Skip to main content
Log in

Viral lysis of Micromonas pusilla: impacts on dissolved organic matter production and composition

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

The viral mediated transformation of phytoplankton organic carbon to dissolved forms (“viral shunt”) has been suggested as a major source of dissolved organic carbon (DOC) in marine systems. Despite the potential implications of viral activity on the global carbon fluxes, studies investigating changes in the DOC composition from viral lysis is still lacking. Micromonas pusilla is an ecologically relevant picoeukaryotic phytoplankter, widely distributed in both coastal and oceanic marine waters. Viruses have been found to play a key role in regulating the population dynamics of this species. In this study we used axenic cultures of exponentially growing M. pusilla to determine the impact of viral lysis on the DOC concentration and composition, as estimated from lysate-derived production of transparent exopolymer particles (TEP) and two fractions of fluorescent dissolved organic matter (DOM): aromatic amino acids (excitation/emission; 280/320 nm; F(280/320)) and marine humic-like fluorescent DOM (320/410 nm; F(320/410)). DOC concentration increased 4.5 times faster and reached 2.6 times higher end concentration in the viral infected compared with the non-infected cultures. The production of F(280/320) and F(320/410) were 4.1 and 2.8 times higher in the infected cultures, and the elevated ratio between F(280/320) and F(320/410) in lysates suggested a higher contribution of labile (protein) components in viral produced DOM than in algal exudates. The TEP production was 1.8 times faster and reached a 1.5 times higher level in the viral infected M. pusilla culture compared with the non- infected cultures. The measured increase in both DOC and TEP concentrations suggests that viral lysis has multiple and opposite implications for the production and export processes in the pelagic ocean: (1) by releasing host biomass as DOC it decreases the organic matter sedimentation and promotes respiration and nutrient retention in the photic zone, whereas (2) the observed enhanced TEP production could stimulate particle aggregation and thus carbon export out of the photic zone.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Balch WM, Vaughn JJ, Goes JI, Novotny JF, Drapeau DT, Booth ES, Vining CL (2007) Bio-optical consequences of viral infection of phytoplankton: I. Experiments with the cyanobacterium Synechococcus sp. Limnol Oceanogr 52:727–738

    Article  Google Scholar 

  • Blough NV, Vecchio RD (2002) Chromophoric DOM in the coastal environment. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic Press, San Diego, pp 509–546

    Chapter  Google Scholar 

  • Bratbak G, Heldal M, Thingstad TF, Riemann B, Haslund OH (1992) Incorporation of viruses into the budget of microbial C-transfer—a 1st approach. Mar Ecol Prog Ser 83:273–280

    Article  Google Scholar 

  • Bratbak G, Thingstad TF, Heldal M (1994) Viruses and the microbial loop. Microb Ecol 28:209–221

    Article  Google Scholar 

  • Bratbak G, Jacobsen A, Heldal M (1998) Viral lysis of Phaeocystis pouchetii and bacterial secondary production. Aquat Microb Ecol 16:11–16

    Article  Google Scholar 

  • Brussaard CPD (2004a) Viral control of phytoplankton populations—a review. J Eukaryot Microbiol 51:125–138

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Brussaard CPD, Riegman R, Noordeloos AAM, Cadee GC, Witte HJ, Kop AJ, Nieuwland G, Van Duyl FC, Bak RPM (1995) Effects of grazing, sedimentation and phytoplankton cell lysis on the structure of a coastal pelagic food web. Mar Ecol Prog Ser 123:259–271

    Article  Google Scholar 

  • Brussaard CPD, Gast GJ, Van Duyl FC, Riegman R (1996) Impact of phytoplankton bloom magnitude on a pelagic microbial food web. Mar Ecol Prog Ser 144:211–221

    Article  Google Scholar 

  • Brussaard CPD, Thyrhaug R, Marie D, Bratbak G (1999) Flow cytometric analyses of viral infection in two marine phytoplankton species, Micromonas pusilla (Prasinophyceae) and Phaeocystis pouchetii (Prymnesiophyceae). J Phycol 35:941–948

    Article  Google Scholar 

  • Brussaard CPD, Marie D, Thyrhaug R, Bratbak G (2001) Flow cytometric analysis of phytoplankton viability following viral infection. Aquat Microb Ecol 26:157–166

