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Seasonal variations in viral distribution, dynamics, and viral-mediated host mortality in the Arabian Sea

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Abstract

Viruses are key players in the marine ecosystem. It is critical to study specific viral processes and their inter-relationship with various biotic and abiotic variables to quantify their impact on the marine environment. This study investigates the influence of seasonality on viral distribution and their mediated processes in the coastal region of the southeastern Arabian Sea (India) for two consecutive years (2014 and 2015). Water samples were collected from four sampling stations, S1, S2, S3 and S4, in the southeastern Arabian Sea on a monthly basis. Samples were analyzed for the variations in viral abundance, viral production, and viral-induced host mortality covering three seasons namely, pre-monsoon, monsoon and post-monsoon. Viruses and bacteria were enumerated by epifluorescence microscopy following staining with SYBR Green I and viral production was estimated using viral dilution method. Seasonal variations in viral-mediated mortality and microzooplankton grazing mortality of phytoplankton hosts were estimated by modified dilution method. The results revealed a pronounced seasonal pattern of viral abundance (0.04–4.03 × 107 viruses mL−1) and viral production (0.71 × 1010–4.94 × 1010 L−1d−1). The observed high viral-induced mortality of prokaryotes (25.85%) and phytoplankton (7.98–28.9%) during the pre-monsoon season was eventually linked to high viral abundance and production rates. Viral-mediated processes were essentially linked to host density and water temperature. Transmission electron microscopy analysis revealed that myoviruses and non-tailed viruses were dominant in the study region with rod-shaped bacteria being more susceptible to viral infection. The results indicated the prevalence of seasonally induced active viral processes in this tropical marine ecosystem which may significantly contribute to rapid recycling of nutrients in this region.

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Availability of data and material

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Auguet JC, Montanie H, Lebaron P (2006) Structure of virioplankton in the Charente Estuary (France): transmission electron microscopy versus pulsed field gel electrophoresis. Microb ecol 51:197–208

    CAS  PubMed  Google Scholar 

  • Baudoux AC, Noordeloos AA, Veldhuis MJ, Brussaard CP (2006) Virally induced mortality of Phaeocystis globosa during two spring blooms in temperate coastal waters. Aquat Microb Ecol 44:207–217

    Google Scholar 

  • Baudoux AC, Veldhuis MJ, Witte HJ, Brussaard CP (2007) Viruses as mortality agents of picophytoplankton in the deep chlorophyll maximum layer during IRONAGES III. Limnol Oceanogr 52:2519–2529

    CAS  Google Scholar 

  • Baudoux AC, Veldhuis MJ, Noordeloos AA, Van Noort G, Brussaard CP (2008) Estimates of virus-vs. grazing induced mortality of picophytoplankton in the North Sea during summer. Aquat Microb Ecol 52:69–82

    Google Scholar 

  • Binder B (1999) Reconsidering the relationship between virally induced bacterial mortality and frequency of infected cells. Aquat Microb Ecol 18:207–215

    Google Scholar 

  • Borrel G, Colombe J, Robin A, Lehours AC, Prangishvili D, Sime-Ngando T (2012) Unexpected and novel putative viruses in the sediments of a deep-dark permanently anoxic freshwater habitat. ISME J 6:2119

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bratbak G, Heldal M, Norland S, Thingstad TF (1990) Viruses as partners in spring bloom microbial trophodynamics. Appl Environ Microbiol 56:1400–1405

    CAS  PubMed  PubMed Central  Google Scholar 

  • Breitbart M, Bonnain C, Malki K, Sawaya NA (2018) Phage puppet masters of the marine microbial realm. Nat Microbiol 3:754

    CAS  PubMed  Google Scholar 

  • Brum JR, Schenck RO, Sullivan MB (2013) Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses. The ISME J 7:1738–1751

    CAS  PubMed  Google Scholar 

  • Burkill PH, Mantoura RF, Owens NJ (1993) Biogeochemical cycling in the northwestern Indian Ocean: a brief overview. Deep Sea Res Part II Top Stud Oceanogr 40:643–649

