycle in three contrasting Antarctic lakes. Freshwater Biol 50(8):1291–1300

    Google Scholar 

  • Maranger R, Bird DF (1995) Viral abundance in aquatic systems : a comparison between marine and fresh waters. Mar Ecol Prog Ser 121:217–226

    Google Scholar 

  • Maranger R, Bird DF, Juniper SK (1994) Viral and bacterial dynamics in Arctic sea ice during the spring algal bloom near Resolute, NWT, Canada. Mar Ecol Prog Ser 111:121–128

    Article  Google Scholar 

  • Middelboe M, Jørgensen NOG, Kroer N (1996) Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl Environ Microbiol 62(6):1991–1997

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M, Mikhailova N, Rubin E, Ivanova NN, Kyrpides NC (2016) Uncovering Earth’s virome. Nature 536(7617):425–430

    Google Scholar 

  • Paul JH (2008) Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J 2(6):579–589

    Article  CAS  PubMed  Google Scholar 

  • Payet JP, Suttle CA (2008) Physical and biological correlates of virus dynamics in the southern Beaufort Sea and Amundsen Gulf. J Mar Syst 74(3–4):933–945

    Google Scholar 

  • Payet J, Suttle CA (2013) To kill or not to kill: the balance between lytic and lysogenic viral infection is driven by trophic status. Limnol Oceanogr 58(2):465–474

    Google Scholar 

  • Proctor LM, Fuhrman JA (1990) Viral mortality of marine bacteria and cyanobacteria. Nature 343:60–62

    Article  Google Scholar 

  • Rinke C, Low LY, Woodcroft BJ, Raina JB, Skarshewski A, Le X, Butler MK et al (2016) Validation of picogram- and femtogram-input DNA libraries for microscale metagenomics. PeerJ, 1–28

    Google Scholar 

  • Santini S, Jeudy S, Bartoli J, Poirot O, Lescot M, Abergel C, Barbe V et al (2013) Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes. Proc Natl Acad Sci U S A 110(26):10800–10805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Säwström C, Mumford P, Marshall W, Hodson A, Laybourn-Parry J (2002) The microbial communities and primary productivity of cryoconite holes in an Arctic glacier (Svalbard 79 degrees N). Polar Biol 25:591–596.

    Google Scholar 

  • Säwström C, Laybourn-Parry J, Granéli W, Anesio AM (2007a) Heterotrophic bacterial and viral dynamics in Arctic freshwaters: results from a field study and nutrient-temperature manipulation experiments. Polar Biol 30(11):1407–1415

    Article  Google Scholar 

  • Säwström C, Anesio MA, Granéli W, Laybourn-Parry J (2007b) Seasonal viral loop dynamics in two large ultraoligotrophic Antarctic freshwater lakes. Microb Ecol 53(1):1–11

    Article  PubMed  Google Scholar 

  • Säwström C, Granéli W, Laybourn-Parry J, Anesio AM (2007c) High viral infection rates in Antarctic and Arctic bacterioplankton. Environ Microbiol 9(1):250–255

    Article  PubMed  Google Scholar 

  • Säwström C, Lisle J, Anesio AM, Priscu JC, Laybourn-Parry J (2008a) Bacteriophage in polar inland waters. Extremophiles: Life under Extreme Conditions 12(2):167–175

    Article  Google Scholar 

  • Säwström C, Pearce I, Davidson AT, Rosén P, Laybourn-Parry J (2008b) Influence of environmental conditions, bacterial activity and viability on the viral component in 10 Antarctic lakes. FEMS Microbiol Ecol 63(1):12–22

    Article  PubMed  Google Scholar 

  • Short CM, Suttle CA (2005) Nearly identical bacteriophage structural gene sequences are widely distributed in both marine and freshwater environments. Appl Environ Microbiol 71(1):480–486

    Google Scholar 

  • Slimani M, Pagnier I, Raoult D, La Scola B (2013) Amoebae as battlefields for bacteria, giant viruses, and virophages. J Virol 87(8):4783–4785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steward GF, Smith DC, Azam F (1996) Abundance and production of bacteria and viruses in the Bering and Chukchi Seas 131:287–300

    Google Scholar 

  • Sullivan MB, Coleman ML, Quinlivan V, Rosenkrantz JE, DeFrancesco AS, Tan G, Fu R et al (2008) Portal protein diversity and phage ecology. Environ Microbiol 10(10):2810–2823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suttle CA (2005) Viruses in the sea. Nature 437(7057):356–361

