References

Biogeosciences

1726-4189

Copernicus Publications

Göttingen, Germany

10.5194/bg-11-6841-2014

Enhanced viral production and virus-mediated mortality of bacterioplankton in a natural iron-fertilized bloom event above the Kerguelen Plateau

Malits

¹ ² Christaki

³ Obernosterer

⁴ ⁵ Weinbauer

M. G.

² ¹

Sorbonne Universités, UPMC Univ Paris 06, UMR7093, LOV, Observatoire océanographique, 06230, Villefranche/mer, France

CNRS, UMR7093, LOV, Observatoire océanographique, 06230, Villefranche/mer, France

INSU-CNRS, UMR8187 LOG, Laboratoire d'Océanologie et des Géosciences, Université du Littoral, ULCO, 32 avenue Foch, 62930 Wimereux, France

Sorbonne Universités, UPMC Univ Paris 06, UMR7621, LOMIC, Observatoire océanographique, 66650 Banyuls/mer, France

CNRS, UMR7621, LOMIC, Observatoire océanographique, 66650 Banyuls/mer, France

08 12 2014

11 23 6841 6853

2014

This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/

This article is available from https://bg.copernicus.org/articles/11/6841/2014/bg-11-6841-2014.html

The full text article is available as a PDF file from https://bg.copernicus.org/articles/11/6841/2014/bg-11-6841-2014.pdf

Above the Kerguelen Plateau in the Southern Ocean natural iron fertilization sustains a large phytoplankton bloom over 3 months during austral summer. During the KEOPS1 project (KErguelen Ocean and Plateau compared Study1) we sampled this phytoplankton bloom during its declining phase along with the surrounding high-nutrient–low-chlorophyll (HNLC) waters to study the effect of natural iron fertilization on the role of viruses in the microbial food web. Bacterial and viral abundances were 1.7 and 2.1 times, respectively, higher within the bloom than in HNLC waters. Viral production and virus-mediated mortality of bacterioplankton were 4.1 and 4.9 times, respectively, higher in the bloom, while the fraction of infected cells (FIC) and the fraction of lysogenic cells (FLC) showed no significant differences between environments. The present study suggests viruses to be more important for bacterial mortality within the bloom and dominate over grazing of heterotrophic nanoflagellates (HNFs) during the late bloom phase. As a consequence, at least at a late bloom stage, viral lysis shunts part of the photosynthetically fixed carbon in iron-fertilized regions into the dissolved organic matter (DOM) pool with potentially less particulate organic carbon transferred to larger members of the food web or exported.

References 1

Arrieta, J. M., Weinbauer, M. G., and Herndl, G. J.: Interspecific variability in sensitivity to uv radiation and subsequent recovery in selected isolates of marine bacteria, Appl. Environ. Microb., 66, 1468–1473, 2000.

Bergh, O., Børsheim, K. Y., Bratbak, G., and Heldal, M.: High abundance of viruses found in aquatic environments, Nature, 340, 467–468, 1989.

Biller, S. J., Schubotz, F., Roggensack, S. E., Thompson, A. W., Summons, R. E., and Chisholm, S. W.: Bacterial vesicles in marine ecosystems, Science, 343, 183–186, <a href="http://dx.doi.org/10.1126/science.1243457">https://doi.org/10.1126/science.1243457</a>, 2014.

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

Bird, D. F., Maranger, R., and Karl, D.: Palmer lter: Aquatic virus abundances near the antarctic peninsula, Antarct. J. US., 28, 234–235, 1993.

Blain, S., Queguiner, B., Armand, L., Belviso, S., Bombled, B., Bopp, L., Bowie, A., Brunet, C., Brussaard, C., Carlotti, F., Christaki, U., Corbiere, A., Durand, I., Ebersbach, F., Fuda, J. L., Garcia, N., Gerringa, L., Griffiths, B., Guigue, C., Guillerm, C., Jacquet, S., Jeandel, C., Laan, P., Lefevre, D., Lo Monaco, C., Malits, A., Mosseri, J., Obernosterer, I., Park, Y. H., Picheral, M., Pondaven, P., Remenyi, T., Sandroni, V., Sarthou, G., Savoye, N., Scouarnec, L., Souhaut, M., Thuiller, D., Timmermans, K., Trull, T., Uitz, J., van Beek, P., Veldhuis, M., Vincent, D., Viollier, E., Vong, L., and Wagener, T.: Effect of natural iron fertilization on carbon sequestration in the southern ocean, Nature, 446, 1070–1074, 2007.

Blain, S., Queguiner, B., and Trull, T.: The natural iron fertilization experiment keops (kerguelen ocean and plateau compared study): An overview, Deep-Sea Res. Pt.-II, 55, 559–565, 2008.

