Antonie van Leeuwenhoek

, Volume 81, Issue 1–4, pp 435–452

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

  • Josep M. Gasol
  • Carlos Pedrós-Alió
  • Dolors Vaqué
Article
  • 316 Downloads

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.

bacteria bottom-up flagellates oligotrophy open sea predation regulation top-down 

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References

  1. Andersen P & Fenchel T (1985) Bacterivory by microheterotrophic flagellates in seawater samples. Limnol. Oceanogr. 30: 198–202Google Scholar
  2. 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: 257–263Google Scholar
  3. 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: 2–14Google Scholar
  4. Berninger U-G, Finlay B & Kuuppo-Leinikki P (1991) Protozoan control of bacterial abundances in freshwater. Limnol. Oceanogr. 36: 139–147Google Scholar
  5. Biddanda B, Ogdahl M & Cotner J (2001) Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol. Oceanogr. 46: 730–739CrossRefGoogle Scholar
  6. Billen G, Servais P & Becquevort S (1990) Dynamics of bacterioplankton in oligotrophic and eutrophic aquatic environments: bottom-up or top-down control? Hydrobiologia 207: 37–42CrossRefGoogle Scholar
  7. 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: 283–292Google Scholar
  8. Carlson CA, Ducklow HW & Sleeter TD (1996) Stocks and dynamics of bacterioplankton in the northwestern Sargasso Sea. Deep-Sea Res. 43: 491–515CrossRefGoogle Scholar
  9. 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: 259–272Google Scholar
  10. Cochlan, WP (2001) The heterotrophic bacterial response during a mesoscale iron enrichment experiment (IronEx II) in the eastern equatorial Pacific Ocean. Limnol. Oceanogr. 46: 428–435CrossRefGoogle Scholar
  11. Coffin RB & Sharp JH (1987) Microbial trophodynamics in the Delaware Estuary. Mar. Ecol. Prog. Ser. 41: 253–266Google Scholar
  12. Cole JJ, Findlay S & Pace ML (1988) Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Mar. Ecol. Prog. Ser. 43: 1–10Google Scholar
  13. 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: 1718–1730CrossRefGoogle Scholar
  14. 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: 23–32Google Scholar
  15. 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: 297–307Google Scholar
  16. 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: 455–466PubMedCrossRefGoogle Scholar
  17. del Giorgio PA & Gasol JM (1995) Biomass distribution in freshwater plankton communities. Am. Nat. 146: 135–152CrossRefGoogle Scholar
  18. 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: 1169–1179CrossRefGoogle Scholar
  19. del Giorgio PA, Cole JJ, & Cimbleris A (1997) Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385: 148–151CrossRefGoogle Scholar
  20. Ducklow HW (1992) Factors regulating bottom-up control of bacteria biomass in open ocean plankton communities. Arch. Hydrobiol. Beih. Ergebn. Limnol. 37: 207–217Google Scholar
  21. Ducklow HW (1999) The bacterial component of the oceanic euphotic zone. FEMS Microb. Ecol. 30: 1–10CrossRefGoogle Scholar
  22. 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: 245–263CrossRefGoogle Scholar
  23. 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: 1305–1320CrossRefGoogle Scholar
  24. Eriksson C & Pedrós-Alió C (1990) Selenium as a nutrient for freshwater bacterioplankton and its interactions with phosphorus. Can. J. Microbiol. 36: 475–483Google Scholar
  25. 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: 80–94Google Scholar
  26. Fenchel T (1982) Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and importance as bacterial consumers. Mar. Ecol. Prog. Ser. 9: 35–42Google Scholar
  27. Fenchel T (1986) The ecology of heterotrophic microflagellates. Adv. Microb. Ecol. 9: 57–97Google Scholar
  28. Furhman JA & Noble RT (1995) Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol. Oceanogr. 40: 1236–1242Google Scholar
  29. Gasol JM (1994) A framework for the assessment of top-down vs bottom-up control of heterotrophic nanoflagellate abundance. Mar. Ecol. Prog. Ser. 113: 291–300Google Scholar
  30. Gasol JM & Duarte CM (2000) Comparative analyses in aquatic microbial ecology: how far do they go? FEMS Microb. Ecol. 31: 99–106CrossRefGoogle Scholar
