Bacterial Influence on the Variability in the Ocean’s Biogeochemical State: A Mechanistic View

  • F. Azam
  • D. C. Smith
Part of the NATO ASI Series book series (volume 27)


Traditionally, the only component of the microbial communities studied seriously by biological oceanographers was phytoplankton. Bacteria, protozoa, viruses and fungi were relegated to “specialists” and it was implicitly assumed that, by and large, the ocean’s productivity mechanisms and biogeochemical dynamics could be understood and modelled without taking into account the activities of these other components of the pelagic microbiota. This view was challenged by the seminal paper of Pomeroy (1974) and by quantitative studies inspired by it, leading up to the discovery that the pathway DOM -- > bacteria -- > protozoa -- > metazoa (microbial loop; Azam et al., 1983) is a major route for the flows of material and energy in pelagic marine ecosystems. Further, very recently it has been suggested that viruses may also play important ecological roles (Bergh et al., 1989; Proctor and Fuhrman, 1990; Suttle et al., 1990), including a role in the mortality of bacteria and phytoplankton.


Euphotic Zone Phytoplankton Cell Attached Bacterium Carbon Demand Dissolve Free Amino Acid 
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  1. Alldredge AL, Youngbluth MJ (1985) The significance of macroscopic aggregates (marine snow) as sites for heterotrophic bacterial production in the mesopelagic zone of the subtropical Atlantic. Deep-Sea Res 32:1445–1456CrossRefGoogle Scholar
  2. Ammerman JW, Azam F (1985) Bacterial 5′-nucleotidase in aquatic ecosystems: a novel mechanism of phosphorus regeneration. Science 227:1338–1340CrossRefGoogle Scholar
  3. Azam, F (1984) The radioecological role of marine bacterioplankton In: Bonnyns-Van Gelder E, Kirchmann R (eds), Role of microorganisms on the behaviour of radionuclides in aquatic and terrestrial systems and their transfer to man. Int. Union Radioecologists, Brussels pp 2–7Google Scholar
  4. Azam F, Ammerman JW (1984) Cycling of organic matter by bacterioplankton in pelagic marine ecosystems: microenvironmental considerations., pp. 345–360 In: Fasham MJR (eds) Flows of energy and materials in marine ecosystems. Plenum PublishingGoogle Scholar
  5. Azam F, Cho BC (1987) Bacterial utilization of organic matter in the sea., pp. 261–281 In: (eds) Ecology of microbial communities. Cambridge University PressGoogle Scholar
  6. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil L A, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263CrossRefGoogle Scholar
  7. Belas R, Simon M, Silverman M (1986) Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus. J Bacteriol 167:210–218Google Scholar
  8. Bergh φ, Bφrsheim KY, Bratbak G, Heldal M (1989) High abundance of viruses found in aquatic environments. Nature 340:467–468CrossRefGoogle Scholar
  9. Biddanda BA, Pomeroy LR (1988) Microbial aggregation and degradation of phytoplankton-derived detritus in seawater. I. Microbial succession. Mar Ecol Prog Ser 42:79–88CrossRefGoogle Scholar
  10. Bjφrnsen PK (1988) Phytoplankton exudation of organic matter: Why do healthy cells do it? Limnol Oceanogr 33:151–154CrossRefGoogle Scholar
  11. Bratbak G, Thingstad TF (1985) Phytoplankton — bacteria interactions: an apparent paradox? Analysis of a model system with both competition and commensalism. Mar Ecol Prog Ser. 25:23–30CrossRefGoogle Scholar