    Google Scholar 

  • Calleja ML, Al-Otaibi N, Morán XA (2019) Dissolved organic carbon contribution to oxygen respiration in the central Red Sea. Sci Rep. https://doi.org/10.1038/s41598-019-40753-w

    Article  PubMed  PubMed Central  Google Scholar 

  • Campbell L, Landry MR, Constantinou J, Nolla HA, Brown SL, Liu H, Caron DA (1998) Response of microbial community structure to environmental forcing in the Arabian Sea. Deep Sea Res Part Top Stud Oceanogr 45:2301–2325

    Google Scholar 

  • Clokie MR, Millard AD, Mehta JY, Mann NH (2006) Virus isolation studies suggest short-term variations in abundance in natural cyanophage populations of the Indian Ocean. J Mar Biolog Assoc UK 86:499–505

    CAS  Google Scholar 

  • Cram JA, Parada AE, Fuhrman JA (2016) Dilution reveals how viral lysis and grazing shape microbial communities. Limnol Oceanogr 61:889–905

    Google Scholar 

  • De Corte D, Sintes E, Yokokawa T, Lekunberri I, Herndl GJ (2016) Large-scale distribution of microbial and viral populations in the South Atlantic Ocean. Environ Microbiol Rep 8:305–315

    PubMed  PubMed Central  Google Scholar 

  • Demory D, Arsenieff L, Simon N, Six C, Rigaut-Jalabert F, Marie D et al (2017) Temperature is a key factor in Micromonas–virus interactions. ISME J 11:601

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ducklow HW (1993) Bacterioplankton distributions and production in the northwestern Indian Ocean and Gulf of Oman, September 1986. Deep Sea Res Part Top Stud Oceanogr 40:753–771

    Google Scholar 

  • Evans C, Archer SD, Jacquet S, Wilson WH (2003) Direct estimates of the contribution of viral lysis and microzooplankton grazing to the decline of a Micromonas spp. population. Aquat Microb Ecol 30:207–219

    Google Scholar 

  • Finke J, Hunt B, Winter C, Carmack E, Suttle C (2017) Nutrients and other environmental factors influence virus abundances across oxic and hypoxic marine environments. Viruses 9:152

    PubMed Central  Google Scholar 

  • Gainer PJ, Pound HL, Larkin AA, LeCleir GR, DeBruyn JM, Zinser ER, Johnson ZI, Wilhelm SW (2017) Contrasting seasonal drivers of virus abundance and production in the North Pacific Ocean. PLoS ONE 12:e0184371

    PubMed  PubMed Central  Google Scholar 

  • Gerson VJ, Madhu NV, Jyothibabu R, Balachandran KK, Nair M, Revichandran C (2014) Oscillating environmental responses of the eastern Arabian Sea. Indian J Mar Sci 43:67–75

    Google Scholar 

  • Grasshoff K, Ehrhardt MKK (1983) Methods of seawater analysis. Verlag Chemie, Weinheim

    Google Scholar 

  • Hammer O, Harper DA, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  • Hoppe HG, Breithaupt P, Walther K, Koppe R, Bleck S, Sommer U, Jürgens K (2008) Climate warming in winter affects the coupling between phytoplankton and bacteria during the spring bloom: a mesocosm study. Aquat Microb Ecol 51:105–115

    Google Scholar 

  • Jain A, Bandekar M, Gomes J, Shenoy D, Meena RM, Naik H, Khandeparkar R, Ramaiah N (2014) Temporally invariable bacterial community structure in the Arabian Sea oxygen minimum zone. Aquat Microb Ecol 73:51–67

    Google Scholar 

  • Jasna V, Parvathi A, Ram ASP, Balachandran KK, Madhu NV, Nair M, Jyothibabu R, Jayalakshmi KV, Revichandran C, Sime-Ngando T (2017) Viral-induced mortality of prokaryotes in a tropical monsoonal estuary. Front Microbiol 8:895

