Microbial Ecology

, Volume 31, Issue 3, pp 225–247 | Cite as

A mini-review of microbial consortia: Their roles in aquatic production and biogeochemical cycling

  • H. W. Paerl
  • J. L. Pinckney


Molecular oxygen (O2) is a potent inhibitor of key microbial processes, including photosynthesis, N2 fixation, denitrification, sulfate reduction, methanogenesis, iron, and metal reduction reactions. Prokaryote survival and proliferation in aquatic environments is often controlled by the ability to tolerate exposure to oxic conditions. Many prokaryotes do not have subcellular organelles for isolating O2-producing from O2-consuming processes and have developed consortial associations with other prokaryotes and eukaryotes that alleviate metabolic constraints of high O2. Nutrient transformations often rely on appropriate cellular and microenvironmental, or microzonal, redox conditions. The spatial and temporal requirements for microenvironmental overlap among microbial groups involved in nutrient transformations necessitates close proximity and diffusional exchange with other biogeochemically distinct, yet complementary, microbial groups. Microbial consortia exist at different levels of community and metabolic complexity, as shown for detrital, microbial mat, biofilm, and planktonic microalgal-bacterial assemblages. To assess the macroscale impacts of consortial interactions, studies should focus on the range of relevant temporal (minutes to hours) and spatial (microns to centimeters) scales controlling microbial production, nutrient exchange, and cycling. In this review, we discuss the utility and application of techniques suitable for determining microscale consortial activity, production, community composition, and interactions in the context of larger scale aquatic ecosystem structure and function.


