Skip to main content

Advertisement

SpringerLink
Log in

Significant contribution of lytic mortality to bacterial production and DOC cycles in Funka Bay, Japan

  • Original Article
  • Published:
Journal of Oceanography Aims and scope Submit manuscript

Abstract

A modified dilution experiment was conducted to evaluate the relative contribution of viral lysis and protozoan grazing to the mortalities of heterotrophic bacteria in Funka Bay, a subarctic coastal bay. The experiment included the stepwise dilution of the original seawater with virus-free seawater (10 kDa ultrafiltered) to change the encounter rate of both virus and protozoa to heterotrophic bacteria, incubation for 48 h and monitoring the change in the abundance of heterotrophic bacteria. In a parallel experiment, the original seawater was replaced by 1.0 µm fractionated seawater to eliminate protozoa, and the same dilution was conducted with the virus-free seawater to estimate only lytic mortality. The viral lysis and protozoan grazing rates in the surface water ranged from 0.40 to 1.19 and 0.08 to 0.27 days−1, respectively. Viral lysis was the main cause for the bacterial mortality (79.8 ± 3.2 %). The net (in situ) growth rate of heterotrophic bacteria was about 0.15 days−1. In the bottom water (90 m), both mortalities were lower than those at the surface and the net growth rate was mostly a negative value. The contribution of released dissolved organic matter (DOM) through lysis to the bacterial carbon demand (BCD) was evaluated. The lysed bacterial cells might release DOM to the ambient environment, in which bacterial organic matter is recycled in the subsequent bacterial production. The potential contribution was estimated to range from 25 to 27 % in the surface water and to be 31 % in the bottom water, suggesting that the lytic mortality significantly fueled DOM to the subsequent bacterial production.

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

  • Almeida MA, Cunha MA, Alcântara F (2001) Loss of estuarine bacteria by viral infection and predation in microcosm conditions. Microb Ecol 42:562–571

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ban S (2000) Grazing and microbial food chains during diatom blooming and post-diatom-blooming period. Bull Coast Oceanogr 38:23–28 (in Japanese with English abstract)

    Google Scholar 

  • Berninger UG, Finlay BJ, Kuuppo-Leinikki P (1991) Protozoan control of bacterial abundances in freshwater. Limnol Oceanogr 36:139–147

    Article  Google Scholar 

  • Boras JA, Sala MM, Vázquez-Dominuez E, Weinbauer MG, Vaqué D (2009) Annual changes of bacterial mortality due to viruses and protists in an oligotrophic coastal environment (NW Mediterranean). Environ Microbiol 11:1181–1193

    Article  Google Scholar 

  • Bratbak G, Egge JK, Heldal M (1993) Viral mortality of the marine alga Emiliana huxleyi (Haptophyceae) and termination of algal blooms. Mar Ecol Prog Ser 93:39–48

    Article  Google Scholar 

  • Carlson CA, Ducklow HW (1995) Dissolved organic carbon in the upper ocean of the central equatorial Pacific Ocean. Deep Sea Res 42:639–656

    Article  Google Scholar 

  • Cauwet G (1999) Determination of dissolved organic carbon and nitrogen by high temperature combustion. In: Grasshoff K, Kremling K, Ehrhardt M (eds) Methods of seawater analysis, 3rd edn. Wiley-VCH, Weinheim, pp 407–420

    Chapter  Google Scholar 

  • Chen F, Lu J, Binder BJ, Liu Y, Hodson RE (2001) Application of digital image analysis and flow cytometry to enumerate marine viruses stained with SYBR Gold. Appl Environ Microb 68:539–545

    Article  Google Scholar 

  • Cochlan WP, Winlner J, Steward GF, Smith DC, Azam F (1993) Spatial distribution of viruses, bacteria and chlorophyll a in neritic, oceanic and estuarine environments. Mar Ecol Prog Ser 92:77–97

    Article  Google Scholar 

  • Copping AE, Lorenzen CJ (1980) Carbon budget of a marine phytoplankton-herbivore system with carbon-14 as a tracer. Limnol Oceanogr 25:873–883

    Article  Google Scholar 

  • Cully AI, Welschmeyer NA (2002) The abundance, distribution, and correlation of viruses, phytoplankton, and prokaryotes along a Pacific Ocean transect. Limnol Oceanogr 47:1508–1513

