Microbial mats: A joint venture

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Abstract

Microbial mats characteristically are dominated by a few functional groups of microbes: cyanobacteria, colorless sulfur bacteria, purple sulfur bacteria, and sulfate-reducing bacteria. Their combined metabolic activities result in steep environmental microgradients, particularly of oxygen and sulfide.

The driving force of most microbial mats is photosynthesis by cyanobacteria and algae. Subsequently, sulfate-reducing bacteria, using excretion-, lysis-, and decomposition products of cyanobacteria, produce sulfide by the dissimilatory reduction of sulfate. The sulfide can be reoxidized to sulfate by colorless and purple sulfur bacteria.

Colorless sulfur bacteria are chemotrophic organisms primarily oxidizing sulfide and other reduced forms of sulfur with oxygen to obtain energy. The oxidation of reduced sulfur species also provides reducing equivalents for the reduction of carbon dioxide to cellular carbon. The final product of sulfide oxidation is sulfate, with elemental sulfur, deposited extracellularly, as the principal intermediate.

Purple sulfur bacteria primarily are anaerobic phototrophic organisms using sulfide and other reduced forms of sulfur exclusively as the electron donor for the reduction of CO2 to cellular carbon. Usually, sulfur is temporarily stored intracellularly. The final product of the oxidation of reduced forms of sulfur is sulfate.

The niches for these metabolically different groups of microbes in ecosystems with steep, often non-overlapping, gradients of oxygen and sulfide appear to be spatially separated. However, maximum viable counts of colorless sulfur bacteria and purple sulfur bacteria were both found in the top 5–10 mm of mats. Unexpectedly, viable counts of sulfate-reducing bacteria also peaked at the same depth horizon.

Sulfide is inhibitory for most oxygenic phototrophs. Sulfide production immediately underneath the layer of cyanobacteria might inhibit their growth, and, consequently, that of the entire ecosystem. In microbial mats this effect is minimized by the combined action of colorless and purple sulfur bacteria. Colorless sulfur bacteria generally have a much higher affinity for sulfide than purple sulfur bacteria, however, in microbial mats, their activity is hampered by low oxygen supply rates. As shown by pure culture studies with colorless sulfur bacteria, sulfide is incompletely oxidized when oxygen is short in supply, resulting in the production of potential electron donors for purple sulfur bacteria, such as sulfur, thiosulfate and polysulfides. In the absence of purple sulfur bacteria, colorless sulfur bacteria would not be able to maintain a low sulfide concentration due to shortage of oxygen, which in turn would result in increased inhibition of oxygenic photosynthesis.

It thus appears that the combined action of all four groups of functional microbes mentioned effectively results in optimal growth of these recent “stromatolites”.

References (113)

  • J.A. Nicholson et al.

    Structure of a microbial mat at Great Sippewissett Marsh, Cape Cod, Masschusetts

    FEMS Microbiol. Ecol.

    (1987)
  • B.K. Pierson et al.

    Pigments, light penetration and photosynthetic activity in the multilayered microbial mats of Great Sippewissett Salt Marsh, Masschusetts

    FEMS Microbiol. Ecol.

    (1987)
  • J. Sørensen et al.

    Early diagenesis in sediments from Danish coastal waters: microbial activity and Mn-Fe-S geochemistry

    Geochim. Cosmochim. Acta

    (1987)
  • L.J. Stal et al.

    Structure and development of a benthic marine microbial mat

    FEMS Microbiol. Ecol.

    (1985)
  • H.G. Trüper

    Microorganisms and the sulfur cycle

  • Z. Aizenshtat et al.

    The geochemical sulphur enrichment of recent organic matter by polysulfides in the Solar-Lake

  • S.M. Awramik

    Ancient stromatolites and microbial mats

  • L.G.M. Baas Becking

    Studies on the sulphur bacteria

    Anal. Bot.

    (1925)
  • F. Bak et al.

    A novel type of energy metabolism involving fermentation of inorganic sulphur compounds

    Nature

    (1987)
  • F. Bak et al.

    Chemolithotrophic growth of Desulfovibrio sulfodismutans sp. nov. by disproportionation of inorganic sulfur compounds

    Arch. Microbiol.

    (1987)
  • M.M. Bateson et al.

    Photoexcretion and fate of glycolate in a hot spring cyanobacterial mat

    Appl. Environ. Microbiol.