Denitrification Molecular Oxygen Methanogenesis Microbial Consortium Microbial Group 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Alldredge AL, Cohen Y (1987) Can microscale chemical patches persist in the sea? Microelectrode study of marine snow, fecal pellets. Science 235:689–691Google Scholar
  2. 2.
    Alldredge AL, Silver MW (1988) Characteristics, dynamics, and significance of marine snow. Prog Oceanogr 20:41–82Google Scholar
  3. 3.
    Allen MB (1952) The cultivation of myxophyceae. Arch Mikrobiol 17:34–53Google Scholar
  4. 4.
    Ahmadjian V, Paracer S (1986) Symbiosis: an introduction to biological associations. Clark University Press, HanoverGoogle Scholar
  5. 5.
    Bautista MF, Paerl HW (1985) Diel N2 fixation in an intertidal marine cyanobacterial mat community. Mar Chem 16:369–377Google Scholar
  6. 6.
    Bebout B, Paerl H, Crocker K, Prufert L (1987) Diel interactions of oxygenic photosynthesis and N2 fixation (acetylene reducion) in a marine microbial mat community. Appl Environ Microbiol 53:2353–2362Google Scholar
  7. 7.
    Bershova OI, Kopteva ZH, Tantsyurenko EV (1968) The interrelations between blue-green algae—the causative agents of water “blooms”—and bacteria. In: Topachevsky A (ed) Tsventenie Vody. Naukova Dunka, Kiev, Ukraine, pp 159–171Google Scholar
  8. 8.
    Caldwell DE (1977) The planktonic microflora of lakes. Crit Rev Microbiol 5:305–370Google Scholar
  9. 9.
    Caldwell DE (1979) Associations between photosynthetic and heterotrophic prokaryotes in plankton. In: Nichols JM (ed) Abstracts of the third international symposium on photosynthetic prokaryotes. Oxford Univ. Press, Oxford, EnglandGoogle Scholar
  10. 10.
    Caldwell DE, Caldwell SJ (1978) A Zoogloea sp. associated with blooms of Anabaena flosaquae. Can J Microbiol 24:922–931Google Scholar
  11. 11.
    Canfield DE, Des Marais DJ (1993) Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat. Geochim Cosmochim Acta 57:3971–3984Google Scholar
  12. 12.
    Carmichael WW (1991) Toxic freshwater blue-green algae (cyanobacteria): an overlooked health threat. Health Environ Digest 5:1–4Google Scholar
  13. 13.
    Carpenter EJ, Capone DG (1983) Nitrogen in the marine environment, Academic Press, New YorkGoogle Scholar
  14. 14.
    Chrost RJ, Brzeska D (1978) Extracellular release of organic products and growth of bacteria in Anabaena cylindrica (blue-green alga) culture. Acta Microbiol Polon 27:287–295Google Scholar
  15. 15.
    Cliff A, Ord J (1973) Spatial autocorrelation. Pion, LondonGoogle Scholar
  16. 16.
    Cliff A, Ord J (1981) Spatial processes: models and applications. Pion, LondonGoogle Scholar
  17. 17.
    Cloud P (1976) Beginnings of biospheric evolution and their biogeochemical consequences. Paleobiology 2:351–387Google Scholar
  18. 18.
    Cohen Y, Rosenberg E (1989) Microbial mats: physiological ecology of benthic microbial communities. American Society Microbiol, Washington, DCGoogle Scholar
  19. 19.
    Collins M (1978) Algal toxins. Microbiological Rev 42:725–746CrossRefGoogle Scholar
  20. 20.
    DeLong EF, Franks DG, Alldredge AL (1993) Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38:924–934Google Scholar
  21. 21.
    Delwiche CC (1970) The nitrogen cycle. Sci Am 223:136–146Google Scholar
  22. 22.
    DeYoe HR, Marks JC, Lowe RL (1992) The effect of nitrogen and phosphorus on the endosymbiont load of Rhopalodia gibba and Epithemia turgida (Bacillariophyceae). J Phycol 28:773–777Google Scholar
  23. 23.
    Donze M, Haveman J, Schiereck P (1972) Absence of pbotosystem 11 in heterocysts of the blue-green algae Anabaena. Biochim Biophys Acta 256:157–161Google Scholar
  24. 24.
    Dugdale RC (1967) Nutrient limitation in the seas: dynamics, identification, and significance. Limnol Oceanogr 12:685–695.Google Scholar
  25. 25.
    Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 546:340–373Google Scholar
  26. 26.
    Fogg GE (1982) Marine plankton. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell Scientific, Oxford, England, pp 491–513Google Scholar
  27. 27.
    Fogg GE (1982) Nitrogen cycling in sea water. Philos Trans R Soc London Ser 296:511–520Google Scholar
  28. 28.