Bonilla-Findji, O., Malits, A., Lefevre, D., Rochelle-Newall, E., Lemee, R., Weinbauer, M. G., and Gattuso, J.-P.: Viral effects on bacterial respiration, production and growth efficiency: Consistent trends in the southern ocean and the mediterranean sea, Deep-Sea Res. Pt.-II, 55, 790–800, 2008.

Boras, J. A., Sala, M. M., Vazquez-Dominguez, E., Weinbauer, M. G., and Vaque, D.: Annual changes of bacterial mortality due to viruses and protists in an oligotrophic coastal environment (nw mediterranean), Environ. Microbiol., 11, 1181–1193, <a href="http://dx.doi.org/10.1111/j.1462-2920.2008.01849.x">https://doi.org/10.1111/j.1462-2920.2008.01849.x</a>, 2009.

Boras, J., Sala, M., Arrieta, J., Sà, E., Felipe, J., Agustí, S., Duarte, C., and Vaqué, D.: Effect of ice melting on bacterial carbon fluxes channelled by viruses and protists in the arctic ocean, Polar Biol., 33, 1695–1707, <a href="http://dx.doi.org/10.1007/s00300-010-0798-8">https://doi.org/10.1007/s00300-010-0798-8</a>, 2010.

Bratbak, G., Heldal, M., Thingstad, T. F., Riemann, B., and Haslund, O. H.: Incorporation of viruses into the budget of microbial c-transfer, A first approach, Mar. Ecol. Prog. Ser., 83, 273–280, 1992.

Brussaard, C. P. D.: Optimization of procedures for counting viruses by flow cytometry, Appl. Environ. Microbiol., 70, 1506–1513, 2004.

Brussaard, C. P. D., Wilhelm, S. W., Thingstad, F., Weinbauer, M. G., Bratbak, G., Heldal, M., Kimmance, S. A., Middelboe, M., Nagasaki, K., Paul, J. H., Schroeder, D. C., Suttle, C. A., Vaque, D., and Wommack, K. E.: Global-scale processes with a nanoscale drive: The role of marine viruses, Isme J., 2, 575–578, <a href="http://dx.doi.org/10.1038/ismej.2008.31">https://doi.org/10.1038/ismej.2008.31</a>, 2008a.

Brussaard, C. P. D., Timmermans, K. R., Uitz, J., and Veldhuis, M. J. W.: Virioplankton dynamics and virally induced phytoplankton lysis versus microzooplankton grazing southeast of the kerguelen (southern ocean), Deep-Sea Res. Pt.-II, 55, 752–765, 2008b.

Buesseler, K. O. and Boyd, P. W.: Climate change, Will ocean fertilization work?, Science, 300, 67–68, 2003.

Christaki, U., Obernosterer, I., Van Wambeke, F., Veldhuis, M., Garcia, N., and Catala, P.: Microbial food web structure in a naturally iron fertilized area in the southern ocean (kerguelen plateau), Deep-Sea Res. Pt.-II, 55, 706–719, 2008.

Christaki, U., Lefèvre, D., Georges, C., Colombet, J., Catala, P., Courties, C., Sime-Ngando, T., Blain, S., and Obernosterer, I.: Microbial food web dynamics during spring phytoplankton blooms in the naturally iron-fertilized Kerguelen area (Southern Ocean), Biogeosciences, 11, 6739–6753, <a href="http://dx.doi.org/10.5194/bg-11-6739-2014">https://doi.org/10.5194/bg-11-6739-2014</a>, 2014.

Daughney, C. J., Chatellier, X., Chan, A., Kenward, P., Fortin, D., Suttle, C. A., and Fowle, D. A.: Adsorption and precipitation of iron from seawater on a marine bacteriophage (pwh3a-p1), Mar. Chem., 91, 101–115, 2004.

de Baar, H. J. W., Boyd, P. W., Coale, K. H., Landry, M. R., Tsuda, A., ASSMY, P., Bakker, D. C. E., Bozec, Y., Barber, R. T., Brzezinski, M. A., Buesseler, K. O., Boye, M., Croot, P. L., Gervais, F., Gorbunov, M. Y., Harrison, P. J., Hiscock, M. R., Laan, P., Lancelot, C., Law, C. S., Levasseur, M., Marchetti, A., Millero, F. J., Nishioka, J., Nojiri, Y., van Oijen, T., Riebesell, U., Rijkenberg, M. J. A., Saito, H., Takeda, S., Timmermans, K. L., Veldhuis, M. J. W., Waite, A. M., and Wong, C. S.: Synthesis of iron fertilization experiments: From the iron age in the age of enlightenment, J. Geophys. Res., 110, C09S16, <a href="http://dx.doi.org/10.1029/2004JC002601">https://doi.org/10.1029/2004JC002601</a>, 2005.