  31. Gasol JM & Morán XAG (1999) Effects of filtration on bacterial activity and picoplankton community structure as assessed by flow cytometry. Aquat. Microb. Ecol. 16: 251–264Google Scholar
  32. Gasol JM & Vaqué D (1993) Lack of coupling between heterotrophic nanoflagellates and bacteria: a general phenomenon across aquatic systems? Limnol. Oceanogr. 38: 657–665Google Scholar
  33. Gasol JM, del Giorgio PA & Duarte CM (1997) Biomass distribution in marine planktonic communities. Limnol. Oceanogr. 42: 1353–1363CrossRefGoogle Scholar
  34. 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: 4475–4483PubMedGoogle Scholar
  35. 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: 62–77CrossRefGoogle Scholar
  36. Gili JM & Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Trends Ecol. Evol. 13: 316–320CrossRefGoogle Scholar
  37. 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: 205–213Google Scholar
  38. 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: 827–845CrossRefGoogle Scholar
  39. Hahn MW & Höfle MG (2001) Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microb. Ecol. 35: 113–121CrossRefGoogle Scholar
  40. 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
  41. Jürgens K (1994) Impact of Daphnia on planktonic microbial food webs - a review. Mar. Microb. Food Webs. 8: 295–324Google Scholar
  42. 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: 1241–1250PubMedGoogle Scholar
  43. Jürgens K & Güde H (1994) The potential importance of grazingresistant bacteria in planktonic systems. Mar. Ecol. Prog. Ser. 112: 169–188Google Scholar
  44. Jürgens K, Gasol JM & Vaqué (2000) Bacteria-flagellate coupling in microcosm experiments in the Central Atlantic Ocean. J. Exp. Mar. Biol. Ecol. 245: 127–147CrossRefGoogle Scholar
  45. Kirchman DL & Rich JH (1997) Regulation of bacterial growth rates by dissolved organic carbon and temperature in the equatorial Pacific Ocean. Microb. Ecol. 33: 11–20PubMedCrossRefGoogle Scholar
  46. 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: 1681–1688Google Scholar
  47. Kuuppo-Leinikki P (1990) Protozoan grazing on planktonic bacteria and its impact on bacterial population. Mar. Ecol. Prog. Ser. 63: 227–238Google Scholar
  48. Landry MR (1994) Methods and controls for measuring the grazing impact of planktonic protist. Mar. Microb. Food Webs. 8: 37–57Google Scholar
  49. Landry MR, Haas LW & Fagerness VL (1984) Dynamics of microbial plankton communities: experiments in Kaneohe Bay, Hawaii. Mar. Ecol. Prog. Ser. 16: 127–133Google Scholar
  50. 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: 1775–1782PubMedCrossRefGoogle Scholar
  51. 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: 307–327CrossRefGoogle Scholar
  52. Marrasé C, Lim EL & Caron DA (1992) Seasonal and daily changes in bacterivory in a coastal plankton community. Mar. Ecol. Prog. Ser. 82: 281–289Google Scholar
  53. 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: 1181–1188CrossRefGoogle Scholar
  54. McManus GB & Fuhrman JA (1988) Control of marine bacterioplankton populations: measurement and significance of grazing. Hydrobiologia 159: 51–62Google Scholar
  55. 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: 147–157CrossRefGoogle Scholar
  56. Pace ML & Cole JJ (1994) Comparative and experimental approaches to top-down and bottom-up regulation of bacteria. Microb. Ecol. 28: 181–193CrossRefGoogle Scholar
  57. Pace ML & Cole JJ (1996) Regulation of bacteria by resources and predation tested in whole-lake experiments. Limnol. Oceanogr. 41: 1448–1460Google Scholar
  58. Pakulski JD, Coffin RB, Kelley CA, Holder SL, Downer R, Aas P, Lyons MM & Jeffrey WH (1996) Iron stimulation of Antarctic bacteria. Nature 383: 133–134CrossRefGoogle Scholar
  59. 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: 985–1019CrossRefGoogle Scholar
  60. 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: 157–165Google Scholar
  61. 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: 596–601PubMedGoogle Scholar
  62. 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: 55–64Google Scholar
  63. Prairie Y T & Bird DF (1989) Some misconceptions about the spurious correlation problem in the ecological literature. Oecologia 81: 285–288Google Scholar
