Skip to main content

Advertisement

SpringerLink
Log in

Distribution of marine viruses and their potential hosts in Prydz Bay and adjacent Southern Ocean, Antarctic

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Viruses play a key role in all marine ecosystems, and yet little is known of their distribution in Antarctic waters, especially in bathypelagic waters (>1000 m). In this study, the abundance and distribution of viruses and their potential hosts from the surface to the bottom of Prydz Bay, Antarctic, was investigated using flow cytometry. Viruses and autotrophs were abundant in nearshore and continental shelf waters, while heterotrophic bacteria and picoeukaryotes were abundant in offshore waters. Virus and bacteria abundances generally decreased with increasing depth but increased slightly just above the seafloor. Within the water column, maximum virus numbers coincided with the maximum values of chlorophyll a (when greater than 0.1 μg l−1), in the surface and subsurface (25 m). In the open ocean, however, virus abundance usually correlated with bacterial abundance at greater depths (50, 300 and 500 m) where the surface chlorophyll a concentration was lower than 0.1 μg l−1. Viral abundance was correlated with the host cell abundance, and this was different in different pelagic zones (bacteria and autotrophs (i.e., chlorophyll a concentration) in the epipelagic waters, picoeukaryotes and bacteria in mesopelagic waters and bacteria in bathypelagic waters). Principle component analysis and Pearson correlation analysis indicated that there was a close relationship between virus abundance and chlorophyll a, bacteria and nutrients (NO2 + NO3, phosphate and silicate), and picoeukaryote abundance was mainly correlated with water depth and salinity.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Agawin NSR, Agusti S, Duarte CM (2002) Abundance of Antarctic picophytoplankton and their response to light and nutrient manipulation. Aquat Microbial Ecol 29:161–172

    Article  Google Scholar 

  • Arıstegui J, Gasol JM, Duarte CM, Herndl G (2009) Microbial oceanography of the dark ocean’s pelagic realm. Limnol Oceanogr 54:1501–1529

    Article  Google Scholar 

  • Azam F, Fenchel T, Field J, Gray J, Meyer-Reil L, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bird DF, Maranger R, Karl DM (1993) Palmer LTER: aquatic virus abundances near the Antarctic Peninsula. Antarct J US 28:234–235

    Google Scholar 

  • Boehme J, Frischer M, Jiang S, Kellogg C, Pichard S, Rose J, Steinway C, Paul JH (1993) Viruses, bacterioplankton, and phytoplankton in the southeastern Gulf of Mexico: distribution and contribution to oceanic DNA pools. Mar Ecol Prog Ser 97:1–10

    Article  Google Scholar 

  • Brussaard CPD (2004) Optimization of procedures for counting viruses by flow cytometry. Appl Environ Microbiol 70:1506–1513

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brussaard CPD, Wilhelm SW, Thingstad TF, Weinbauer MG (2010) Quantification of aquatic viruses by flow cytometry. In: Wilhelm SW, Weinbauer MG, Suttle CA (eds) Manual of aquatic viral ecology. ASLO

  • Cai YM, Ning XR, Zhu GH, Shi JX (2005) Size fractionated biomass and productivity of phytoplankton and new production in the Prydz Bay and the adjacent Indian sector of the Southern Ocean during the austral summer of 1998/1999. Acta Oceanol Sin 27:135–147

    Google Scholar 

  • Cai YM, Ning XR, Liu CG, Hao Q (2007) Distribution pattern of photosynthetic picoplankton and heterotrophic bacteria in the northern South China Sea. J Integr Plant Biol 49:282–298

    Article  CAS  Google Scholar 

  • Chen, F,  Lu J-R, Binder BJ, Liu YC, Hodson RE (2001) Application of digital image analysis and flow cytometry to enumerate marine viruses stained with SYBR Gold. Appl Environ Microbiol  67:539–545

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Church MJ, DeLong EF, Ducklow HW, Karner MB, Preston CM, Karl DM (2003) Abundance and distribution of planktonic Archaea and Bacteria in the waters west of the Antarctic Peninsula. Limnol Oceanogr 48:1893–1902

    Article  Google Scholar 

  • Corinaldesi C, Crevatin E, Del Negro P, Marini M, Russo A, Fonda-Umani S, Danovaro R (2003) Large-scale spatial distribution of virioplankton in the Adriatic Sea: testing the trophic state control hypothesis. Appl Environ Microbiol 69:2664–2673