    (1988)
  • J. Bauld

    Microbial mats in marginal marine environments: Shark Bay, Western Australia and Spencer Gulf, South Australia

  • D.E. Canfield et al.

    Aerobic sulfate reduction in microbial mats

    Science

    (1991)
  • R.W. Castenholz et al.

    Photosynthetic and behavorial versatility of the cyanobacterium Oscillatoria boryana in a sulfide-rich microbial mat

    FEMS Microbiol. Ecol.

    (1991)
  • Y. Cohen

    Oxygenic photosynthesis, anoxygenic photo-synthesis and sulfate reduction in cyanobacterial mats

  • Y. Cohen

    Photosynthesis in cyanobacterial mats and its relation to the sulfur cycle: a model for microbial sulfur interactions

  • Y. Cohen et al.

    Sulfide dependent anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica

    Nature

    (1975)
  • Y. Cohen et al.

    Facultative anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica

    J. Bacteriol.

    (1975)
  • J.W.H. Dacey et al.

    Hydroxide decomposition of DMSP to DMS

    J. Geophys. Res. Lett.

    (1987)
  • E.D. D'Amelio et al.

    Comparative functional ultrastructure of two hypersaline submerged cyanobacterial mats: Guerrero Negro, Baja California Sur, Mexico and Solar Lake, Sinai, Egypt

  • R. De Wit et al.

    Interactions between phototrophic bacteria in sediment ecosystems

    Hydrobiol. Bull.

    (1988)
  • R. De Wit et al.

    Growth of the phototrophic purple sulfur bacterium Thiocapsa roseopersicina under oxic/anoxic regimens in the light

    FEMS Microbiol. Ecol.

    (1990)
  • R. De Wit et al.

    Growth and metabolism of the purple sulfur bacterium Thiocapsa roseopersicina under combined light/dark and oxic/anoxic regimens

    Arch. Microbiol.

    (1990)
  • W. Dilling et al.

    Aerobic respiration in sulfate-reducing bacteria

    FEMS Microbiol. Lett.

    (1990)
  • E. Drobner et al.

    Pyrite formation linked with hydrogen evolution under anaerobic conditions

    Nature

    (1990)
  • J.N. Eloff et al.

    Photooxidation of cyanobacteria in natural conditions

    Appl. Environm. Microbiol.

    (1976)
  • T. Fenchel et al.

    Oxygen toxicity, repiration and behavioural responses to oxygen in free-living anaerobic ciliates

    J. Gen. Microbiol.

    (1990)
  • T. Fenchel et al.

    Anaerobic free-living protozoa: growth efficiencies and the structure of anaerobic communities

    FEMS Microbiol. Ecol.

    (1990)
  • U. Fischer

    Enzymatic steps and dissimilatory sulfur metabolism by whole cells of anoxyphotobacteria

  • A. Führböter et al.

    Biostabilisierung von Sandwatten durch Mikroorganismen

  • S. Garlick et al.

    Occurrence of facultative anoxygenic photosynthesis among filamentous and unicellular cyanobacteria

    J. Bacteriol.

    (1977)
  • W.C. Ghiorse

    Microbial reduction of manganese and iron

  • J. Grant et al.

    Prediction of coastal sediment stability from photopigment content of mats of purple sulphur bacteria

    Nature

    (1987)
  • D. Hastings et al.

    Sulfate reduction in the presence of low levels of oxygen in water column of the Cariaco Trench

    Limnol. Oceanogr.

    (1988)
  • R.W. Howarth

    Pyrite: its rapid formation in a salt marsh and its importance in ecosystem metabolism

    Science

    (1979)
  • B.J. Javor et al.

    Laminated microbial mats, Laguna Guerrero Negro, Mexico

    Geomicrobiol. J.

    (1981)
  • B.J. Javor et al.

    Invertebrate grazers of microbial mats

  • B.B. Jørgensen

    Bacterial sulfate reduction within reduced microniches of oxidized marine sediments

    Mar. Biol.

    (1977)
  • B.B. Jørgensen

    The sulfur cycle of a coastal marine sediment (Limfjorden, Denmark)

    Limnol. Oceanogr.

    (1977)
  • B.B. Jørgensen

    A comparison of methods for the quantification of bacterial sulfate reduction in coastal marine sediments. I. Measurement with radiotracer techniques

    Biogeochem. J.

    (1978)
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