    Article  CAS  PubMed  Google Scholar 

  • Suttle CA (2007) Marine viruses-major players in the global ecosystem. Nat Rev Microbiol 5(10):801–812

    Article  CAS  PubMed  Google Scholar 

  • Thingstad TF (2000) Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr 45(6):1320–1328

    Article  Google Scholar 

  • Tschitschko B, Williams TJ, Allen MA, Páez-Espino D, Kyrpides N, Zhong L, Raftery MJ, Cavicchioli R (2015) Antarctic archaea–virus interactions: metaproteome-led analysis of invasion, evasion and adaptation. ISME J 9:2094–2107

    Google Scholar 

  • Veillette J, Lovejoy C, Potvin M, Harding T, Jungblut AD, Antoniades D, Chénard C, Suttle CA, Vincent WF (2011) Milne Fiord epishelf lake: a coastal Arctic ecosystem vulnerable to climate change. Ecoscience 18(3):304–316

    Google Scholar 

  • Weinbauer MG, Winter C, Höfle MG (2002) Reconsidering transmission electron microscopy based estimates of viral infection of bacterioplankton using conversion factors derived from natural communities. Aquat Microb Ecol 27(2):103–110

    Article  Google Scholar 

  • Weitz JS, Wilhelm SW (2012) Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biol Rep 4:17

    Google Scholar 

  • Wells LE, Deming JW (2006a) Characterization of a cold-active bacteriophage on two psychrophilic marine hosts. Aquat Microb Ecol 45(1):15–29

    Article  Google Scholar 

  • Wells LE, Deming JW (2006b) Modelled and measured dynamics of viruses in Arctic winter sea-ice brines. Environ Microbiol 8(6):1115–1121

    Article  PubMed  Google Scholar 

  • Wilhelm SW, Smith REH (2000) Bacterial carbon production in Lake Erie is influenced by viruses and solar radiation. Can J Fish Aquat Sci 57(2):317–326

    Article  Google Scholar 

  • Wilhelm SW, Suttle CA (1999) Viruses and nutrient cycles in the sea aquatic food webs. Bioscience 49(10):781–788

    Article  Google Scholar 

  • Wilhelm SW, Brigden SM, Suttle CA (2002) A dilution technique for the direct measurement of viral production: a comparison in stratified and tidally mixed coastal waters. Microb Ecol 43(1):168–173

    Google Scholar 

  • Wilkins D, Yau S, Williams TJ, Allen MA, Brown MV, DeMaere MZ, Lauro FM, Cavicchioli R (2013) Key microbial drivers in Antarctic aquatic environments. FEMS Microbiol Rev 37(3):303–335

    Google Scholar 

  • Winter C, Garcia JAL, Weinbauer MG, DuBow MS, Herndl GJ (2014) Comparison of deep-water viromes from the Atlantic Ocean and the Mediterranean Sea. PLoS ONE 9(6):1–8

    Google Scholar 

  • Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev: MMBR 64(1):69–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yau S, Lauro FM, DeMaere MZ, Brown MV, Thomas T, Raftery MJ, Andrews-Pfannkoch C et al (2011) Virophage control of antarctic algal host-virus dynamics. Proc Natl Acad Sci U S A 108(15):6163–6168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yilmaz S, Allgaier M, Hugenholtz P (2010) Multiple displacement amplification compromises quantitative analysis of metagenomes. Nature 7(12):943–944

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Asian School of the Environment, Nanyang Technological University, Singapore, Singapore

    Caroline Chénard

  2. Asian School of the Environment and Singapore Centre for Environmental Life Sciences Engineering (SCELSE), Nanyang Technological University, Singapore, Singapore

    Federico M. Lauro

Authors
  1. Caroline Chénard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Federico M. Lauro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Federico M. Lauro .

Editor information

Editors and Affiliations

  1. Singapore Center Envmtl. Life Sc. Engineer., Nanyang Technological Univ., Singapore, Singapore

    Caroline Chénard

  2. Singapore Center Envmtl. Life Sc. Engineer., Nanyang Technological Univ., Singapore, Singapore

    Federico M. Lauro

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Chénard, C., Lauro, F.M. (2017). Exploring the Viral Ecology of High Latitude Aquatic Systems. In: Chénard, C., Lauro, F. (eds) Microbial Ecology of Extreme Environments. Springer, Cham. https://doi.org/10.1007/978-3-319-51686-8_8

Download citation

Publish with us

Policies and ethics

Search

Navigation