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Regulation of bacterial assemblages in oligotrophic plankton systems: results from experimental and empirical approaches

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Abstract

Bacteria are relevant members of planktonic food webs, both in terms of biomass and production share. The assessment and comprehension of the factors that control bacterial abundance and production are, thus, necessary to understand how carbon and nutrients circulate in planktonic food webs. It is commonly believed that bacterial abundance, activity and production are either determined by the available nutrient levels (‘bottom-up’ control) or by the effect of predators (‘top-down’). These factors have also been shown to regulate the internal structure (the physiological and phylogenetic structure) of the bacterioplankton black box. We present here different empirical and experimental ways in which the factors that control bacterial communities are assessed, among them, the direct comparison of the rates of bacterial growth and losses to grazing. Application of several of these methods to open ocean data suggests that bacteria are regulated by resources at the largest scales of analysis, but that this overall regulation is strongly modulated by predators in all types of systems. In the most oligotrophic environments, bacterial abundance and growth are regulated by predators, while in the richest environments it is bacterial (phylogenetic, size, activity) community composition that is most affected by protist predators, while abundance can be influenced by metazoans. Because changes in bacterial community composition require that bacteria have enough nutrient supply, the overall effect of these regulations is that bacterial growth appears to be top-down regulated in the most nutrient-poor environments and bottom-up regulated in the richer ones.

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References

  • Andersen P & Fenchel T (1985) Bacterivory by microheterotrophic flagellates in seawater samples. Limnol. Oceanogr. 30: 198–202

    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

    Google Scholar 

  • Bedo AW, Acuña JL, Robins D & Harris, RP (1993) Grazing in the micron and submicron particle size range: The case of Oikopleura dioica (appendicularia). Bull. Mar. Sci. 53: 2–14

    Google Scholar 

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

    Google Scholar 

  • Biddanda B, Ogdahl M & Cotner J (2001) Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol. Oceanogr. 46: 730–739

    Article  Google Scholar 

  • Billen G, Servais P & Becquevort S (1990) Dynamics of bacterioplankton in oligotrophic and eutrophic aquatic environments: bottom-up or top-down control? Hydrobiologia 207: 37–42

    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

    Google Scholar 

  • Carlson CA, Ducklow HW & Sleeter TD (1996) Stocks and dynamics of bacterioplankton in the northwestern Sargasso Sea. Deep-Sea Res. 43: 491–515

    Article  CAS  Google Scholar 

  • Caron DA, Peele ER, Lim EL & Dennet MR (1999) Picoplankton and nanoplankton and their trophic coupling in surface waters of the Sargasso Sea south of Bermuda. Limnol. Oceanogr. 44: 259–272

    Google Scholar 

  • Cochlan, WP (2001) The heterotrophic bacterial response during a mesoscale iron enrichment experiment (IronEx II) in the eastern equatorial Pacific Ocean. Limnol. Oceanogr. 46: 428–435

    Article  CAS  Google Scholar 

  • Coffin RB & Sharp JH (1987) Microbial trophodynamics in the Delaware Estuary. Mar. Ecol. Prog. Ser. 41: 253–266

    Google Scholar 

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

    Google Scholar 

  • Cole JJ, Pace ML, Carpenter SR & Kitchell JF (2000) Persistence of net heterotrophy in lakes during nutrient addition and food web manipulations. Limnol. Oceanogr. 45: 1718–1730

    Article  Google Scholar 

  • Cho CC, Na SC & Choi DH (2000) Active ingestion of fluorescently labeled bacteria by mesopelagic heterotrophic nanoflagellates in the East Sea, Korea. Mar. Ecol. Prog. Ser. 206: 23–32

    Google Scholar 

  • Christaki U, van Wambeke F & Dolan JR (1999) Nanoflagellates (mixotrophs, heterotrophs and autotrophs) in the oligotrophic eastern Mediterranean: standing stocks, bacterivory and relationships with bacterial production. Mar. Ecol. Prog. Ser. 181: 297–307

    Google Scholar 

  • Church MJ, Hutchins DA & Ducklow HW(2000) Limitation of bacterial growth by dissolved organic matter and iron in the Southern Ocean. Appl. Environ. Microbiol. 66: 455–466