    PubMed  PubMed Central  Google Scholar 

  • Jasna V, Parvathi A, Aswathy VK, Aparna S, Dayana M, Aswathy AJ, Madhu NV (2019) Factors determining variations in viral abundance and viral production in a tropical estuary influenced by monsoonal cycles. Reg Stud Mar Sci. https://doi.org/10.1016/j.rsma.2019.100589

    Article  Google Scholar 

  • Kumar SP, Prasad TG (1996) Winter cooling in the northern Arabian Sea. Curr Sci 71:834–841

    Google Scholar 

  • Kumar SP, Madhupratap M, Kumar MD, Gauns M, Muraleedharan PM, Sarma VV, De Souza SN (2000) Physical control of primary productivity on a seasonal scale in central and eastern Arabian Sea. J Earth Syst Sci 109:433–441

    Google Scholar 

  • Lara E, Vaqué D, Sà EL, Boras JA, Gomes A, Borrull E et al (2017) Unveiling the role and life strategies of viruses from the surface to the dark ocean. Sci Adv 3:e1602565

    PubMed  PubMed Central  Google Scholar 

  • Maat DS, Crawfurd KJ, Timmermans KR, Brussaard CP (2014) Elevated CO2 and phosphate limitation favor Micromonas pusilla through stimulated growth and reduced viral impact. Appl Environ Microbiol 80:3119–3127

    PubMed  PubMed Central  Google Scholar 

  • Maat D, Biggs T, Evans C, van Bleijswijk J, van der Wel N, Dutilh B, Brussaard C (2017) Characterization and temperature dependence of Arctic Micromonas polaris viruses. Viruses 9:134

    PubMed Central  Google Scholar 

  • Mantoura RFC, Law CS, Owens NJP, Burkhill PH, Woodward EMS, Howland RJM, Llewellyn CA (1993) Nitrogen biogeochemical cycling in the northwestern Indian Deep Sea Res Part II Top Stud Oceanogr 40:651–671

    CAS  Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Google Scholar 

  • Middelboe M (2000) Bacterial growth rate and marine virus–host dynamics. Microb Ecol 40:114–124

    CAS  PubMed  Google Scholar 

  • Mojica KD, Brussaard CP (2014) Factors affecting virus dynamics and microbial host–virus interactions in marine environments. FEMS Microbiol Ecol 89:495–515

    CAS  PubMed  Google Scholar 

  • Mojica KD, Huisman J, Wilhelm SW, Brussaard CP (2016) Latitudinal variation in virus-induced mortality of phytoplankton across the North Atlantic Ocean. ISME J 10:500

    CAS  PubMed  Google Scholar 

  • Motegi C, Kaiser K, Benner R, Weinbauer MG (2014) Effect of P-limitation on prokaryotic and viral production in surface waters of the Northwestern Mediterranean Sea. J Plankton Res 37:16–20

    Google Scholar 

  • Naqvi SWA, Noronha RJ, Somasundar K, Gupta RS (1990) Seasonal changes in the denitrification regime of the Arabian Sea. Deep Sea Res Oceanogr Res Pap 37:593–611

    CAS  Google Scholar 

  • Olson DB, Hitchcock GL, Fine RA, Warren BA (1993) Maintenance of the low-oxygen layer in the central Arabian Sea. Deep Sea Res Top Stud Oceanogr 40:673–685

    CAS  Google Scholar 

  • Ortmann AC, Metzger RC, Liefer JD, Novoveska L (2011) Grazing and viral lysis vary for different components of the microbial community across an estuarine gradient. Aquat microb ecol 65:143–157

    Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A Manual for Biological and Chemical Methods for Seawater Analysis. Pergamon, Oxford

    Google Scholar 

  • Parsons RJ, Breitbart M, Lomas MW, Carlson CA (2012) Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J 6:273