    Article  Google Scholar 

  • Brussaard CPD, Kuipers B, Veldhuis MJW (2005a) A mesocosm study of Phaeocystis globosa population dynamics. I. Regulatory role of viruses in bloom control. Harmful algae 4:859–874

    Article  Google Scholar 

  • Brussaard CPD, Mari X, Van Bleijswijk JDL, Veldhuis MJW (2005b) A mesocosm study of Phaeocystis globosa population dynamics. II. Significance for the microbial community. Harmful algae 4:875–893

    Article  Google Scholar 

  • Brussaard CPD, Wilhelm SW, Thingstad TF, Weinbauer MG, Bratbak G, Heldal M, Kimmance SA, Middelboe M, Nagasaki K, Paul JH, Schroeder DC, Suttle CA, Vaque D, Wommack KE (2008) Global scale processes with a nanoscale drive—the role of marine viruses. ISME J 2:575–578

    Article  Google Scholar 

  • Cammack WKL, Kalff J, Prairie YT, Smith EM (2004) Fluorescent dissolved organic matter in lakes: relationships with heterotrophic metabolism. Limnol Oceanogr 49:2034–2045

    Article  Google Scholar 

  • Coble PG (1996) Characterization of marine and terrestrial DOM in seawater using excitation-emission matrix spectroscopy. Mar Chem 51:325–346

    Article  Google Scholar 

  • Coble PG, Green SA, Blough NV, Gasgosian RB (1990) Characterization of dissolved organic matter in the Black Sea by fluorescence spectroscopy. Nature 348:432–435

    Google Scholar 

  • Coffin RB (1989) Bacterial uptake of dissolved free and combined amino acids in estuarine waters. Limnol Oceanogr 34:531–542

    Article  Google Scholar 

  • Cottrell MT, Suttle CA (1995) Dynamics of a lytic virus infecting the photosynthetic marine picoflagellate Micromonas pusilla. Limnol Oceanogr 40:730–739

    Article  Google Scholar 

  • Evans C, Kadner SV, Darroch LD, Wilson WH, Liss PS, Malin G (2007) The relative significance of viral lysis and microzooplankton grazing as pathways of dimethylsulfoniopropionate (DMSP) cleavage: an Emiliania huxleyi culture study. Limnol Oceanogr 52:1036–1045

    Article  Google Scholar 

  • Evans CD, Pond W, Wilson WH (2009) Changes in Emiliania huxleyi fatty acid profiles during infection with E. huxleyi virus 86: physiological and ecological implications. Aquat Microb Ecol 55:219–228

    Article  Google Scholar 

  • Fowler SW, Knauer GA (1986) Role of large particles in the transport of elements and organic compounds through the oceanic water column. Prog Oceanogr 16:147–194

    Article  Google Scholar 

  • Geider RJ, La Roche J, Greene RM, Olaizola M (1993) Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation. J Phycol 29:755–766

    Article  Google Scholar 

  • Gobler CJ, Hutchins DA, Fisher NS, Cosper EM, Sanudo-Wilhelmy SA (1997) Release and bioavailability of elements following viral lysis of a marine chrysophyte. Limnol Oceanogr 42:1492–1504

    Article  Google Scholar 

  • Grossart HP, Simon M (1998) The significance of limnetic organic aggregates (lake snow) for the sinking flux of particulate organic matter in a large lake. Aquat Microb Ecol 15:115–125

    Article  Google Scholar 

  • Grossart HP, Berman T, Simon M, Pohlmann K (1998) Occurrence and microbial dynamics of macroscopic organic aggregates (lake snow) in Lake Kinneret, Israel, in fall. Aquat Microb Ecol 14:59–67

    Article  Google Scholar 

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Chanley MH (ed) Culture of marine invertebrate animals. Plenum, New York, pp 29–60

    Chapter  Google Scholar 

  • Haaber J, Middelboe M (2009) Viral lysis of Phaeocystis pouchetii: implications for algal population dynamics and heterotrophic C, N, and P cycling. ISME J 3:430–441

    Article  Google Scholar 

  • Hansell DA, Carlson CA, Repeta DJ, Schlitzer R (2009) Dissolved organic matter in the ocean: new insights stimulated by a controversy. Oceanography 22:52–61

    Article  Google Scholar 

  • Hansen HP, Koroleff F (1999) Automated chemical analysis. In: Grasshoff K, Kermling K, Ehrhardt M (eds) Methods of seawater analysis. Wiley-VCH, Germany, pp 159–226