    Article  PubMed  CAS  Google Scholar 

  • del Giorgio PA & Gasol JM (1995) Biomass distribution in freshwater plankton communities. Am. Nat. 146: 135–152

    Article  Google Scholar 

  • del Giorgio PA, Gasol JM, Vaqué D, Mura P, Agustí S & Duarte CM (1996) Bacterioplankton community structure: Protists control net production and the proportion of active bacteria in a coastal marine community. Limnol. Oceanogr. 41: 1169–1179

    Article  Google Scholar 

  • del Giorgio PA, Cole JJ, & Cimbleris A (1997) Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385: 148–151

    Article  CAS  Google Scholar 

  • Ducklow HW (1992) Factors regulating bottom-up control of bacteria biomass in open ocean plankton communities. Arch. Hydrobiol. Beih. Ergebn. Limnol. 37: 207–217

    Google Scholar 

  • Ducklow HW (1999) The bacterial component of the oceanic euphotic zone. FEMS Microb. Ecol. 30: 1–10

    Article  CAS  Google Scholar 

  • Ducklow HW, Kirchman DL, Quinby HL, Carlson CA & Dam HG (1993) Stocks and dynamics of bacterioplankton carbon during the spring bloom in the eastern North Atlantic Ocean. Deep-Sea Res 40: 245–263

    Article  Google Scholar 

  • Dufour P & Torréton J-P (1996) Bottom-up and top-down control of bacterioplankton from eutrophic to oligotrophic sites in the tropical northeastern Atlantic Ocean. Deep-Sea Res. 43: 1305–1320

    Article  CAS  Google Scholar 

  • Eriksson C & Pedrós-Alió C (1990) Selenium as a nutrient for freshwater bacterioplankton and its interactions with phosphorus. Can. J. Microbiol. 36: 475–483

    CAS  Google Scholar 

  • Fasham MJR, Boyd PW & Savidge G (1999) Modeling the relative contributions of autotrophs and heterotrophs to carbon flow at a Lagrangian JGOFS station in the Northeast Atlantic: The importance of DOC. Limnol. Oceanogr. 44: 80–94

    Google Scholar 

  • Fenchel T (1982) Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and importance as bacterial consumers. Mar. Ecol. Prog. Ser. 9: 35–42

    Google Scholar 

  • Fenchel T (1986) The ecology of heterotrophic microflagellates. Adv. Microb. Ecol. 9: 57–97

    Google Scholar 

  • Furhman JA & Noble RT (1995) Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol. Oceanogr. 40: 1236–1242

    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

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gasol JM & Morán XAG (1999) Effects of filtration on bacterial activity and picoplankton community structure as assessed by flow cytometry. Aquat. Microb. Ecol. 16: 251–264

    Google Scholar 

  • Gasol JM & Vaqué D (1993) Lack of coupling between heterotrophic nanoflagellates and bacteria: a general phenomenon across aquatic systems? Limnol. Oceanogr. 38: 657–665

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gasol JM, Zweifel U-L, Peters F, Fuhrman JA & Hagström Å (1999) Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria. Appl. Environ. Microbiol. 65: 4475–4483

    PubMed  CAS  Google Scholar 

  • Gasol JM, Šimek K, Kojecká P, Comerma M, García J-C, Casamayor EO & Armengol J (2002) A transplant experiment to identify the factors controlling bacterial abundance, activity, production and community composition in a eutrophic canyon-shaped reservoir. Limnol. Oceanogr. 47: 62–77

    Article  CAS  Google Scholar 

  • Gili JM & Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Trends Ecol. Evol. 13: 316–320

    Article  Google Scholar 

  • Guixa-Boixereu N, Vaqué D, Gasol JM & Pedrós-Alió C (1999) Distribution of viruses and their potential effect on bacterioplankton in an oligotrophic marine system. Aquat. Microb. Ecol. 19: 205–213

    Google Scholar 

  • Guixa-Boixereu N, Vaqué D, Gasol JM, Sánchez-Cámara J & Pedrós-Alió C (2002) Viral distribution and activity in Antarctic waters. Deep-Sea Res. II 49: 827–845

    Article  Google Scholar 

  • Hahn MW & Höfle MG (2001) Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microb. Ecol. 35: 113–121

    Article  CAS  Google Scholar 

  • Herndl GJ, Kaltenböck E & Müller-Niklas G (1993) Dialysis bag incubation as a nonradiolabeling technique to estimate bacterioplankton productionin situ. In: Kemp PF, Sherr BF, Sherr EB & Cole JJ (Eds) Handbook of Methods in Aquatic Microbial Ecology (pp 553–556). Lewis Publishers, Boca Raton, FL.