Evans, C. and Brussaard, C. P. D.: Regional variation in lytic and lysogenic viral infection in the southern ocean and its contribution to biogeochemical cycling, Appl. Environ. Microbiol., 78, 6741–6748, <a href="http://dx.doi.org/10.1128/aem.01388-12">https://doi.org/10.1128/aem.01388-12</a>, 2012.

Evans, C., Pearce, I., and Brussaard, C. P. D.: Viral-mediated lysis of microbes and carbon release in the sub-antarctic and polar frontal zones of the australian southern ocean, Environ. Microbiol., 11, 2924–2934, 2009.

Fuhrman, J. A.: Marine viruses and their biogeochemical and ecological effects, Nature, 399, 541–548, 1999.

Fuhrman, J. A. and Noble, R. T.: Viruses and protists cause similar bacterial mortality in coastal seawater, Limnol. Oceanogr., 40, 1236–1242, 1995.

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

Gasol, J. M., Zweifel, U. L., Peters, F., Fuhrman, J. A., and Hagstrom, A.: Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria, Appl. Environ. Microb., 65, 4475–4483, 1999.

Gobler, C. J., Hutchins, D. A., Fisher, N. S., Cosper, E. M., and Sanudo-Wilhelmy, S. A.: Release and bioavailability of C, N, P, Se, and Fe following viral lysis of a marine chrysophyte, Limnol. Oceanogr., 42, 1492–1504, 1997.

Guixa-Boixereu, N., Vaqué , D., Gasol, J. M., Sánchez-Cámara, J., and Pedrós-Alió, C.: Viral distribution and activity in antarctic waters, Deep-Sea Res., 49, 827–845, 2002.

Helton, R. R., Cottrell, M. T., Kirchman, D. L., and Wommack, K. E.: Evaluation of incubation-based methods for estimating virioplankton production in estuaries, Aquat. Microb. Ecol., 41, 209–219, 2005.

Higgins, J. L., Kudo, I., Nishioka, J., Tsuda, A., and Wilhelm, S. W.: The response of the virus community to the seeds ii mesoscale iron fertilization, Deep-Sea Res. Pt.-II, 56, 2788–2795, 2009.

Jiao, N., Herndl, G. J., Hansell, D. A., Benner, R., Kattner, G., Wilhelm, S. W., Kirchman, D. L., Weinbauer, M., G., Luo, T., Chen, F., and Azam, F.: Microbial production of recalcitrant dissolved organic matter: Long-term carbon storage in the global ocean, Nat. Rev. Microbiol., 8, 593–599, 2010.

Kirchman, D. L.: Leucine incorporation as a measure of biomass production by heterotrophic bacteria, in: Handbook of methods in aquatic microbial ecology, edited by: Kemp, P. F., Sherr, B. F., Sherr, E. B., and Cole, J. J., Lewis Publishers, Boca Raton, FL, 509–512, 1993.

Kirchman, D. L.: Microbial ferrous wheel, Nature, 383, 303–304, 1996.

Manganelli, M., Malfatti, F., Samo, T. J., Mitchell, B. G., Wang, H., and Azam, F.: Major role of microbes in carbon fluxes during austral winter in the southern drake passage, PLoS ONE, 4, e6941, <a href="http://dx.doi.org/10.1371/journal.pone.0006941">https://doi.org/10.1371/journal.pone.0006941</a>, 2009.

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

Martin, J. H.: Glacial interglacial CO<sub>2</sub> change: The iron hypothesis, Paleoceanography, 5, 1–13, 1990.

Martin, J. H. and Fitzwater, S. E.: Iron deficiency limits phytoplankton growth in the north-east pacific subarctic, Nature, 331, 341–343, 1988.

Middelboe, M. and Lyck, P. G.: Regeneration of dissolved organic matter by viral lysis in marine microbial communities, Aquat. Microb. Ecol., 27, 187–194, 2002.

Middelboe, M., Jorgensen, N., and Kroer, N.: Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton, Appl. Environ. Microbiol., 62, 1991–1997, 1996.

Mioni, C. E., Poorvin, L., and Wilhelm, S. W.: Virus and siderophore-mediated transfer of available fe between heterotrophic bacteria: Characterization using an fe-specific bioreporter, Aquat. Microb. Ecol., 41, 233–245, 2005.