    CAS  PubMed  Google Scholar 

  • Parvathi A, Jasna V, Jina S, Jayalakshmy KV, Lallu KR, Madhu NV, Muraleedharan KR, Naveen Kumar KR, Balachandran KK (2015) Effects of hydrography on the distribution of bacteria and virus in Cochin estuary, India. Ecol Res 30:85–92

    CAS  Google Scholar 

  • Parvathi A, Jasna V, Aparna S, Ram ASP, Aswathy V, Balachandran KK, Muraleedharan KR, Mathew D, Sime-Ngando T (2018) High Incidence of Lysogeny in the Oxygen Minimum Zones of the Arabian Sea (Southwest Coast of India). Viruses 10:588

    CAS  PubMed Central  Google Scholar 

  • Patel A, Noble RT, Steele JA, Schwalbach MS, Hewson I, Fuhrman JA (2007) Virus and prokaryote enumeration from planktonic aquatic environments by epifluorescence microscopy with SYBR Green I. Nat Protoc 2:269

    CAS  PubMed  Google Scholar 

  • Pradeep Ram AS, Arnous B, Danger M, Carrias JF, Lacroix G, Sime-Ngando T (2010) High and differential viral infection rates within bacterial ‘morphopopulations’ in a shallow sand pit lake (Lac de Créteil, France). FEMS Microbiol Ecol 74:83–92

    Google Scholar 

  • Ramaiah N, Raghukumar S, Gauns M (1996) Bacterial abundance and production in the central and eastern Arabian Sea. Curr Sci 71:878–882

    Google Scholar 

  • Ramaiah N, Fernandes V, Rodrigues VV, Paul JT, Gauns M (2009) Bacterioplankton abundance and production in Indian Ocean Regions. Indian Ocean Biogeochem Process Ecol Variabil 1:119–132

    Google Scholar 

  • Rao AD, Joshi M, Ravichandran M (2008) Oceanic upwelling and downwelling processes in waters off the west coast of India. Ocean Dyn 58:213–226

    Google Scholar 

  • Rodriguez F, Fernandez E, Head RN, Harbour DS, Bratbak G, Heldal M, Harris RP (2000) Temporal variability of viruses, bacteria, phytoplankton and zooplankton in the western English Channel off Plymouth. J Mar Biolog Assoc UK 80:575–586

    CAS  Google Scholar 

  • Rowe JM, Saxton MA, Cottrell MT, DeBruyn JM, Berg GM, Kirchman DL, Hutchins DA, Wilhelm SW (2008) Constraints on viral production in the Sargasso Sea and North Atlantic. Aquat Microb Ecol 52:233–244

    Google Scholar 

  • Rowe JM, DeBruyn JM, Poorvin L, LeCleir GR, Johnson ZI, Zinser ER, Wilhelm SW (2012) Viral and bacterial abundance and production in the Western Pacific Ocean and the relation to other oceanic realms. FEMS Microbiol Ecol 79:359–370

    CAS  PubMed  Google Scholar 

  • Sabbagh EI, Huete-Stauffer TM, Calleja ML, Silva L, Viegas M, Morán XA (2020) Weekly variations of viruses and heterotrophic nanoflagellates and their potential impact on bacterioplankton in shallow waters of the central Red Sea. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiaa033

    Article  PubMed  PubMed Central  Google Scholar 

  • Sarmento H, Montoya JM, Vázquez-Domínguez E, Vaqué D, Gasol JM (2010) Warming effects on marine microbial food web processes: how far can we go when it comes to predictions? Philos Trans R Soc Lond B Biol Sci 365:2137–2149

    PubMed  PubMed Central  Google Scholar 

  • Shelford EJ, Middelboe M, Møller EF, Suttle CA (2012) Virus-driven nitrogen cycling enhances phytoplankton growth. Aquat Microb Ecol 66:41–46

    Google Scholar 

  • Stopar D, Černe A, Žigman M, Poljšak-Prijatelj M, Turk V (2003) Viral abundance and a high proportion of lysogens suggest that viruses are important members of the microbial community in the Gulf of Trieste. Microb ecol 46:249–256