    Google Scholar 

  • Jürgens K (1994) Impact of Daphnia on planktonic microbial food webs - a review. Mar. Microb. Food Webs. 8: 295–324

    Google Scholar 

  • Jürgens K, Pernthaler J, Schalla S & Amann R (1999) Morphological and compositional changes in a planktonic bacterial community in response to enhanced protozoan grazing. Appl. Environ. Microbiol. 65: 1241–1250

    PubMed  Google Scholar 

  • Jürgens K & Güde H (1994) The potential importance of grazingresistant bacteria in planktonic systems. Mar. Ecol. Prog. Ser. 112: 169–188

    Google Scholar 

  • Jürgens K, Gasol JM & Vaqué (2000) Bacteria-flagellate coupling in microcosm experiments in the Central Atlantic Ocean. J. Exp. Mar. Biol. Ecol. 245: 127–147

    Article  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  PubMed  Google Scholar 

  • Kirchman DL, Meon B, Cottrell MT, Hutchins DA, Weeks D & Bruland KW (2000) Carbon versus iron limitation of bacterial growth in the California upwelling regime. Limnol. Oceanogr. 45: 1681–1688

    Google Scholar 

  • Kuuppo-Leinikki P (1990) Protozoan grazing on planktonic bacteria and its impact on bacterial population. Mar. Ecol. Prog. Ser. 63: 227–238

    Google Scholar 

  • Landry MR (1994) Methods and controls for measuring the grazing impact of planktonic protist. Mar. Microb. Food Webs. 8: 37–57

    Google Scholar 

  • Landry MR, Haas LW & Fagerness VL (1984) Dynamics of microbial plankton communities: experiments in Kaneohe Bay, Hawaii. Mar. Ecol. Prog. Ser. 16: 127–133

    CAS  Google Scholar 

  • Lebaron P, Servais P, Agogué H, Courties C & Joux F (2001) Does the high nucleic acid content of individual bacterial cells allow us to discriminate between active cells and inactive cells in aquatic systems? Appl. Environ. Microbiol. 67: 1775–1782

    Article  PubMed  CAS  Google Scholar 

  • Li WKW, Dickie PM, Harrison WG & Irwin BD (1993) Biomass and production of bacteria and phytoplankton during the spring bloom in the western North Atlantic Ocean. Deep-Sea Res. 40: 307–327

    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

    Google Scholar 

  • Massana R, Pedrós-Alió C, Casamayor EO & Gasol JM (2001) Changes in marine bacterioplankton phylogenetic composition during incubations designed to measure biogeochemically significant parameters. Limnol. Oceanogr. 46: 1181–1188

    Article  Google Scholar 

  • McManus GB & Fuhrman JA (1988) Control of marine bacterioplankton populations: measurement and significance of grazing. Hydrobiologia 159: 51–62

    Google Scholar 

  • Newell SY, Sherr BF, Sherr EB & Fallon RD (1983) Bacterial response to presence of eukaryote inhibitors in water from a coastal marine environment. Mar. Environ. Res. 10: 147–157

    Article  Google Scholar 

  • Pace ML & Cole JJ (1994) Comparative and experimental approaches to top-down and bottom-up regulation of bacteria. Microb. Ecol. 28: 181–193

    Article  Google Scholar 

  • Pace ML & Cole JJ (1996) Regulation of bacteria by resources and predation tested in whole-lake experiments. Limnol. Oceanogr. 41: 1448–1460

    CAS  Google Scholar 

  • Pakulski JD, Coffin RB, Kelley CA, Holder SL, Downer R, Aas P, Lyons MM & Jeffrey WH (1996) Iron stimulation of Antarctic bacteria. Nature 383: 133–134