    Fogg GE (1952) The production of extracellular nitrogenous substances by blue-green algae. Proc R Soc Lond [Biol] 139:372–397Google Scholar
  29. 29.
    Fogg GE, Westlake DF (1955) The importance of extracellular products of algae in freshwater. Verb Int Verein Theor Angew Limnol 12:219–232Google Scholar
  30. 30.
    Fogg GE, Stewart WDP, Fay P, Walsby AE (1973) The blue-green algae. Academic Press, LondonGoogle Scholar
  31. 31.
    Gallon JR (1992) Reconciling the incompatible:. N2 fixation and 02. Tansley review No. 144. New Phytol 122:571–609Google Scholar
  32. 32.
    Gallon JR, Kurz WGW, LaRue TA (1975) The physiology of nitrogen fixation by free-living microorganisms. Cambridge University Press, Cambridge, EnglandGoogle Scholar
  33. 33.
    Gibson CE, Smith RV (1982) Freshwater plankton. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell Scientific, Oxford, England, pp 463–490Google Scholar
  34. 34.
    Gorham PR (1964) Toxic algae. In: Jackson DF (ed) Algae and man. Plenum Press, New York, pp 307–336Google Scholar
  35. 35.
    Gorham PR, Carmichael WW (1980) Toxic substances from freshwater algae. Prog Wat Tech 12:189–198Google Scholar
  36. 36.
    Hattori A (1983) Denitrification and dissimilatory nitrate reduction. In: Carpenter EJ, Capone DG (eds) Nitrogen in the marine environment. Academic Press, New York, pp 191–232Google Scholar
  37. 37.
    Hellebust JA (1967) Excretion of organic compounds by cultured and natural populations of marine phytoplankton. In: Lauff GH (ed) Estuaries. AAAS special publication, AAAS, Washington, DC, pp 361–366Google Scholar
  38. 38.
    Herbst V, Overbeck J (1978) Metabolic coupling between the alga Oscillatoria redekei and accompanying bacteria. Naturwissenschaften 65:598–599Google Scholar
  39. 39.
    Henriksen K (1980) Measurement of in situ sites of nitrification in sediment. Microb Ecol 6:329–337Google Scholar
  40. 40.
    Holland JD (1978) The chemistry of the atmosphere and oceans. John Wiley & Sons, New YorkGoogle Scholar
  41. 41.
    Jørgensen BB (1983) Processes at the sediment-water interface. In: Bolin B, Cook R (eds) The major biogeochemical cycles and their interactions. John Wiley & Sons, New York, pp 477–509Google Scholar
  42. 42.
    Jørgensen BB, Des Marais D (1988) Optical properties of benthic photosynthetic communities: fiber optic studies of cyanobacterial mats. Limnol Oceanogr 33:99–113zbMATHGoogle Scholar
  43. 43.
    Jørgensen BB, Revsbech NP (1989) Oxygen uptake, bacterial distribution, and carbon-nitrogensulfur cycling in sediments from the Baltic Sea-North Sea transition. Ophelia 31:51–72Google Scholar
  44. 44.
    Joye SB, Paerl HW (1994) Nitrogen cycling in microbial mats: rates and patterns of denitrification and nitrogen fixation. Mar Biol 119:285–295Google Scholar
  45. 45.
    Kellar PE, Pearl HW (1980) Physiological adaptations in response to environmental stress during an N2-fixing Anabaena bloom. Appl Environ Microbiol 40:587–595Google Scholar
  46. 46.
    Knowles R (1982) Denitrificaiton. Microbiol Rev 46:43–70Google Scholar
  47. 47.
    Krieg NR, Hoffman PS (1986) Microaerophily and oxygen toxicity. Annu Rev Microbiol 40:107–130Google Scholar
  48. 48.
    Kuentzel EL (1969) Bacteria, carbon dioxide, and algal blooms. J Water Pollut Control Fed 41:1737–1747Google Scholar
  49. 49.
    Lange W (1967) Effects of carbohydrates on the symbiotic growth of the planktonic blue-green algae with cyanobacteria. Nature 215:1277–1278Google Scholar
  50. 50.
    Lange W (1971) Enhancement of algal growth in cyanophyta-bacteria systems by carbonaceous compounds. Can J Microbiol 17:303–314Google Scholar
  51. 51.
    Levin S, Paine R (1974) Disturbance, patch formation, and community structure. Proc Natl Acad Sci USA 71:2744–2747Google Scholar
  52. 52.
    Likens GE (1972) Nutrients and eutrophication. Am Soc Limnol Oceanogr Special Symp 1Google Scholar
  53. 53.
    Lupton FS, Marshall KC (1981) Specific adhesion of bacteria to heterocysts of Anabaena spp and its ecological significance. Appl Environ Microbiol 42:1085–1092Google Scholar
  54. 54.
    Margulis L, Schwartz K (1982) Five kingdoms: An illustrated guide to the phyla of life on Earth. WH Freeman, San FranciscoGoogle Scholar
  55. 55.