  12. Chett I, Mitchell R (1976) Ecological aspects of microbial chemotactic behavior. Ann Rev Microbiol 30:221–239CrossRefGoogle Scholar
  13. Cho BC (1988) Significance of bacteria in biogeochemical fluxes in the pelagic ocean. Ph. D. thesis, University of California, San Diego.Google Scholar
  14. Cho BC, Azam F (1990) Biogeochemical significance of bacterial biomass in the oceans euphotic zone. Mar Ecol Prog Ser 63:253–259CrossRefGoogle Scholar
  15. Dawson MP, Humphrey B, Marshall KC (1981) Adhesion: a tactic in the survival strategy of a marine vibrio during starvation. Curr Microbiol 6:195–198CrossRefGoogle Scholar
  16. Ducklow HW, Hill SW, Gardner WD (1985) Bacterial growth and the decomposition of particulate organic carbon collected in sediment traps. Cont Shelf Res 4: 445–464CrossRefGoogle Scholar
  17. Fuhrman JA, Sleeter TD, Carlson C, Proctor LM (1989) Dominance of bacterial biomass in the Sargasso Sea and its ecological implications. Mar Ecol Prog Ser 57:207–217CrossRefGoogle Scholar
  18. Goldman JC (1984) Conceptual role for microaggregates in pelagic waters. Bull Mar Sci 35:462–47Google Scholar
  19. Gottschalk G (ed) (1986) Bacterial Metabolism. Springer-Verlag New YorkGoogle Scholar
  20. Hollibaugh JT, Azam F (1983) Microbial degradation of dissolved proteins in seawater. Limnol Oceanogr 28:1104–1116CrossRefGoogle Scholar
  21. Hoppe H-G (1984) Attachment of bacteria: advantage or disadvantage for survival in the aquatic environment., pp. 283–301 In: Marshall KC (ed) Microbial adhesion and aggregation. SpringerCrossRefGoogle Scholar
  22. Iturriaga R, Mitchell BG (1986) Chroococcoid cyanobacteria: a significant component in the food web dynamics of the open ocean. Mar Ecol Prog Ser 28:291–297CrossRefGoogle Scholar
  23. Jackson GA (1989) Simulation of bacterial attraction and adhesion to falling particles in an aquatic environment. Limnol Oceanogr 34:514–530CrossRefGoogle Scholar
  24. Jacobsen JT, Azam F (1984) Role of bacteria in copepod fecal pellet decomposition: colonization, growth rates and mineralization. Bull Mar Sci 35:495–502Google Scholar
  25. Johnson PW, Xu H-S, Sieburth JMcN (1982) The utilization of chroococcoid cyanobacteria by marine protozooplankters but not by calanoid copepods. Ann Inst Oceanogr Paris 58:297–308Google Scholar
  26. Karl DM, Knauer GA, Martin JH (1988) Downward flux of particulate organic matter in the ocean: a particle decomposition paradox. Nature 332:438–441CrossRefGoogle Scholar
  27. Kirchman DL (1983) The production of bacteria attached to particles suspended in a freshwater pond. Limnol. Oceanogr. 28:858–872CrossRefGoogle Scholar
  28. Koike I, Shigemitsu H, Kazuki T, Kogure K (1990) Role of sub-micrometre particles in the ocean. Nature 345:242–244CrossRefGoogle Scholar
  29. Laws EA, Redalje DG, Haas LW, Bienfang PK, Eppley RW, Harrison WG, Karl DM, Marra J (1984) High phytoplankton growth rates in oligotrophic Hawaiian coastal waters. Limnol Oceanogr 29:1161–1169CrossRefGoogle Scholar
  30. McCarthy JJ, Goldman JC (1979) Nitrogenous nutrition of marine phytoplankton in nutrient-depleted waters. Science 203:670–672CrossRefGoogle Scholar
  31. Mitchell JG, Okubo A, Fuhrman JA (1985) Microzones surrounding phytoplankton form the basis for a stratified marine microbial ecosystem. Nature 316:58–59CrossRefGoogle Scholar
  32. Mitchell JG, Okubo A, Fuhrman JA (1990) Gyrotaxis as a new mechanism for generating spatial heterogeneity and migration in microplankton. Limnol. Oceanogr. 35:123–130CrossRefGoogle Scholar
