Skip to main content
Log in

Bacterial growth rate and the relative abundance of bacteria to heterotrophic nanoflagellates in the euphotic and disphotic layers in temperate coastal waters of Sagami Bay, Japan

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

Abstract

This study aimed to clarify the vertical differences in bacterial growth and grazing pressure on bacteria by heterotrophic nanoflagellates (HNF) and to identify the controlling factors of bacterial growth in temperate coastal waters of Sagami Bay, Japan. In addition to environmental factors, the annual monthly variations in bacterial growth rate (BGR) and the relative abundance of bacteria to HNF (BA/HNFA) were investigated in the euphotic and disphotic layers between May 2012 and May 2013. Significant vertical differences in BGR and BA/HNFA were evident between the two layers during the thermal stratification times of May to October 2012 and April to May 2013. BGR indicated significantly stronger limitation of bacterial growth in the euphotic layer compared to the disphotic layer. In contrast, significantly lower BA/HNFA was observed in the euphotic layer, suggesting significantly higher grazing pressure on bacteria by HNF. However, significant differences in BGR and BA/HNFA were not observed between the two layers from November 2012 to Match 2013, when the water column was well-mixed vertically due to the cooling and wind-induced mixing of surface water. This study indicates that bacteria in the euphotic layer grow less actively and are more vulnerable to predatory grazing by HNF relative to the disphotic layer during the stratification period. Further, multiple regression analyses indicate that bacterial growth was most controlled by the concentrations of chlorophyll a and dissolved organic carbon in the euphotic and disphotic layers, respectively.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aas P, Lyons MM, Pledger R, Mitchell DL, Jeffrey WH (1996) Inhibition of bacterial activities by solar radiation in nearshore waters and the Gulf of Mexico. Aquat Microb Ecol 11:229–238

    Article  Google Scholar 

  • Ara K, Hiromi J (2009) Seasonal variability in plankton food web structure and trophodynamics in the neritic area of Sagami Bay, Japan. J Oceanogr 65:757–779

    Article  Google Scholar 

  • Ara K, Yamaki K, Wada K, Fukuyama S, Okutsu T, Nagasaka S, Shiomoto A, Hiromi J (2011) Temporal variability in physicochemical properties, phytoplankton standing crop and primary production for 7 years (2002–2008) in the neritic area of Sagami Bay, Japan. J Oceanogr 67:87–111

    Article  Google Scholar 

  • Azam F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280:694–696

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Baek SH, Shimode S, Han MS, Kikuchi T (2008) Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: the role of nutrients. Harmful Algae 7:729–739

    Article  Google Scholar 

  • Baines SB, Pace ML (1991) The production of dissolved organic matter by phytoplankton and its importance to bacteria: patterns across marine and freshwater systems. Limnol Oceanogr 36:1078–1090

    Article  Google Scholar 

  • Baki MA, Motegi C, Shibata A, Fukuda H, Shimode S, Kikuchi T (2009) Temporal changes in chlorophyll a concentrations and bacterial, viral, and heterotrophic nanoflagellate abundances in the coastal zone of Sagami Bay, Japan: implications of top-down and bottom-up effects. Coast Mar Sci 33:29–38

    Google Scholar 

  • Bird DF, Kalff J (1984) Empirical relationships between bacterial abundance and chlorophyll concentration in fresh and marine waters. Can J Fish Aquat Sci 41:1015–1023

    Article  Google Scholar 

  • Bustillos-Guzmán J, Claustre H, Marty JC (1995) Specific phytoplankton signatures and their relationship to hydrographic conditions in the coastal northwestern Mediterranean Sea. Mar Ecol Prog Ser 124:247–258

    Article  Google Scholar 

  • Calbet A, Landry MR, Nunnery S (2001) Bacteria-flagellate interactions in the microbial food web of the oligotrophic subtropical North Pacific. Aquat Microb Ecol 23:283–292

    Article  Google Scholar 

  • Cole JJ, Findlay S, Pace ML (1988) Bacterial production in fresh and saltwater ecosystem: a cross-system overview. Mar Ecol Prog Ser 43:1–10

    Article  Google Scholar 

  • Ducklow HW (2000) Bacterial production and biomass in the oceans. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley, New York, pp 85–120