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • De Corte D, Sintes E, Winter C, Yokokawa T, Reinthaler T, Herndl GJ (2010) Links between viral and prokaryotic communities throughout the water column in the (sub) tropical Atlantic Ocean. ISME J 4:1431–1442

    Article  PubMed  Google Scholar 

  • De Corte D, Sintes E, Yokokawa T, Reinthaler T, Herndl GJ (2012) Links between viruses and prokaryotes throughout the water column along a North Atlantic latitudinal transect. ISME J 6:1566–1577

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Evans C, Brussaard CP (2012b) Viral lysis and microzooplankton grazing of phytoplankton throughout the Southern Ocean. Limnol Oceanogr 57(6):1826–1837

    Article  Google Scholar 

  • Evans C, Thomson PG, Davidson AT, Bowie AR, van den Enden R, Witte H, Brussaard CPD (2011) Potential climate change impacts on microbial distribution and carbon cycling in the Australian Southern Ocean. Deep Sea Res II 58:2150–2161

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fukuda R, Ogawa H, Nagata T, Koike I (1998) Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microbiol 64:3352–3358

    PubMed Central  CAS  PubMed  Google Scholar 

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

    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 

  • Gowing MM, Garrison DL, Gibson AH, Krupp JM, Jeffries MO, Fritsen CH (2004) Bacterial and viral abundance in Ross Sea summer pack ice communities. Mar Ecol Prog Ser 279:3–12

    Article  CAS  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 II 49:827–845

    Article  Google Scholar 

  • Hara S, Koike I, Terauchi K, Kamiya H, Tanoue E (1996) Abundance of viruses in deep oceanic waters. Mar Ecol Prog Ser 145:269–277

    Article  Google Scholar 

  • Hewson I, Fuhrman JA (2003) Viriobenthos production and virioplankton sorptive scavenging by suspended sediment particles in coastal and pelagic waters. Microb Ecol 46:337–347

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa A, Wright SW, van den Enden RL, Davidson AT, Marchant HJ (2002) Abundance, size structure and community composition of phytoplankton in the Southern Ocean in the austral summer 1999/2000. Polar Biosci 15:11–26

    Google Scholar 

  • Jacobs SS, Georgi DT (1977) Observations on the southwest Indian/Antarctic Ocean. Deep Sea Res 24:43–84

    Google Scholar 

  • Jiao N, Yang Y, Hong N, Ma Y, Harada S, Koshikawa H, Watanabe M (2005) Dynamics of autotrophic picoplankton and heterotrophic bacteria in the East China Sea. Cont Shelf Res 25:1265–1279

    Article  Google Scholar 

  • Jiao N, Herndl GJ, Hansell DA et al (2010) Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol 8:593–599

    Article  CAS  PubMed  Google Scholar 

  • Jin S, Pan J, Han Z (2012) Spatial and temporal variability of chlorophyll a during the Austral summer in Prydz Bay, Antarctic. Chin J Polar Res 24:361–371 (in Chinese with English abstract)

    Article  CAS  Google Scholar 

  • Kopczyńska EE, Goeyens L, Semeneh M, Dehairs F (1995) Phytoplankton composition and cell carbon distribution in Prydz Bay, Antarctica-relation to organic particulate matter and its delta-C-13 values. J Plankton Res 17:685–707

    Article  Google Scholar 

  • Krempin DW, Sullivan CW (1981) The seasonal abundance, vertical distribution, and relative microbial biomass of chroococcoid cyanobacteria at a station in southern California coastal waters. Can J Microbiol 27:1341–1344

    Article  Google Scholar 

  • Li WKW, Jellett JF, Dickie PM (1995) DNA distributions in planktonic bacterial stained with TOTO or TO-PRO. Limnol Oceanogr 40:1485–1495

    Article  CAS  Google Scholar 

  • Li Y, Luo T, Sun J, Cai L, Liang Y, Jiao N, Zhang R (2014) Lytic viral infection of bacterioplankton in deep waters of the western Pacific Ocean. Biogeosciences 11:2531–2542

    Article  Google Scholar 

  • Liang Y, Li L, Luo T, Zhang Y, Zhang R, Jiao N (2014) Horizontal and vertical distribution of marine virioplankton: a basin scale investigation based on a global cruise. PLoS ONE 9:e11634