Mosseri, J., Quéguiner, B., Armand, L., and Cornet-Barthaux, V.: Impact of iron on silicon utilization by diatoms in the southern ocean: A case study of si/n cycle decoupling in a naturally iron-enriched area, Deep-Sea Res. Pt.-II, 55, 801–819, 2008.

Murray, A. G. and Jackson, A. G.: Viral dynamics: A model of the effects of size, shape, motion and abundance if single-celled planktonic organisms and other particles, Mar. Ecol. Prog. Ser., 89, 103–116, 1992.

Obernosterer, I., Christaki, U., Lefevre, D., Catala, P., Van Wambeke, F., and Lebaron, P.: Rapid bacterial mineralization of organic carbon produced during a phytoplankton bloom induced by natural iron fertilization in the southern ocean, Deep-Sea Res. Pt.-II, 55, 777–789, 2008.

Park, Y.-H., Roquet, F., Durand, I., and Fuda, J.-L.: Large-scale circulation over and around the northern kerguelen plateau, Deep-Sea Res. Pt.-II, 55, 566–581, <a href="http://dx.doi.org/10.1016/j.dsr2.2007.12.030">https://doi.org/10.1016/j.dsr2.2007.12.030</a>, 2008.

Paul, J. H.: Prophages in marine bacteria: Dangerous molecular time bombs or the key to survival in the seas?, Isme J., 2, 579–589, 2008.

Paul, J. H. and Weinbauer, M. G.: Detection of lysogeny in marine environments, in: Manual of Aquatic Virus Ecology, ASLO, edited by: Suttle, C. A., Wilhelm, S. W., and Weinbauer, M. G., 30-33, 2010.

Paul, J. H., Sullivan, M. B., Segall, A. M., and Rohwer, F.: Marine phage genomics, Comp. Biochem. Phys. B., 133, 463–476, 2002.

Payet, J. P. and Suttle, C. A.: Physical and biological correlates of virus dynamics in the southern beaufort sea and amundsen gulf, Sea ice and life in a river-influenced arctic shelf ecosystem, J. Mar. Syst., 74, 933–945, 2008.

Payet, J. P. and Suttle, C. A.: To kill or not to kill: The balance between lytic and lysogenic viral infection is driven by trophic status, Limnol. Oceanogr., 58, 465–474, 2013.

Poorvin, L., Rinta-Kanto, J. M., Hutchins, D. A., and Wilhelm, S. W.: Viral release of iron and its bioavailability to marine plankton, Limnol. Oceanogr., 49, 1734–1741, 2004.

Poorvin, L., Sander, S. G., Velasquez, I., Ibisanmi, E., LeCleir, G. R., and Wilhelm, S. W.: A comparison of fe bioavailability and binding of a catecholate siderophore with virus-mediated lysates from the marine bacterium vibrio alginolyticus pwh3a, J. Exp. Mar. Biol. Ecol., 399, 43–47, 2011.

Proctor, L. M. and Fuhrman, J. A.: Viral mortality of marine bacteria and cyanobacteria, Nature, 343, 60–62, 1990.

Rue, E. L. and Bruland, K. W.: The role of organic complexation on ambient iron chemistry in the equatorial pacific ocean and the response of a mesoscale iron addition experiment, Limnol. Oceanogr., 43, 901–910, 1997.

Sarthou, G., Vincent, D., Christaki, U., Obernosterer, I., Timmermans, K. R., and Brussaard, C. P. D.: The fate of biogenic iron during a phytoplankton bloom induced by natural fertilization: Impact of copepod grazing, Deep-Sea Res. Pt.-II, 55, 734–751, 2008.

Smetacek, V., Klaas, C., Strass, V. H., Assmy, P., Montresor, M., Cisewski, B., Savoye, N., Webb, A., d/'Ovidio, F., Arrieta, J. M., Bathmann, U., Bellerby, R., Berg, G. M., Croot, P., Gonzalez, S., Henjes, J., Herndl, G. J., Hoffmann, L. J., Leach, H., Losch, M., Mills, M. M., Neill, C., Peeken, I., Rottgers, R., Sachs, O., Sauter, E., Schmidt, M. M., Schwarz, J., Terbruggen, A., and Wolf-Gladrow, D.: Deep carbon export from a southern ocean iron-fertilized diatom bloom, Nature, 487, 313–319, 2012.

Smith, D. C. and Azam, F.: A simple, economical method for measuring bacterial protein synthesis rates in seawater using <sup>3</sup>h-leucine, Mar. Microb. Food Webs, 6, 107–114, 1992.

Smith, D. C., Steward, G. F., and Azam, F.: Virus and bacteria abundances in the drake passage during january and august 1991, Antarct. J. US., 27, 125–127, 1992.