  64. Psenner R & Sommaruga R (1992) Are rapid changes in bacterial biomass caused by shifts from top-down to bottom-up control? Limnol. Oceanogr. 37: 1092–1100CrossRefGoogle Scholar
  65. Safi KA & Hall JA (1999) Mixotrophic and heterotrophic nanoflagellate grazing in the convergence zone east of New Zealand. Aquat. Microb. Ecol. 20: 83–93Google Scholar
  66. 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: 673–687Google Scholar
  67. 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: 1–14Google Scholar
  68. 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: 103–118Google Scholar
  69. Sherr EB & Sherr BF (1987) High rates of consumption of bacteria by pelagic ciliates. Nature 325: 710–711CrossRefGoogle Scholar
  70. Sherr BF, Sherr EB & Hopkinson CS (1988) Trophic interactions within pelagic microbial communities: indications of feedback regulation of carbon flow. Hydrobiologia 159: 19–26Google Scholar
  71. Sherr BF, Sherr EB & Pedrós-Alió C (1989) Simultaneous measurement of bacterioplankton production and protozoan bacterivory in estuarine water. Mar. Ecol. Prog. Ser. 54: 209–219Google Scholar
  72. Sherr EB, Sherr BF & Fessender L (1997) Heterotrophic protists in the Central Arctic Ocean. Deep-Sea Res. II 44: 1665–1682CrossRefGoogle Scholar
  73. 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: 795–808Google Scholar
  74. 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: 1634–1644CrossRefGoogle Scholar
  75. 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: 103–110Google Scholar
  76. 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
  77. Suzuki MT (1999) Effect of protistan bacterivory on coastal bacterioplankton diversity. Aquat. Microb. Ecol. 20: 261–272Google Scholar
  78. 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: 123–134Google Scholar
  79. Thingstad TF (1992) Modeling the microbial food web structure in pelagic ecosystems. Arch. Hydrobiol. Beih. Ergebn. Limnol. 37: 111–119Google Scholar
  80. Thingstad TF & Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13: 19–27Google Scholar
  81. 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: 271–282CrossRefGoogle Scholar
  82. 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: 11–18Google Scholar
  83. Vaqué D (1996) Seasonal dynamics of planktonic microbial communities on the coast of the northwest Mediterranean Sea. Publ. Espec. Inst. Esp. Oceanogr. 22: 39–46Google Scholar
  84. 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: 155–163Google Scholar
  85. Vaqué D, Gasol JM & Marrasé C (1994) Protists grazing rates: the significance of methodology and ecological factors. Mar. Ecol. Prog. Ser. 109: 263–274Google Scholar
  86. 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: 163–177Google Scholar
  87. Weimbauer MG & Peduzzi P (1995) Significance of viruses versus heterotrophic nanoflagellates for controlling bacterial abundance in the northern Adriatic Sea. J. Plankton Res. 17: 1851–1856Google Scholar
  88. Weisse T (1989) The microbial loop in the Read Sea: dynamics of pelagic bacteria and heterotrophic nanoflagellates. Mar. Ecol. Prog. Ser. 55: 241–250Google Scholar
  89. Weisse T (1999) Bacterivory in the northwestern Indian Ocean during the intermonsoon - northeast monsoon period. Deep Sea Res. II 46: 795–814CrossRefGoogle Scholar
  90. 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: 195–205Google Scholar
  91. 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: 4–8PubMedGoogle Scholar
  92. 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
  93. Wright RT (1988) Methods for evaluating the interaction of substrate and grazing as factors controlling planktonic bacteria. Arch. Hydrobiol. Beih. Ergebn. Limnol. 31: 229–242Google Scholar
  94. Wright RT & Coffin RB (1984) Measuring microzooplankton grazing on planktonic marine bacteria by its impact on bacterial production. Microb. Ecol. 10: 137–149CrossRefGoogle Scholar
  95. 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: 685–771CrossRefGoogle Scholar
  96. 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: 987–1001CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Josep M. Gasol
    • 1
  • Carlos Pedrós-Alió
    • 1
  • Dolors Vaqué
    • 1
  1. 1.Departament de Biologia Marina i OceanografiaInstitut de Ciències del Mar-CMIMA, CSICBarcelonaSpain

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