    Google Scholar 

  • Lin L, He J, Zhao Y, Zhang F, Cai M (2012) Flow cytometry investigation of picoplankton across latitudes and along the circum Antarctic Ocean. Acta Oceanol Sin 31:134–142

    Article  Google Scholar 

  • Magagnini M, Corinaldesi C, Monticelli LS, De Domenico E, Danovaro R (2007) Viral abundance and distribution in mesopelagic and bathypelagic waters of the Mediterranean Sea. Deep Sea Res 54:1209–1220

    Article  Google Scholar 

  • Magiopoulos I, Pitta P (2012) Viruses in a deep oligotrophic sea: seasonal distribution of marine viruses in the epi-, meso- and bathypelagic waters of the Eastern Mediterranean Sea. Deep Sea Res 66:1–10

    Article  Google Scholar 

  • Marchant H, Davidson A, Wright S, Glazebrook J (2000) The distribution and abundance of viruses in the Southern Ocean during spring. Antarct Sci 12:414–417

    Article  Google Scholar 

  • Marie D, Partensky F, Jacquet S, Vaulot D (1997) Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR green I. Appl Environ Microbiol 63:186–193

    PubMed Central  CAS  PubMed  Google Scholar 

  • Marie D, Brussaard CPD, Thyrhaug R, Bratbak G, Vaulot D (1999) Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl Environ Microbiol 65:45–52

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nedwell DB, Rutter M (1994) Influence of temperature on growth rate and competition between two psychrotolerant antarctic bacteria: low temperature diminishes affinity for substrate uptake. Appl Environ Microbiol 60:1984–1992

    PubMed Central  CAS  PubMed  Google Scholar 

  • Olson RJ, Chisholm SW, Zettler ER, Altabet MA, Dusenberry JA (1990) Spatial and temporal distributions of prochlorophyte picoplankton in the North Atlantic Ocean. Deep Sea Res II 37:1033–1051

    Article  Google Scholar 

  • Parada V, Sintes E, van Aken HM, Weinbauer MG, Herndl GJ (2007) Viral abundance, decay, and diversity in the meso- and bathypelagic waters of the North Atlantic. Appl Environ Microbiol 73:4429–4438

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pearce DA, Wilson WH (2003) Viruses in Antarctic ecosystems. Antarct Sci 15:319–331

    Article  Google Scholar 

  • Pearce I, Davidson AT, Bell EM, Wright S (2007) Seasonal changes in the concentration and metabolic activity of bacteria and viruses at an Antarctic coastal site. Aquat Microbial Ecol 47:11–23

    Article  CAS  Google Scholar 

  • Pearce I, Davidson AT, Thomson PG, Wright S, van den Enden R (2010) Marine microbial ecology off East Antarctica (30–80 degrees E): rates of bacterial and phytoplankton growth and grazing by heterotrophic protists. Deep Sea Res II 57:849–862

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Smith DC, Steward GF, Azam F, Hollibaugh JT (1992) Virus and bacteria abundance in the Drake Passage during January and August 1991. Antarct J US 27:125–127

    Google Scholar 

  • Steward GF, Montiel JL, Azam F (2000) Genome size distributions indicate variability and similarities among marine viral assemblages from diverse environments. Limnol Oceanogr 45:1697–1706

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Suttle CA, Chan AM, Cottrell MT (1990) Infection of phytoplankton by viruses and reduction of primary productivity. Nature 347:467–469

    Article  Google Scholar 

  • Tarran GA, Zubkov MV, Sleigh MA, Burkill PH, Yallop M (2001) Microbial community structure and standing stocks in the NE Atlantic in June and July of 1996. Deep Sea Res II 48:963–985

    Article  Google Scholar 

  • Thingstad T, Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microbial Ecol 13:19–27

    Article  Google Scholar 

  • Thomson PG, Davidson AT, Van den Enden R, Pearce I, Seuront L, Paterson JS, Williams GD (2010) Distribution and abundance of marine microbes in the Southern Ocean between 30 and 80°E. Deep Sea Res Part II 57:815–827

    Article  CAS  Google Scholar 

  • Wang M, Liang Y, Bai X, Jiang X, Wang F, Qiao Q (2010) Distribution of microbial populations and their relationship with environmental parameters in the coastal waters of Qingdao, China. Environ Microbiol 12:1926–1939