    CAS  PubMed  Google Scholar 

  • Suh SS, Park M, Hwang J, Kil EJ, Jung SW, Lee S, Lee TK (2015) Seasonal dynamics of marine microbial community in the South Sea of Korea. PLoS ONE 10:e0131633

    PubMed  PubMed Central  Google Scholar 

  • Taylor GT, Hein C, Iabichella M (2003) Temporal variations in viral distributions in the anoxic Cariaco Basin. Aquat Microb Ecol 30:103–116

    Google Scholar 

  • Thomas R, Berdjeb L, Sime-Ngando T, Jacquet S (2011) Viral abundance, production, decay rates and life strategies (lysogeny versus lysis) in Lake Bourget (France). Environ Microbiol 13:616–630

    CAS  PubMed  Google Scholar 

  • Vazquez-Dominiguez E, Vaque D, Gasol JM (2007) Ocean warming enhances respiration and carbon demand of coastal microbial plankton. Glob Chang Biol 13:1327–1334

    Google Scholar 

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

    Google Scholar 

  • Weinbauer MG, Bonilla-Findji O, Chan AM, Dolan JR, Short SM, Šimek K, Wilhelm SW, Suttle CA (2011) Synechococcus growth in the ocean may depend on the lysis of heterotrophic bacteria. J Plankton Res 33:1465–1476

    Google Scholar 

  • Wiebinga CJ, Veldhuis MJ, De Baar HJ (1997) Abundance and productivity of bacterioplankton in relation to seasonal upwelling in the northwest Indian Ocean. Deep Sea Res Oceanogr Res Pap 44:451–476

    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. Microb Ecol 43:168–173

    CAS  PubMed  Google Scholar 

  • Williamson SJ, Paul JH (2006) Environmental factors that influence the transition from lysogenic to lytic existence in the ϕHSIC/Listonella pelagia marine phage–host system. Microb Ecol 52:217–225

    CAS  PubMed  Google Scholar 

  • Winter C, Moeseneder MM, Herndl GJ, Weinbauer MG (2008) Relationship of geographic distance, depth, temperature, and viruses with prokaryotic communities in the eastern tropical Atlantic Ocean. Microb Ecol 56:383–389

    PubMed  Google Scholar 

  • Winter C, Payet JP, Suttle CA (2012) Modeling the Winter–to–Summer Transition of Prokaryotic and Viral Abundance in the Arctic Ocean. PLoS ONE 7:e52794

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

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Acknowledgements

The authors are thankful to the Director, CSIR-NIO, Goa, India and the Scientist-in-Charge, NIO (RC), Cochin, India for their support and advice. The authors are grateful to Dr. R Jyothibabu for helping with sample collection.

Funding

This work was supported by Indian National Centre for Ocean Information Services through grant-in-aid project [NIO GAP 2807]. AS is grateful to University Grants Commission (UGC), New Delhi, India for her senior research fellowship grant. JV is grateful to Council of Scientific and Industrial Research (CSIR), New Delhi, for her senior research fellowship grant.

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  1. CSIR-National Institute of Oceanography, Regional Centre (CSIR), Dr. Salim Ali Road, Post Box No. 1913, Kochi, 682 018, India

    Aparna Sreekumar, Parvathi Ammini & Jasna Vijayan

  2. Department of Aquatic Life Medicine, College of Fisheries Science, Pukyong National University, Busan, Republic of Korea

    Jasna Vijayan

  3. Laboratoire Microorganismes: Génome Et Environnement, UMR CNRS 6023, Université Clermont-Auvergne, 1 Impasse Amélie Murat, 63178, Aubière Cedex, France

    Pradeep Ram Angia Sriram & Sime-Ngando Telesphore

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  1. Aparna Sreekumar
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Sreekumar, A., Ammini, P., Vijayan, J. et al. Seasonal variations in viral distribution, dynamics, and viral-mediated host mortality in the Arabian Sea. Mar Biol 168, 28 (2021). https://doi.org/10.1007/s00227-020-03816-5

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