    Chapter  Google Scholar 

  • Hedges JI (2002) Why dissolved organic matter? In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic Press, London, pp 1–33

    Chapter  Google Scholar 

  • Jiao N, Herndl GJ, Hansell DA, Benner R, Kattner G, Wilhelm SW, Kirchman DL, Weinbauer MG, Luo T, Chen F, Azam F (2010) Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol 8:593–599

    Article  Google Scholar 

  • Kirchman DL (2004) A primer on dissolved organic material and heterotrophic prokaryotes in the oceans. In: Follows M, Oguz T (eds) The ocean carbon cycle and climate. Kluwer Academic Publishers, Netherlands, pp 31–63

    Chapter  Google Scholar 

  • Levy JA, Fraenkel-Conrat H, Owens RA (eds) (1994) Virology, 3rd edn. Prentice Hall, Englewood Cliffs, NJ, p 447

  • Llewellyn CA, Evans C, Airs RL, Cook I, Bale N, Wilson WH (2007) The response of carotenoids and chlorophylls during virus infection of Emiliania huxleyi (Prymnesiophyceae). J Exp Mar Biol Ecol 344:101–112

    Article  Google Scholar 

  • Lønborg C, Álvarez-Salgado XA (2012) Recycling versus export of bioavailable dissolved organic matter in the coastal ocean and efficiency of the continental shelf pump. Global Biogeochem Cycl. doi:10.1029/2012GB004353

    Google Scholar 

  • Lønborg C, Álvarez-Salgado XA, Davidson K, Miller AEJ (2009) Production of bioavailable and refractory dissolved organic matter by coastal heterotrophic microbial populations. Estuar Coast Shelf Sci 82:682–688

    Article  Google Scholar 

  • Lønborg C, Álvarez-Salgado XA, Davidson K, Martínez-García SE, Teira E (2010) Assessing the microbial bioavailability and degradation rate constants of dissolved organic matter by fluorescence spectroscopy in the coastal upwelling system of the Ría de Vigo. Mar Chem 119:121–129

    Article  Google Scholar 

  • Mari X, Rassoulzadegan F, Brussaard CPD, Wassmann P (2005) Dynamics of transparent exopolymeric particles (TEP) production by Phaeocystis globosa under N- or P-limitation: a controlling factor of the retention/export balance? Harmful algae 4:895–914

    Article  Google Scholar 

  • Middelboe M, Jørgensen NOG (2006) Viral lysis of bacteria: an important source of dissolved amino acids and cell wall compounds. J Mar Biol Ass 86:605–612

    Article  Google Scholar 

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

    Google Scholar 

  • Middelboe M, Riemann L, Steward GL, Hansen V, Nybroe O (2003) Virus-induced transfer of organic carbon between marine bacteria in a model community. Aquat Microb Ecol 33:1–10

    Article  Google Scholar 

  • Montagnes DJS, Berges JA, Harrison PJ, Taylor FJR (1994) Estimating carbon, nitrogen, protein, and chlorophyll a from cell volume in marine phytoplankton. Limnol Oceanogr 39:1044–1060

    Article  Google Scholar 

  • Myklestad SM (2000) Dissolved organic carbon from phytoplankton. In: Wangersky P (ed) The handbook of environmental chemistry. Marine chemistry part D, vol. 5. Springer, Berlin, pp 111–148

  • Nagata T (2000) Production mechanisms of dissolved organic carbon. In: Kirchman DL (ed) Microbial ecology of the oceans, vol 1. Wiley-Liss, New York, pp 121–153

    Google Scholar 

  • Nieto-Cid M, Álvarez-Salgado XA, Pérez FF (2006) Microbial and photochemical reactivity of fluorescent dissolved organic matter in a coastal upwelling system. Limnol Oceanogr 51:1391–1400

    Article  Google Scholar 

  • Noble RT, Fuhrman JA (1999) Breakdown and microbial uptake of marine viruses and other lysis products. Aquat Microb Ecol 20:1–11

    Article  Google Scholar 

  • Not F, Latasa M, Marie D, Cariou T, Vaulot D, Simon N (2004) A single species, Micromonas pusilla (Prasinophyceae), dominates the eukaryotic picoplankton in the Western English Channel. Appl Environ Microbiol 70:4064–4072