    Article  CAS  Google Scholar 

  • Pedrós-Alió C, Calderón-Paz JI, Guixa-Boixereu N, Estrada M & Gasol JM (1999) Bacterioplankton and phytoplankton biomass and production during summer stratification in the northwestern Mediterranean Sea. Deep-Sea Res. I 46: 985–1019

    Article  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 Microb. Ecol. 32: 157–165

    Google Scholar 

  • Pernthaler J, Posch T, Šimek K, Vrba J, Amann R & Psenner R (1997) Contrasting bacterial strategies to coexist with a flagellate predator in an experimental microbial assemblage. Appl. Environ. Microbiol. 63: 596–601

    PubMed  CAS  Google Scholar 

  • Posch, T, Loferer-Krößbacher M, Gao G, Alfreider A, Pernthaler J & Psenner R (2001) Precision of bacterioplankton biomass determination: a comparison of two fluorescent dyes, and of allometric and linear volume-to-carbon conversion factors. Aquat. Microb. Ecol. 25: 55–64

    Google Scholar 

  • Prairie Y T & Bird DF (1989) Some misconceptions about the spurious correlation problem in the ecological literature. Oecologia 81: 285–288

    Google Scholar 

  • Psenner R & Sommaruga R (1992) Are rapid changes in bacterial biomass caused by shifts from top-down to bottom-up control? Limnol. Oceanogr. 37: 1092–1100

    Article  Google Scholar 

  • Safi KA & Hall JA (1999) Mixotrophic and heterotrophic nanoflagellate grazing in the convergence zone east of New Zealand. Aquat. Microb. Ecol. 20: 83–93

    Google Scholar 

  • Sanders RW, Porter KG, Bennett SJ & DeBiase AE (1989) Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol. Oceanogr. 34: 673–687

    Google Scholar 

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

    Google Scholar 

  • Sanders RW, Berninger U-G, Lim EL, Kemp PF & Caron DA (2000) Heterotrophic and mixotrophic nanoplankton predation on picoplankton in the Sargasso Sea and on Georges Bank. Mar. Ecol. Prog. Ser. 192: 103–118

    Google Scholar 

  • Sherr EB & Sherr BF (1987) High rates of consumption of bacteria by pelagic ciliates. Nature 325: 710–711

    Article  Google Scholar 

  • Sherr BF, Sherr EB & Hopkinson CS (1988) Trophic interactions within pelagic microbial communities: indications of feedback regulation of carbon flow. Hydrobiologia 159: 19–26

    Google Scholar 

  • Sherr BF, Sherr EB & Pedrós-Alió C (1989) Simultaneous measurement of bacterioplankton production and protozoan bacterivory in estuarine water. Mar. Ecol. Prog. Ser. 54: 209–219

    Google Scholar 

  • Sherr EB, Sherr BF & Fessender L (1997) Heterotrophic protists in the Central Arctic Ocean. Deep-Sea Res. II 44: 1665–1682

    Article  CAS  Google Scholar 

  • Shiah F-K, Kao SJ & Liu KK (1998) Bacterial production in the Western Equatorial Pacific: Implications of inorganic nutrient effects on dissolved organic carbon accumulation and consumption. Bull. Mar. Sci. 62: 795–808

    Google Scholar 

  • Šimek K, Kojecká P, Nedoma J, Hartman P, Vrba J & Dolan JR (1999) Shifts in bacterial community composition associated with different microzooplankton size fractions in a eutrophic reservoir. Limnol. Oceanogr. 44: 1634–1644

    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

    Google Scholar 

  • Strom SL (2000) Bacterivory: interactions between bacteria and their grazers. In: Kirchman DL (Ed) Microbial Ecology of the Oceans (pp 351–386). Wiley-Liss, New York.