    Google Scholar 

  • Ducklow HW, Carlson CA (1992) Oceanic bacterial production. Adv Microb Ecol 12:113–181

    Article  Google Scholar 

  • Fukami K, Murata N, Morio Y, Nishijima T (1996) Distribution of heterotrophic nanoflagellates and their importance as the bacterial consumer in a eutrophic coastal seawater. J Oceanogr 52:399–407

    Article  Google Scholar 

  • Gasol JM (1994) A framework for the assessment of top-down vs. bottom-up control of heterotrophic nanoflagellate abundance. Mar Ecol Prog Ser 113:291–300

    Article  Google Scholar 

  • Gasol JM, Duarte CM (2000) Comparative analyses in aquatic microbial ecology: how far do they go? FEMS Microbiol Ecol 31:99–106

    Article  Google Scholar 

  • Gasol JM, del Giorgio PA, Duarte CM (1997) Biomass distribution in marine planktonic communities. Limnol Oceanogr 42:1353–1363

    Article  Google Scholar 

  • Hamasaki K (2006) Comparison of bromodeoxyuridine immunoassay with tritiated thymidine radioassay for measuring bacterial productivity in oceanic waters. J Oceanogr 62:793–799

    Article  Google Scholar 

  • Herndl GJ, Müller-Niklas G, Frick J (1993) Major role of ultraviolet-B in controlling bacterioplankton growth in the surface layer of the ocean. Nature 361:717–719

    Article  Google Scholar 

  • Hirano T (1969) Investigation of impact of river water withdrawal on fisheries. Agricultural Policy Planning Department, Japan, pp 9–13

    Google Scholar 

  • Hyun JH, Kim KH (2003) Bacterial abundance and production during the unique spring phytoplankton bloom in the central Yellow Sea. Mar Ecol Prog Ser 252:77–88

    Article  Google Scholar 

  • Japan Meteorological Agency (2014) Meteorological data acquisition system (AMeDAS). http://www.jma.go.jp/ Accessed 1 Mar 2014

  • Kanda J, Fujiwara S, Kitazato H, Okada Y (2003) Seasonal and annual variation in the primary production regime in the central part of Sagami Bay. Prog Oceanogr 57:17–29

    Article  Google Scholar 

  • Kirchman DL (2000) Uptake and regeneration of inorganic nutrients by marine heterotrophic bacteria. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley, New York, pp 261–288

    Google Scholar 

  • Kirchman DL, Rich JH (1997) Regulation of bacterial growth rates by dissolved organic carbon and temperature in the equatorial Pacific Ocean. Microb Ecol 33:11–20

    Article  Google Scholar 

  • Kirk JTO, Hargreaves BR, Morris DP, Coffin RB, David B, Fredrickson D, Karentz D, Lean DRS, Lesser MP, Madronich S, Morrow JH, Nelson NB, Scully NM (1994) Measurements of UV-B radiation in two freshwater lakes: an instrument intercomparison. Arch Hydrobiol Beih Ergebn Limnol 43:71–99

    Google Scholar 

  • Kobari T, Fujii T, Kobari Y, Habano A (2010) Seasonal variations in abundance, growth and mortality of heterotrophic bacteria in Kagoshima Bay. J Oceanogr 66:845–853

    Article  Google Scholar 

  • Kuwahara VS, Ogawa H, Toda T, Kikuchi T, Taguchi S (2000) Variability of bio-optical factors influencing the seasonal attenuation of ultraviolet radiation in temperate coastal waters of Japan. Photochem Photobiol 72:193–199

    Article  Google Scholar 

  • Kuwahara VS, Nozaki S, Nakano J, Toda T, Kikuchi T, Taguchi S (2015) 18-year variability of ultraviolet radiation penetration in the mid-latitude coastal waters of the western boundary Pacific. East Coast Shelf Sci 160:1–9

    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 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lekunberri I, Lefort T, Romera-Castillo C, Cardelús C, Coll-Lladó M, Ruiz-González C, Marrasé C, Gasol JM (2012) Relationship between induced phytoplankton blooms and the structure and dynamics of the free-living heterotrophic bacterial community. Mar Ecol Prog Ser 448:23–37

    Article  Google Scholar 

  • Lorenzo JI, Nieto-Cid M, Álvarez-Salgado XA, Pérez P, Beiras R (2007) Contrasting complexing capacity of dissolved organic matter produced during the onset, development and decay of a simulated bloom of the marine diatom Skeletonema costatum. Mar Chem 103:61–75