    Article  CAS  PubMed  Google Scholar 

  • Waters RL, van den Enden R, Marchant HJ (2000) Summer microbial ecology off East Antarctica (80–150°E): protistan community structure and bacterial abundance. Deep Sea Res II 47:2401–2435

    Article  CAS  Google Scholar 

  • Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181

    Article  CAS  PubMed  Google Scholar 

  • Weinbauer MG, Peduzzi P (1995) Significance of viruses versus heterotrophic nanofiagellates for controlling bacterial abundance in the northern Adriatic Sea. J Plank Res 17:1851–1856

    Article  Google Scholar 

  • Weinbauer MG, Brettar I, Höfle MG (2003) Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol Oceanogr 48:1457–1465

    Article  Google Scholar 

  • Weinbauer MG, Arrieta JM, Griebler C, Herndl GJ (2009) Enhanced viral production and infection of bacterioplankton during an iron-induced phytoplankton bloom in the Southern Ocean. Limnol Oceanogr 54:774–784

    Article  CAS  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. Microbial Ecol 43:168–173

    Article  CAS  Google Scholar 

  • Winter C, Kerros M-E, Weinbauer MG (2009) Seasonal and depth-related dynamics of prokaryotes and viruses in surface and deep waters of the northwestern Mediterranean Sea. Deep Sea Res I 56:1972–1982

    Article  CAS  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wommack KE, Hill RT, Kessel M, Russek-Cohen E, Colwell RR (1992) Distribution of viruses in the Chesapeake Bay. Appl Environ Microbiol 58:2965–2970

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wommack KE, Ravel J, Hill RT, Colwell RR (1999a) Hybridization analysis of Chesapeake Bay virioplankton. Appl Environ Microbiol 65:241–250

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wommack KE, Ravel J, Hill RT, Chun J, Colwell RR (1999b) Population dynamics of Chesapeake Bay virioplankton: total-community analysis by pulsed-field gel electrophoresis. Appl Environ Microbiol 65:231–240

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yang Y, Motegi C, Yokokawa T, Nagata T (2010) Large-scale distribution patterns of virioplankton in the upper ocean. Aquat Microbial Ecol 60:233–246

    Article  Google Scholar 

  • Yang Y, Yokokawa T, Motegi C, Nagata T (2014) Large-scale distribution of viruses in deep waters of the Pacific and Southern Oceans. Aquat Microbial Ecol 71:193–202

    Article  Google Scholar 

  • Zubkov M, Sleigh M, Tarran G, Burkill P, Leakey R (1998) Picoplanktonic community structure on an Atlantic transect from 50°N to 50°S. Deep Sea Res I 45:1339–1355

    Article  Google Scholar 

Download references

Acknowledgments

We thank the crews of RV “Xuelong” for their assistance with sample collection during the cruise. This research was supported by the Grants from “Marine biodiversity in the surrounding waters of Antarctic and investigation of ecological environment” (No. CHINARE-2012-01-05 till 2015-01-05), the National Key Basic Research Program of China (No. 2013CB955700) and the SOA Project (No. GASI-03-01-02-05).

Author information

Author notes

    Authors and Affiliations

    1. Key Laboratory of Marine Genetics and Breeding, College Marine Life Sciences, Ministry of Education of China, Ocean University of China, Qingdao, 266003, China

      Y. Liang, X. Bai, Y. Jiang & M. Wang

    2. Qingdao Institute of BioEnergy and BioProcess Technology, Chinese Academy of Sciences, Qingdao, 266101, China

      Y. Liang

    3. SOA Key Laboratory for Polar Science, Polar Research Institute of China, Shanghai, 200136, China

      X. Bai & J. He

    4. No.39 Middle School, Qingdao, Shandong, 266003, China

      X. Bai

    5. Key Lab of Polar Oceanography and Global Ocean Change, Ocean University of China, Qingdao, China

      M. Wang

    6. Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, Australia

      A. McMinn

    Authors
    1. Y. Liang
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. X. Bai
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Y. Jiang
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. M. Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. J. He
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. A. McMinn
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to M. Wang or J. He.

    Additional information

    Y. Liang and X. Bai have contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Liang, Y., Bai, X., Jiang, Y. et al. Distribution of marine viruses and their potential hosts in Prydz Bay and adjacent Southern Ocean, Antarctic. Polar Biol 39, 365–378 (2016). https://doi.org/10.1007/s00300-015-1787-8

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00300-015-1787-8

    Keywords

    Search

    Navigation