    Nalewajko C (1978) Release of organic substances. In: Hellebust JA, Craigie JS (eds) Handbook of phycological methods. Cambridge University Press, Cambridge, England, pp 389–398Google Scholar
  56. 56.
    Oremland RS (1988) Biogeochemistry of methanogenic bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. John Wiley & Sons, New York, pp 641–705Google Scholar
  57. 57.
    Paerl HW (1973) Detritus in Lake Tahoe: structural modification by attached microflora. Science 180:496–498Google Scholar
  58. 58.
    Paerl HW (1978) Role of heterotrophic bacteria in promoting N2 fixation by Anabaena in aquatic habitats. Microb Ecol 4:215–231Google Scholar
  59. 59.
    Paerl HW (1982) Interactions with bacteria. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell Scientific, Oxford, England, pp 441–461Google Scholar
  60. 60.
    Paerl HW (1982) Partitioning of CO2 fixation in the colonial cyanobacterium Microcystis aeruginosa: mechanism promoting formation of surface scums. Appl Environ Microbiol 46:252–259Google Scholar
  61. 61.
    Paerl HW (1984) Transfer of N2 and CO2 fixation products from Anabaena oscillarioides to associated bacteria during inorganic carbon sufficiency and deficiency. J Phycol 20: 600–608Google Scholar
  62. 62.
    Paerl HW (1990) Physiological ecology and regulation of N2 fixation in natural waters. Adv Microbiol Ecol 11:305–344Google Scholar
  63. 63.
    Paerl HW (1992) Cyanobacterial epi- and endobiotic interactions. In: Reisser W (ed) Algal sumbioses. Biopress, Bristol, England, pp 537–566Google Scholar
  64. 64.
    Paerl HW (1993) Interactions of nitrogen and carbon cycles in the marine environment. In: Ford TE (ed) Aquatic microbiology: an ecological approach. Blackwell Scientific, Oxford, England, pp 343–382Google Scholar
  65. 65.
    Paerl HW Bebout BM (1988) Direct measurement of O2-depleted microzones in marine Oscillatoria: relation to N2 fixation. Science 242:441–445Google Scholar
  66. 66.
    Paerl HW Bland PT (1982) Localized tetrazolium reduction in relation to N2 fixation, CO2 fixation, and H2 uptake in aquatic filamentous cyanobacteria. Appl Environ Microbiol 43:218–226Google Scholar
  67. 67.
    Paerl HW, Carlton RG (1988) Control of nitrogen fixation by oxygen depletion in surface-associated microzones. Nature 332:260–262Google Scholar
  68. 68.
    Paerl HW, Galluci KK (1985) Role of chemotaxis in establishing a specific nitrogen-fixing cyanobacterial-bacterial association. Science 227:647–649Google Scholar
  69. 69.
    Paerl HW, Kellar PE (1978) Significance of bacterial (cyanophyceae) Anabaena associations with respect to N2 fixation in freshwater. J Phycol 14:254–260Google Scholar
  70. 70.
    Paerl HW, Prufert LE (1987) Oxygen-poor microzones as potential sites of microbial N2 fixation in nitrogen-depleted aerobic marine waters. Appl Environ Microbiol 53:1078–1087Google Scholar
  71. 71.
    Paerl HW Ustach J (1982) Blue-green algal scums: an explanation for their occurrence during freshwater blooms. Limnol Oceanogr 27:212–217Google Scholar
  72. 72.
    Paerl HW Richards RC, Leonard RC, Goldman CR (1975) Seasonal nitrate cycling as evidence for complete vertical mixing in Lake Tahoe, California-Nevada. Limnol Oceanogr 20:1–8Google Scholar
  73. 73.
    Paerl HW, Bebout B, Prufert L (1989) Naturally occurring patterns of oxygenic photosynthesis and N2 fixation in a marine microbial mat: physiological and ecological ramifications. In: Cohen Y, Rosenberg E (eds) Microbial mats: physiological ecology of benthic microbial communities. American Society Microbiology, Washington, DC, pp 326–341Google Scholar
  74. 74.
    Paerl HW Crocker KM, Prufert LE (1987) Limitation of N2 fixation in coastal marine waters: relative importance of molybdenum, iron, phosphorus, and organic matter availability. Limnol Oceanogr 32:525–536Google Scholar
  75. 75.
    Pinckney J, Sandulli R (1990) Spatial autocorrelation analysis of meiofaunal and microalgal populations on an intertidal sandflat: scale linkage between consumers and resources. Est Coast Shelf Sci 30:341–353Google Scholar
  76. 76.
    Pinckney J, Piceno Y, Lovell C (1994) Short-term changes in the vertical distribution of benthic microalgal biomass in intertidal, muddy sediments. Diatom Res 9:143–153Google Scholar
  77. 77.