    Article  Google Scholar 

  • Marrasé C, Lim EL, Caron DA (1992) Seasonal and daily changes in bacterivory in a coastal plankton community. Mar Ecol Prog Ser 82:281–289

    Article  Google Scholar 

  • Naganuma T (1997) Abundance and production of bacterio plankton along a transect of Ise Bay, Japan. J Oceanogr 53:579–584

    Google Scholar 

  • Naganuma T, Miura S (1997) Abundance, production and viability of bacterioplankton in the Seto Inland Sea, Japan. J Oceanogr 53:435–442

    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

    Google Scholar 

  • Obernosterer I, Herndl GJ (1995) Phytoplankton extracellular release and bacterial growth: dependence on the inorganic N: P ratio. Mar Ecol Prog Ser 116:247–257

    Article  Google Scholar 

  • Opsahl S, Benner R (1997) Distribution and cycling of terrigenous dissolved organic matter in the ocean. Nature 386:480–482

    Article  Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford, p 173

    Google Scholar 

  • Pedrós-Alió C, Calderón-Paz JI, Gasol JM (2000) Comparative analysis shows that bacterivory, not viral lysis, controls the abundance of heterotrophic prokaryotic plankton. FEMS Microbiol Ecol 32:157–165

    Article  Google Scholar 

  • Peters F (1994) Prediction of planktonic protistan grazing rates. Limnol Oceanogr 39:195–206

    Article  Google Scholar 

  • Probyn TA (1987) Ammonium regeneration by microplankton in an upwelling environment. Mar Ecol Prog Ser 37:53–64

    Article  Google Scholar 

  • Robinson C (2008) Heterotrophic bacterial respiration. In: Kirchman DL (ed) Microbial ecology of the oceans, 2nd edn. Wiley, New York, pp 299–334

    Chapter  Google Scholar 

  • Rose JM, Caron DA (2007) Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold waters. Limnol Oceanogr 52:886–895

    Article  Google Scholar 

  • Servais P, Anzil A, Ventresque C (1989) Simple method for determination of biodegradable dissolved organic carbon in water. Appl Environ Microbiol 55:2732–2734

    Google Scholar 

  • Sherr BF, Sherr EB (1991) Proportional distribution of total numbers, biovolume and bacterivory among size classes of 2–20 µm nonpigmented marine flagellates. Mar Microb Food Webs 5:227–237

    Google Scholar 

  • Sherr EB, Caron DA, Sherr BF (1993) Staining of heterotrophic protists for visualization via epifluorescence microscopy. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis, London, pp 213–228

    Google Scholar 

  • Shiah FK, Ducklow HW (1994) Temperature regulation of heterotrophic bacterioplankton abundance, production, and specific growth rate in Chesapeake Bay. Limnol Oceanogr 39:1243–1258

    Article  Google Scholar 

  • Shiah FK, Gong GC, Chen TY, Chen CC (2000) Temperature dependence of bacterial specific growth rates on the continental shelf of the East China Sea and its potential application in estimating bacterial production. Aquat Microb Ecol 22:155–162

    Article  Google Scholar 

  • Shibata A, Goto Y, Saito H, Kikuchi T, Toda T, Taguchi S (2006) Comparison of SYBR Green I and SYBR Gold stains for enumerating bacteria and viruses by epifluorescence microscopy. Aquat Microb Ecol 43:223–231

    Article  Google Scholar 

  • Shimode S, Toda T, Kikuchi T (2006) Spatio-temporal changes in diversity and community structure of planktonic copepods in Sagami Bay, Japan. Mar Biol 148:581–597

    Article  Google Scholar 

  • Simon M, Cho BC, Azam F (1992) Significance of bacterial biomass in lakes and the ocean: comparison to phytoplankton biomass and biogeochemical implications. Mar Ecol Prog Ser 86:103–110

    Article  Google Scholar 

  • Šolić M, Krstulović N (1994) Role of predation in controlling bacterial and heterotrophic nanoflagellate standing stocks in the coastal Adriatic Sea: seasonal patterns. Mar Ecol Prog Ser 114:219–235