  33. Mykelstad S (1977) Production of carbohydrates by marine planktonic diatoms. II. Influence of the N/P ratio n the growth medium on the assimilation ratio, growth rate, and production of cellular and extracellular carbohydrates by Chaetoceros affinis var. willei (Gran) Hustedt and Skeletonema costatum (Grev.) Cleve. J. Exp. Mar. Biol. Ecol. 29:161–179CrossRefGoogle Scholar
  34. Paerl HW, Gallucci KK (1985) Role of Chemotaxis in establishing a specific nitrogen-fixing cyanobacterial-bacterial association. Science 227:647–649CrossRefGoogle Scholar
  35. Paul JH, DeFlaun MF, Jeffrey WH (1988) Mechanisms of DNA utilization by estuarine microbial populations. Appl Environ Microbiol 54:1682–1688Google Scholar
  36. Pedrós-Alió C, Brock TD (1983) The importance of attachment to particles for planktonic bacteria. Arch Hydrobiol 98:354–379Google Scholar
  37. Phinney DA, Yentsch CS (1986) The relationship between phytoplankton and light attenuation in ocean waters. SPIE 637 Ocean Optics VIII:321–327Google Scholar
  38. Pomeroy LR (1974) The ocean’s food web, a changing paradigm. BioScience 24:499–504CrossRefGoogle Scholar
  39. Pomeroy LR, Wiebe WJ (1988) Energetics of microbial food webs. Hydrobiologia 159:7–18CrossRefGoogle Scholar
  40. Priest FG (ed) (1984) Extracellular enzymes. Van Nostrand Reinhold Wokingham, U.K.Google Scholar
  41. Proctor LM, Fuhrman JA (1990) Viral mortality of marine bacteria and cyanobacteria. Nature 343:60–62CrossRefGoogle Scholar
  42. Silver MW, Alldredge AL (1981) Bathypelagic marine snow: deep-sea algal and detrital community. J. Mar. Res. 39:501–530Google Scholar
  43. Silver MW, Bruland KW (1981) Differential feeding and fecal pellet composition of salps and pteropods, and the possible origin of deep water flora and olive-green “cells”. Mar Biol 62:263–273CrossRefGoogle Scholar
  44. Simon M, Alldredge AL, Azam F (1990) Bacterial carbon dynamics on marine snow. Mar Ecol Prog Ser 65:205–211CrossRefGoogle Scholar
  45. Smetacek V (1985) Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance. Mar Biol 84:239–251CrossRefGoogle Scholar
  46. Somville M, Billen G (1983) A method for determining exoproteolytic activity in natural waters. Limnol Oceanogr 28:190–193CrossRefGoogle Scholar
  47. Strickler JR (1982) Calanoid copepods, feeding currents, and the role of gravity. Science 218:158–160CrossRefGoogle Scholar
  48. Suttle CA, Chan AM, Cottrell MT (1990) Infection of phytoplankton by viruses and reduction of primary productivity. Nature 347:467–469CrossRefGoogle Scholar
  49. Tupas L, Koike I (1990) Amino acid and ammonium utilization by heterotrophic marine bacteria grown in enriched sea water. Limnol Oceanogr 35:1146–1155CrossRefGoogle Scholar
  50. Wheeler PA, Kirchman DL (1986) Utilization of inorganic and organic nitrogen by bacteria in marine systems. Limnol Oceanogr 31:998–1009CrossRefGoogle Scholar
  51. Williams PJLeB (1990) The importance of losses during microbial growth: commentary on the physiology, measurement and ecology of the release of dissolved organic material. Mar Microbial Food Webs 4:141–256Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1991

Authors and Affiliations

  • F. Azam
    • 1
  • D. C. Smith
    • 1
  1. 1.Marine Biology Research Division Scripps Institution of OceanographyUniversity of California, San DiegoLa JollaUSA

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