Steward, G. F., Smith, D. C., and Azam, F.: Abundance and production of bacteria and viruses in the bering and chukchi seas, Mar. Ecol. Prog. Ser., 131, 287–300, 1996.

Street, J. H. and Paytan, A.: Iron, phytoplankton growth, and the carbon cycle, Met. Ions. Biol. Syst., 43, 153–193, 2005.

Strzepek, R. F., Maldonado, M. T., Higgins, J. L., Hall, J., Safi, K., Wilhelm, S. W., and Boyd, P.: Spinning the "ferrous wheel": The importance of the microbial community in an iron budget during the fecycle experiment, Global Biogeochem. Cy., 19, GB4S26, <a href="http://dx.doi.org/10.1029/2005GB002490">https://doi.org/10.1029/2005GB002490</a>, 2005.

Suttle, C. A.: Marine viruses-major players in the global ecosystem, Nat. Rev. Microbiol., 5, 801–812, 2007.

Suttle, C. A., Chan, A. M., and Cottrell, M. T.: Infection of phytoplankton by viruses and reduction of primary productivity, Nature, 347, 467–469, 1990.

Tortell, P. D., Maldonado, M. T., and Price, N. M.: The role of heterotrophic bacteria in iron-limited ocean ecosystems, Nature, 383, 330–332, 1996.

Uitz, J., Claustre, H., Griffiths, F. B., Ras, J., Garcia, N., and Sandroni, V.: A phytoplankton class-specific primary production model applied to the Kerguelen Islands region (Southern Ocean), Deep Sea Res. Pt.-I, 56, 541–560, 2009.

Van Heukelem, L. and Thomas, C. S.: Computer-assisted high-performance liquid chromatography method development with applications to the isolation and analysis of phytoplankton pigments, J. Chromatogr. A, 910, 31–49, 2001.

Weinbauer, M. G. and Suttle, C. A.: Potential significance of lysogeny to bacteriophage production and bacterial mortality in coastal waters of the gulf of mexico, Appl. Environ. Microbiol., 62, 4374–4380, 1996.

Weinbauer, M. G., Fuks, D., and Peduzzi, P.: Distribution of viruses and dissolved DNA along a coastal trophic gradient in the northern adriatic sea, Appl. Environ. Microbiol., 59, 4074–4082, 1993.

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

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

Weinbauer, M. G., Arrieta, J. M., Griebler, C., and Herndl, G. J.: Enhanced viral production and infection of bacterioplankton during an iron induced phytoplankton bloom in the southern ocean, Limnol. Oceanogr., 54, 774–784, 2009.

Weinbauer, M. G., Rowe, J. M., and Wilhelm, S. W.: Determining rates of virus production in aquatic systems by the virus reduction approach, in: Manual of Aquatic Virus Ecology, ASLO, edited by: Suttle, C. A., Wilhelm, S. W., and Weinbauer, M. G., 1–8, 2010.

Weinbauer, G., Chen, F., and Wilhelm, A. W.: Virus-mediated redistribution and partitioning of carbon in the global oceans, in: Microbial carbon pump, edited by: Jiao, N., Azam, F., and Sanders, S., Science/AAAS, Washington, DC, 54–56, 2011.

Wells, L. E. and Deming, J. W.: Significance of bacterivory and viral lysis in bottom waters of franklin bay, canadian arctic, during winter, Aquat. Microb. Ecol., 43, 209–221, 2006.

Wilhelm, S. W. and Suttle, C. A.: Virus and nutrient cycles in the sea, BioScience, 49, 781–787, 1999.

Wilhelm, S. W., Weinbauer, M. G., Suttle, C. A., and Jeffrey, W. H.: The role of sunlight in the removal and repair of viruses in the sea, Limnol. Oceanogr., 43, 586–592, 1998.

Wilhelm, S., Brigden, S., and Suttle, C.: A dilution technique for the direct measurement of viral production: A comparison in stratified and tidally mixed coastal waters, Microb. Ecol., 43, 168–173, 2002.

Williamson, S. J., Houchin, L. A., McDaniel, L., and Paul, J. H.: Seasonal variation in lysogeny as depicted by prophage induction in tampa bay, florida, Appl. Environ. Microbiol., 68, 4307–4314, 2002.

Wilson, W. H. and Mann, N. H.: Lysogenic and lytic viral production in marine microbial communities, Aquat. Microb. Ecol., 13, 95–100, 1997.

Winget, D. M., Williamson, K. E., Helton, R. R., and Wommack, K. E.: Tangential flow diafiltration: An improved technique for estimation of virioplankton production, Aquat. Microb. Ecol., 41, 221–232, 2005.