    Article  Google Scholar 

  • Šolić M, Krstulović N, Vilibić I, Bojanić N, Kušpilić G, Šestanović S, Šantić D, Ordulj M (2009) Variability in the bottom-up and top-down controls of bacteria on trophic and temporal scales in the middle Adriatic Sea. Aquat Microb Ecol 58:15–29

    Article  Google Scholar 

  • Sommaruga R, Obernosterer I, Herndl GJ, Psenner R (1997) Inhibitory effect of solar radiation on thymidine and leucine incorporation by freshwater and marine bacterioplankton. Appl Environ Microbiol 63:4178–4184

    Google Scholar 

  • Steward GF, Azam F (1999) Bromodeoxyuridine as an alternative to 3H-thymidine for measuring bacterial productivity in aquatic samples. Aquat Microb Ecol 19:57–66

    Article  Google Scholar 

  • Suzuki R, Ishimaru T (1990) An improved method for the determination of phytoplankton chlorophyll using N, N-dimethylformamide. J Oceanogr 46:190–194

    Google Scholar 

  • Tanaka T, Taniguchi A (1999) Predator-prey eddy in heterotrophic nanoflagellate-bacteria relationships in a bay on the northeastern Pacific coast of Japan. Mar Ecol Prog Ser 179:123–134

    Article  Google Scholar 

  • Tsai AY, Chiang KP, Chang J, Gong GC (2008) Seasonal variations in trophic dynamics of nanoflagellates and picoplankton in coastal waters of the western subtropical Pacific Ocean. Aquat Microb Ecol 51:263–274

    Article  Google Scholar 

  • Tupas L, Koike I (1991) Simultaneous uptake and regeneration of ammonium by mixed assemblages of heterotrophic marine bacteria. Mar Ecol Prog Ser 70:273–282

    Article  Google Scholar 

  • Tupas LM, Koike I, Karl DM, Holm-Hansen O (1994) Nitrogen metabolism by heterotrophic bacterial assemblages in Antarctic coastal waters. Polar Biol 14:195–204

    Article  Google Scholar 

  • Unrein F, Massana R, Alonso-Sáez L, Gasol JM (2007) Significant year-round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system. Limnol Oceanogr 52:456–469

    Article  Google Scholar 

  • Vaqué D, Gasol JM, Marrasé C (1994) Grazing rates on bacteria: the significance of methodology and ecological factors. Mar Ecol Prog Ser 109:263–274

    Article  Google Scholar 

  • Vázquez-Domínguez E, Vaqué D, Gasol JM (2012) Temperature effects on the heterotrophic bacteria, heterotrophic nanoflagellates, and microbial top predators of the NW Mediterranean. Aquat Microb Ecol 67:107–121

    Article  Google Scholar 

  • Weinbauer MG, Liu J, Motegi C, Maier C, Pedrotti ML, Dai M, Gattuso JP (2013) Seasonal variability of microbial respiration and bacterial and archaeal community composition in the upper twilight zone. Aquat Microb Ecol 71:99–115

    Article  Google Scholar 

  • Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992

    Article  Google Scholar 

  • Wikner J, Hagström Å (1988) Evidence for a tightly coupled nanoplanktonic predator-prey link regulating the bacterivores in marine environment. Mar Ecol Prog Ser 50:137–145

    Article  Google Scholar 

  • Williams PJLB (2000) Heterotrophic bacteria and the dynamics of dissolved organic material. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley, New York, pp 153–200

    Google Scholar 

  • Zöllner E, Hoppe HG, Sommer U, Jürgens K (2009) Effect of zooplankton-mediated trophic cascades on marine microbial food web components (bacteria, nanoflagellates, ciliates). Limnol Oceanogr 54:262–275

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to T. Kikuchi (Yokohama National University) for his support in field sampling. We also express our gratitude to K. Hamasaki (The University of Tokyo) and Y. Tada (Hokkaido University) for their support in sample analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Youta Sugai.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sugai, Y., Tsuchiya, K., Kuwahara, V.S. et al. Bacterial growth rate and the relative abundance of bacteria to heterotrophic nanoflagellates in the euphotic and disphotic layers in temperate coastal waters of Sagami Bay, Japan. J Oceanogr 72, 577–587 (2016). https://doi.org/10.1007/s10872-016-0352-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10872-016-0352-6

Keywords

Navigation