    Article  Google Scholar 

  • Dagg MJ (1993) Grazing by the copepod community does not control phytoplankton production in the subarctic Pacific Ocean. Prog Oceanogr 32:163–183

    Article  Google Scholar 

  • del Giorgio PA, Cole JJ (2000) Bacterial energetics and growth efficiency. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, New York, pp 289–326

    Google Scholar 

  • Felip M, Pace ML, Cole JJ (1996) Regulation of planktonic bacterial growth rates: the effects of temperature and resources. Microb Ecol 31:15–28

    Article  Google Scholar 

  • Fuhrman JA (2000) Impact of viruses on bacterial processes. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, New York, pp 327–350

  • Fuhrman JA, Noble RT (1995) Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol Oceanogr 40:1238–1242

    Article  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

    Google Scholar 

  • Gobler CJ, Hutchins DA, Fisher NS, Cosper EM, Sañudo-Wilhelmy SA (1997) Release and bioavailability of C, N, P, Se, and Fe following viral lysis of marine chrysophyte. Limnol Oceanogr 42:1492–1504

    Article  Google Scholar 

  • Guixa-Boixereu N, Lysnes K, Pedrós-Alió C (1999) Viral lysis and bacterivory during a phytoplankton bloom in a coastal water microcosm. Appl Environ Microbiol 65:1949–1958

    Google Scholar 

  • Kudo I, Matsunaga K (1999) Environmental factors affecting the occurrence and production of the spring phytoplankton bloom in Funka Bay, Japan. J Oceanogr 55:505–513

    Article  Google Scholar 

  • Kudo I, Yoshimura T, Yanada M, Matsunaga K (2000) Exhaustion of nitrate terminates a phytoplankton bloom in Funka Bay, Japan: change in SiO4:NO3 consumption rate during the bloom. Mar Ecol Prog Ser 193:45–51

    Article  Google Scholar 

  • Kudo I, Yoshimura T, Lee C-W, Yanada M, Maita Y (2007) Nutrient regeneration at bottom after a massive spring bloom in a subarctic coastal environment, Funka Bay, Japan. J Oceanogr 63:791–801

    Article  Google Scholar 

  • Kudo I, Noiri Y, Cochlan WP, Suzuki K, Aramaki T, Ono T, Nojiri Y (2009) Primary productivity, bacterial productivity and nitrogen uptake in response to iron enrichment during the SEEDS II. Deep Sea Res II 56:2755–2766

    Article  Google Scholar 

  • Kudo I, Hisatoku T, Yoshimura T, Maita Y (2015) Primary productivity and nitrogen assimilation with identifying the contribution of urea in Funka Bay, Japan. Estuar Coast Shelf Sci 158:12–19

    Article  Google Scholar 

  • Lancelot C (1983) Factors affecting phytoplankton extracellular release in the Southern Bight of the North Sea. Mar Ecol Prog Ser 12:115–121

    Article  Google Scholar 

  • Landry MR, Hassett RP (1982) Estimating the grazing impact of marine microzooplankton. Mar Biol 67:283–288

    Article  Google Scholar 

  • Larsson U, Hangström Å (1982) Fractionated phytoplankton primary production, exudate release and bacterial procution in a Baltic eutrophication gradient. Mar Biol 67:57–70

    Article  Google Scholar 

  • Lee C-W, Kudo I, Yanada M, Maita Y (2001a) Bacterial abundance and production and heterotrophic nanoflagellate abundance in a subarctic coastal water (Western North Pacific Ocean). Aquat Microb Ecol 23:263–271

    Article  Google Scholar 

  • Lee C-W, Kudo I, Yanada M, Maita Y (2001b) Bacterial abundance and production and their relation to primary production in Funka Bay. Plankton Biol Ecol 48:1–9

    Google Scholar 

  • Martinussen I, Thingstad TF (1991) A simple dual staining technique for simultaneous quantification of auto- and heterotrophic nano- and pico-plankton. Mar Microb Food Webs 5:5–11

    Google Scholar 

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

    Google Scholar 

  • Miyake H, Yanada M, Nishi T, Hoshizawa K (1998) Short-time variation in low tropic level productivity and hydrographic conditions in Funka Bay. Mem Fac Fish Hokkaido Univ 45:36–41

    Google Scholar 

  • Nagata T (2000) Production mechanisms of dissolved organic matter. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, New York, pp 121–152

