This group of bacteria produces sulfide by oxidizing simple organic compounds, using
sulfate as electron acceptor. The sulfide produced precipitates as iron-sulfide, which
forms the black layer, typical for anoxic marine sediments. Sulfide may act as electron
donor for anoxygenic photosynthesis by purple sulfur bacteria. Conditions given these
bacteria form a red layer between the cyanobacteria and the sulfate reducing bacteria.
Very marked gradients of oxygen and sulfide exist in microbial mats. In the light,
cyanobacteria produce oxygen and purple sulfur bacteria consume sulfide. The interface
of oxygen and sulfide can found at the lower border of the cyanobacteria mat. A
coexistence of low concentrations of oxygen and sulfide has been found in several mat
systems (Jorgensen et al, 1979; 1983; Krumbein et al, 1979; Revsbech et al, 1983). In the
dark, oxygen production by oxygenic photosynthesis of cyanobacteria as well as sulfide
oxidation by the purple sulfur bacteria stops. The oxygen wich eventually accumulated
during the day is rapidly consumed by heterotrophic organisms. Sulfide production by
the sulfate reducing bacteria presumably continues. Therefore also a chemical reduction
of oxygen by sulfide is expected. After some period of darkness the oxygen/sulfide
interface moves up and, finally, can be found at or above the mat surface.
Hence, the cyanobacteria in these systems will be faced by anaerobic conditions in the
dark. Thus far, dark metabolism of cyanobacteria generally is believed to be aerobic
respiration (Smith, 1982). Only in a few occasions anaerobic dark metabolism of a
cyanobacterium was reported. Oscillatoria limnetica has shown to be able to ferment its
carbon reserve polymer polyglucose to lactate. In the presence of elemental sulfur this
organism carries out a sulfur respiration (Oren and Shilo, 1979). Oren and Shilo (1979)
observed sulfide production in Aphanothece halophytica under dark anaerobic conditions. An other type of anaerobic respiration in cyanobacteria was observed in Synechococcus lividus. This organism respires endogenous carbon reserves using sulfate or
thiosulfate as terminal electron acceptors. Sulfide and in the case of thiosulfate as electron
acceptor, also sulfite are the products (Sheridan and Castenholz, 1968; Sheridan, 1973).
The Shallows of the southern North Sea (Wadden Sea) are characterized by large
intertidal flats. In the upper littoral zone of these intertidal flats microbial mats develop.
Because of their green-red-black lamination Schulz (1936) and Schulz and Meyer (1939)
called this biotope “Farbstreifen-Sandwatt” (colour-striped-sand).
The North Sea mats we investigated are dominated by two species of cyanobacteria.
Oscillatoria sp. is particulary important in freshly colonized sediments (Stal et al, 1984b).
Microcoleus chthonoplastes is the main mat builder and is the dominant organism in
well-developed cyanobacterial mats (Stal et al, 1984c). There is a good deal of evidence
that nitrogen fixation is the critical process responsible for initial sediment colonization
(Stal et al, 1984b). Previously, we showed that Oscillatoria sp. strain 23, a filamentous,
non-heterocystous cyanobacterium, isolated from this environment, can fix nitrogen
even under aerobic conditions (Stal and Krumbein, 1981). We also found that this
organism can fix nitrogen in the dark under anaerobic conditions. Here we report
anaerobic dark energy metabolism in cultures of Oscillatoria sp. strain 23 and Microcoleus chthonoplastes.
MATERIALS AND METHODS
Organisms and culture conditions
Oscillatoria sp. strain 23 and Microcoleus chthonoplastes strain 11 were isolated from the
302
sulfate as electron acceptor. The sulfide produced precipitates as iron-sulfide, which
forms the black layer, typical for anoxic marine sediments. Sulfide may act as electron
donor for anoxygenic photosynthesis by purple sulfur bacteria. Conditions given these
bacteria form a red layer between the cyanobacteria and the sulfate reducing bacteria.
Very marked gradients of oxygen and sulfide exist in microbial mats. In the light,
cyanobacteria produce oxygen and purple sulfur bacteria consume sulfide. The interface
of oxygen and sulfide can found at the lower border of the cyanobacteria mat. A
coexistence of low concentrations of oxygen and sulfide has been found in several mat
systems (Jorgensen et al, 1979; 1983; Krumbein et al, 1979; Revsbech et al, 1983). In the
dark, oxygen production by oxygenic photosynthesis of cyanobacteria as well as sulfide
oxidation by the purple sulfur bacteria stops. The oxygen wich eventually accumulated
during the day is rapidly consumed by heterotrophic organisms. Sulfide production by
the sulfate reducing bacteria presumably continues. Therefore also a chemical reduction
of oxygen by sulfide is expected. After some period of darkness the oxygen/sulfide
interface moves up and, finally, can be found at or above the mat surface.
Hence, the cyanobacteria in these systems will be faced by anaerobic conditions in the
dark. Thus far, dark metabolism of cyanobacteria generally is believed to be aerobic
respiration (Smith, 1982). Only in a few occasions anaerobic dark metabolism of a
cyanobacterium was reported. Oscillatoria limnetica has shown to be able to ferment its
carbon reserve polymer polyglucose to lactate. In the presence of elemental sulfur this
organism carries out a sulfur respiration (Oren and Shilo, 1979). Oren and Shilo (1979)
observed sulfide production in Aphanothece halophytica under dark anaerobic conditions. An other type of anaerobic respiration in cyanobacteria was observed in Synechococcus lividus. This organism respires endogenous carbon reserves using sulfate or
thiosulfate as terminal electron acceptors. Sulfide and in the case of thiosulfate as electron
acceptor, also sulfite are the products (Sheridan and Castenholz, 1968; Sheridan, 1973).
The Shallows of the southern North Sea (Wadden Sea) are characterized by large
intertidal flats. In the upper littoral zone of these intertidal flats microbial mats develop.
Because of their green-red-black lamination Schulz (1936) and Schulz and Meyer (1939)
called this biotope “Farbstreifen-Sandwatt” (colour-striped-sand).
The North Sea mats we investigated are dominated by two species of cyanobacteria.
Oscillatoria sp. is particulary important in freshly colonized sediments (Stal et al, 1984b).
Microcoleus chthonoplastes is the main mat builder and is the dominant organism in
well-developed cyanobacterial mats (Stal et al, 1984c). There is a good deal of evidence
that nitrogen fixation is the critical process responsible for initial sediment colonization
(Stal et al, 1984b). Previously, we showed that Oscillatoria sp. strain 23, a filamentous,
non-heterocystous cyanobacterium, isolated from this environment, can fix nitrogen
even under aerobic conditions (Stal and Krumbein, 1981). We also found that this
organism can fix nitrogen in the dark under anaerobic conditions. Here we report
anaerobic dark energy metabolism in cultures of Oscillatoria sp. strain 23 and Microcoleus chthonoplastes.
MATERIALS AND METHODS
Organisms and culture conditions
Oscillatoria sp. strain 23 and Microcoleus chthonoplastes strain 11 were isolated from the
302