    Article  Google Scholar 

  • Pagarete A, Allen MJ, Wilson WH, Kimmance SA, de Vargas C (2009) Host–virus shift of the sphingolipid pathway along an Emiliania huxleyi bloom: survival of the fattest. Environ Microbiol 11:2840–2848

    Article  Google Scholar 

  • Passow U (2002) Transparent exopolymer particles (TEP) in aquatic environments. Prog Oceanogr 55:287–333

    Article  Google Scholar 

  • Passow U, Alldredge AL (1995) A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP). Limnol Oceanogr 40:1326–1335

    Article  Google Scholar 

  • Passow U, Alldredge AL, Logan BE (1994) The role of particulate carbohydrate exudates in the flocculation of diatom blooms. Deep-Sea Res I 41:335–357

    Article  Google Scholar 

  • Poorvin L, Rinta-Kanto JM, Hutchins DA, Wilhelm SW (2004) Viral release of Fe and its bioavailability to marine plankton. Limnol Oceanogr 49:1734–1741

    Article  Google Scholar 

  • Rochelle-Newall EJ, Fisher TR (2002) Production of chromophoric dissolved organic matter fluorescence in marine and estuarine environment: an investigation into the role of phytoplankton. Mar Chem 77:7–21

    Article  Google Scholar 

  • Romera-Castillo C, Sarmento H, Álvarez-Salgado XA, Gasol JM, Marrase C (2010) Production of chromophoric dissolved organic matter by marine phytoplankton. Limnol Oceanogr 55:446–454

    Article  Google Scholar 

  • Sheik AR (2012) Viral regulation on nutrient assimilation by algae and prokaryotes. PhD dissertation, University of Bremen, Germany

  • Sokal FF, Rohlf FJ (1995) Biometry. Freeman, New York

    Google Scholar 

  • Steinberg DK, Nelson NB, Carlson CA, Prusak AC (2004) Production of chromophoric dissolved organic matter (CDOM) in the open ocean by zooplankton and the colonial cyanobacterium Trichodesmium spp. Mar Ecol Prog Ser 267:45–56

    Article  Google Scholar 

  • Stoderegger KE, Herndl GJ (1999) Production of exopolymer particles by marine bacterioplankton under contrasting turbulence conditions. Mar Ecol Prog Ser 189:9–16

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Teira E, Martínez-Garcia S, Lønborg C, Álvarez-Salgado XA (2009) Growth rates of different phylogenetic bacterioplankton groups in a coastal upwelling system. Environ Microbiol Rep 1:545–554

    Article  Google Scholar 

  • Verdugo P, Alldredge AL, Azam F, Kirchman DL, Passow U, Santschi PH (2004) The oceanic gel phase: a bridge in the DOM–POM continuum. Mar Chem 92:67–85

    Article  Google Scholar 

  • Weinbauer MG, Peduzzi P (1995) Effect of virus-rich high molecular weight concentrates of seawater on the dynamics of dissolved amino acids and carbohydrates. Mar Ecol Prog Ser 127:245–253

    Article  Google Scholar 

  • Weinbauer MG, Chen F, Wilhelm SW (2010) Virus-mediated redistribution and partitioning of carbon in the global oceans. In: Jiao N, Azam F, Sanders S (eds) Microbial carbon pump in the ocean. Science AAA/S, Washington, DC, pp 54–56

    Google Scholar 

  • Weinbauer MG, Rowe JM, Wilhelm SW (2011) Determining rates of virus production in aquatic systems by the virus reduction approach. In: Wilhelm SW, Weinbauer MG, Suttle CA (eds) Manual of aquatic viral ecology. ASLO, Waco, pp 1–8

    Google Scholar 

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

    Article  Google Scholar 

  • Yamashita Y, Tanoue E (2003) Chemical characterization of protein-like fluorophores in DOM in relation to aromatic amino acids. Mar Chem 82:255–271

    Article  Google Scholar 

Download references

Acknowledgments

This study was funded by a Post Doc. fellowship to C. L from the Carlsberg Foundation and financial support by the Royal Netherlands Institute for Sea Research (NIOZ). M. M. was supported by The Danish Council for Independent Research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christian Lønborg.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lønborg, C., Middelboe, M. & Brussaard, C.P.D. Viral lysis of Micromonas pusilla: impacts on dissolved organic matter production and composition. Biogeochemistry 116, 231–240 (2013). https://doi.org/10.1007/s10533-013-9853-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-013-9853-1

Keywords

Navigation