  • Noble RT, Fuhrman JA (1998) Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14:113–118

    Article  Google Scholar 

  • Odate T, Maita M (1988) Seasonal changes in the biomass of zooplankton and their food requirement in Funka Bay. J Oceanogr Soc Japan 44:228–234

    Article  Google Scholar 

  • Ohtani K (1971) Studies on the change of the hydrographic conditions in the Funka Bay II. Characteristics of the water occupying the Funka Bay. Bull Fac Fish Hokkaido Univ 22:58–66 (in Japanese with English abstract)

    Google Scholar 

  • Pace ML (1988) Bacterial mortality and the fate of bacterial production. Hydrobiologia 159:41–49

    Article  Google Scholar 

  • Proctor LM, Fuhrman JA (1991) Roles of viral infection in organic particle flux. Mar Ecol Prog Ser 69:133–142

    Article  Google Scholar 

  • Sanders RW, Caron DA, Berninger UG (1992) Relationships between bacteria and heterotrophic nanoplankton in marine and fresh waters: an inter-ecosystem comparison. Mar Ecol Prog Ser 86:1–14

    Article  Google Scholar 

  • Sherr EB, Sherr BF (1984) Role of heterotrophic protozoa in carbon and energy flow in aquatic ecosystems. In: Klug MJ, Reddy CA (eds) Current perspectives in microbial ecology. Am Soc for Microbiol, Washington, DC, pp 412–423

    Google Scholar 

  • Shimada H (2000) Seasonal changes of phytoplankton species composition in Funka Bay. Bull Coast Oceanogr 38:15–22 (in Japanese with English abstract)

    Google Scholar 

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

    Article  Google Scholar 

  • Strom SL, Benner R, Ziegler S, Dagg MJ (1997) Planktonic grazers are a potentially important source of marine dissolved organic carbon. Limnol Oceeanogr 42:1364–1374

    Article  Google Scholar 

  • Suzuki R, lshimaru T (1990) An improved method for the determination of Phytoplankton chlorophyll using N, N-dimethylformamide. J Oceanogr Soc Japan 46:180–184

    Article  Google Scholar 

  • Taira Y, Uchimiya M, Kudo I (2009) Virus dilution for simultaneously estimating viral lysis and protozoan grazing on bacterial mortality. Mar Ecol Prog Ser 379:23–32

    Article  Google Scholar 

  • Tremaine SC, Mills AL (1987) Tests of the critical assumptions of the dilution method for estimating bacterivory by microeucaryotes. Appl Environ Microbiol 53:2914–2921

    Google Scholar 

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

    Article  Google Scholar 

  • Weinbauer MG, Höfle MG (1998) Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake. Appl Environ Microbiol 64:431–438

    Google Scholar 

  • Weinbauer MG, Rassoulzadegan F (2004) Are viruses driving microbial diversification and diversity? Environ Microbiol 6:1–11

    Article  Google Scholar 

  • Weinbauer MG, Suttle CA (1997) Comparison of epifluorescence and transmission electron microscopy for counting viruses in natural marine waters. Aquat Microb Ecol 13:225–232

    Article  Google Scholar 

  • White JR, Roman MR (1992) Seasonal study of grazing by metazoan zooplankton in the mesohaline Chesapeake Bay. Mar Ecol Prog Ser 86:251–261

    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 43:168–173

    Article  Google Scholar 

  • Williams PM, Druffel ERM (1987) Radiocarbon in dissolved organic matter in the central North Pacific Ocean. Nature 330:246–248

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Captain, officers and crew of the T/S Ushio Maru for their helpful assistance. We are also grateful to Dr. M. Uchimiya for technical instruction for the study.

Author information

Authors and Affiliations

  1. Graduate School of Environmental Science, Hokkaido University, Sapporo, 060-0810, Japan

    Kakuta Eri & Isao Kudo

  2. Faculty of Fisheries Sciences, Hokkaido University, Hakodate, 042-8611, Japan

    Isao Kudo

Authors
  1. Kakuta Eri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isao Kudo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isao Kudo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eri, K., Kudo, I. Significant contribution of lytic mortality to bacterial production and DOC cycles in Funka Bay, Japan. J Oceanogr 72, 177–187 (2016). https://doi.org/10.1007/s10872-015-0316-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10872-015-0316-2

Keywords

Search

Navigation