    Google Scholar 

  • Suzuki MT (1999) Effect of protistan bacterivory on coastal bacterioplankton diversity. Aquat. Microb. Ecol. 20: 261–272

    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

    Google Scholar 

  • Thingstad TF (1992) Modeling the microbial food web structure in pelagic ecosystems. Arch. Hydrobiol. Beih. Ergebn. Limnol. 37: 111–119

    Google Scholar 

  • Thingstad TF & Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13: 19–27

    Google Scholar 

  • Turley CM & Lochte K (1986) Diel changes in the specific growth rate and mean cell volume of natural bacterial communities in two different water masses in the Irish Sea. Microb. Ecol. 12: 271–282

    Article  Google Scholar 

  • Turley CM, Bianchi M, Christaki U, Conan P, Harris JRW, Parra S, Ruddy G, Stutt ED, Tselepides A & Van Wambeke F (2000) Relationship between primary producers and bacteria in an oligotrophic sea - the Mediterranean and biogeochemical implications. Mar. Ecol. Prog. Ser. 193: 11–18

    CAS  Google Scholar 

  • Vaqué D (1996) Seasonal dynamics of planktonic microbial communities on the coast of the northwest Mediterranean Sea. Publ. Espec. Inst. Esp. Oceanogr. 22: 39–46

    Google Scholar 

  • Vaqué D, Pace ML, Findlay S & Lints D (1992) Fate of bacterial production in a heterotrophic ecosystem: grazing by protists and metazoans in the Hudson Estuary. Mar. Ecol. Prog. Ser. 89: 155–163

    Google Scholar 

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

    Google Scholar 

  • Vaqué D, Casamayor EO & Gasol JM (2001) Dynamics of whole community bacterial production and grazing losses related to changes in the proportion of bacteria with different DNA-content. Aquat. Microb. Ecol. 25: 163–177

    Google Scholar 

  • Weimbauer MG & Peduzzi P (1995) Significance of viruses versus heterotrophic nanoflagellates for controlling bacterial abundance in the northern Adriatic Sea. J. Plankton Res. 17: 1851–1856

    Google Scholar 

  • Weisse T (1989) The microbial loop in the Read Sea: dynamics of pelagic bacteria and heterotrophic nanoflagellates. Mar. Ecol. Prog. Ser. 55: 241–250

    Google Scholar 

  • Weisse T (1999) Bacterivory in the northwestern Indian Ocean during the intermonsoon - northeast monsoon period. Deep Sea Res. II 46: 795–814

    Article  Google Scholar 

  • Weisse T & Scheffel-Möser U (1991) Uncoupling the microbial loop: growth and grazing loss rates of bacteria and heterotrophic nanoflagellates in the North Atlantic. Mar. Ecol. Prog. Ser. 71: 195–205

    Google Scholar 

  • Wikner J, Andersson A, Normark S & Hagström Å (1986) Use of genetically marked minicells as a probe in measurement of predation on bacteria in aquatic environments. Appl. Environ. Microbiol. 52: 4–8

    PubMed  CAS  Google Scholar 

  • Wright RT (1984) Dynamics and pools of dissolved organic carbon. In: Hobbie JH & Williams PJLeB (Eds) Heterotrophic Activity in the Sea (pp 121–154). Plenum, New York.

    Google Scholar 

  • Wright RT (1988) Methods for evaluating the interaction of substrate and grazing as factors controlling planktonic bacteria. Arch. Hydrobiol. Beih. Ergebn. Limnol. 31: 229–242

    Google Scholar 

  • Wright RT & Coffin RB (1984) Measuring microzooplankton grazing on planktonic marine bacteria by its impact on bacterial production. Microb. Ecol. 10: 137–149

    Article  Google Scholar 

  • Zubkov MV, Sleigh MA, Burkill PH & Leakey RJG (2000) Bacterial growth and grazing loss in contrasting food areas of North and South Atlantic. J. Plankton Res. 22: 685–771

    Article  Google Scholar 

  • Zubkov MV, Sleigh MA & Burkill PH (2001) Heterotrophic bacterial turnover along the 20°W meridian between 59°N and 37°N in July 1996. Deep-Sea Res. II 48: 987–1001

    Article  Google Scholar 

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Gasol, J.M., Pedrós-Alió, C. & Vaqué, D. Regulation of bacterial assemblages in oligotrophic plankton systems: results from experimental and empirical approaches. Antonie Van Leeuwenhoek 81, 435–452 (2002). https://doi.org/10.1023/A:1020578418898

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