    Pinckney J, Zingmark R (1991) Effects of tidal stage and sun angles on intertidal benthic microalgal productivity. Mar Ecol Prog Set 76:81–89Google Scholar
  78. 78.
    Postgate JR (1978) Nitrogen fixation. Studies in biology No. 92. E. Arnold, LondonGoogle Scholar
  79. 79.
    Prufert-Bebout LE, Paerl HW Lassen C (1993) Growth, nitrogen fixation and spectral attenuation in cultivated Trichodesmium. Appl Environ Microbiol 59:1350–1359Google Scholar
  80. 80.
    Ramsing N, Kühl M, J∅rgensen B (1993) Distribution of sulfate-reducing bacteria, O2, and H2S in photosynthetic biofilms determined by oligonucleotide probes and microelectrodes. Appl Environ Microbiol 59:3840–3849Google Scholar
  81. 81.
    Revsbech NP, Christensen PB, Nielsen LP, Sorensen J (1989) Denitrification in a trickling filter biofilm studied by a microsensor for oxygen and nitrous oxide. Wat Res 23:1–5Google Scholar
  82. 82.
    Revsbech N, Jørgensen B (1986) Microelectrodes: their use in microbial ecology. Adv Microb Ecol 9:273–352Google Scholar
  83. 83.
    Ryther JH, Dunstan WM (1971) Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science 171:1008–1012Google Scholar
  84. 84.
    Safferman RS, Morris ME (1964) Growth characteristics of the blue-green algal virus LPP-1. J Bacteriol 88:771–775Google Scholar
  85. 85.
    Schopf JW, Walter MR (1982) Origin and early evolution of cyanobacteria: the geological evidence. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell Scientific, Oxford, England, pp 543–564Google Scholar
  86. 86.
    Smith DC, Simon M, Alldredge AL, Azam F (1992) Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 359:139–141Google Scholar
  87. 87.
    Smith AJ (1981) Cyanobacterial contributions to the heterotrophic connection. In: Dalton H (ed) Microbial growth on C-1 compounds. Heyden, London, pp 122–130Google Scholar
  88. 88.
    Sokal R, Oden N (1978) Spatial autocorrelation in biology. I. methodology. Biol J Linnaean Soc 10:199–228Google Scholar
  89. 89.
    Stal L, Grossberger S, Krumbein W (1984) Nitrogen fixation associated with the cyanobacterial mat of a marine laminated microbial ecosystem. Mar Biol 82:217–224Google Scholar
  90. 90.
    Staub R (1961) Emahrungsphysiologisch-autokologische untersuchungen an der planktanischen blaualge Oscillatoria rubescens DC Schweiz. Z Hydrol 23:84–198Google Scholar
  91. 91.
    Stewart WDP (1975) Nitrogen fixation by free-living microorganisms. Cambridge University Press, LondonGoogle Scholar
  92. 92.
    Straskrabova V (1974) Seasonal occurrence of several groups of heterotrophic bacteria in two reservoirs. Int Rev Ges Hydrobiol 59:9–18Google Scholar
  93. 93.
    Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. John Wiley & Sons, New York, pp 179–243Google Scholar
  94. 94.
    Upton G, Fingleton B (1985) Spatial data analysis by example. John Wiley & Sons, New YorkGoogle Scholar
  95. 95.
    Villareal TA (1993) Marine nitrogen-fixing diatom-cyanobacterial symbioses. In: Carpenter EJ, Capone DG, Reuter JG (eds) Marine pelagic cyanobacteria: Trichodesmium and other diazotrophs. Kluwer Academic, Dordrecht, the Netherlands, pp 163–176Google Scholar
  96. 96.
    Walsby AE (1974) The extracellular products of Anabaena cylindrica Lemm. I. Isolation of a macromolecular pigment-peptide complex. Br Phycol J 9:71–381Google Scholar
  97. 97.
    Ward BB (1986) Nitrification in marine environments. In: Prosser JI (ed) Nitrification. IRL Press, Oxford, England, pp 157–184Google Scholar
  98. 98.
    Whitton BA, Potts M (1982) Marine littoral. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell Scientific, Oxford, pp 515–542Google Scholar
  99. 99.
    Yates M (1980) The biochemistry of nitrogen fixation. In: Miflin BJ (ed) The biochemistry of plants, vol. 5. Academic Press, New YorkGoogle Scholar
  100. 100.
    Zehnder AJB (1978) Ecology of methane formation. In: Mitchell R (ed) Water pollution microbiology. John Wiley & Sons, New York, pp 349–376Google Scholar

Copyright information

© Springer-Verlag New York Inc 1996

Authors and Affiliations

  • H. W. Paerl
    • 1
  • J. L. Pinckney
    • 1
  1. 1.University of North Carolina at Chapel Hill, Institute of Marine SciencesMorehead CityUSA

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