Mathematical simulation of the interactions among cyanobacteria, purple sulfur bacteria and chemotrophic sulfur bacteria in microbial mat communities

A deterministic one-dimensional reaction diffusion model was constructed to simulate benthic stratification patterns and population dynamics of cyanobacteria, purple and colorless sulfur bacteria as found in marine microbial mats. The model involves the major biogeochemical processes of the sulfur cycle and includes growth metabolism and their kinetic parameters as described from laboratory experimentation. Hence, the metabolic production and consumption processes are coupled to population growth. The model is used to calculate benthic oxygen, sulfide and light profiles and to infer spatial relationships and interactions among the different populations. Furthermore, the model is used to explore the effect of different abiotic and biotic environmental parameters on the community structure. A strikingly clear pattern emerged of the interaction between purple and colorless sulfur bacteria: either colorless sulfur bacteria dominate or a coexistence is found of colorless and purple sulfur bacteria. The model predicts that purple sulfur bacteria only proliferate when the studied environmental parameters surpass well-defined threshold levels. However, once the appropriate conditions do occur, the purple sulfur bacteria are extremely successful as their biomass outweighs that of colorless sulfur bacteria by a factor of up to 17. The typical stratification pattern predicted closely resembles the often described bilayer communities which comprise a layer of purple sulfur bacteria below a cyanobacterial top-layer; colorless sulfur bacteria are predicted to sandwich in between both layers. The profiles of oxygen and sulfide shift on a diel basis similarly as observed in real systems.

[1]  H. Gemerden,et al.  Relationships between functional groups of organisms in microbial mats , 1994 .

[2]  R. Hesslein,et al.  Similarity of whole‐sediment molecular diffusion coefficients in freshwater sediments of low and high porosity , 1991 .

[3]  H Rasmussen,et al.  Microelectrode studies of seasonal oxygen uptake in a coastal sediment: role of molecular diffusion , 1992 .

[4]  Y. Cohen,et al.  Diurnal Cycles of Sulfate Reduction under Oxic Conditions in Cyanobacterial Mats , 1992, Applied and environmental microbiology.

[5]  P. Visscher,et al.  Rates of sulfate reduction and thiosulfate consumption in a marine microbial mat , 1992 .

[6]  H. Cypionka Novel metabolic capacities of sulfate-reducing bacteria, and their activities in microbial mats , 1994 .

[7]  P. Visscher,et al.  COMPETITION BETWEEN ANOXYGENIC PHOTOTROPHIC BACTERIA AND COLORLESS SULFUR BACTERIA IN A MICROBIAL MAT , 1992 .

[8]  L. Stal,et al.  STRUCTURE AND DEVELOPMENT OF A BENTHIC MARINE MICROBIAL MAT , 1985 .

[9]  J. Wimpenny CRC Handbook of Laboratory Model Systems for Microbial Ecosystems , 1988 .

[10]  Christophe Rabouille,et al.  Towards the EDGE: Early diagenetic global explanation. A model depicting the early diagenesis of organic matter, O2, NO3, Mn, and PO4 , 1991 .

[11]  B. Jørgensen,et al.  Microalgal photosynthesis and spectral scalar irradiance in coastal marine sediments of Limfjorden, Denmark , 1992 .

[12]  H. Jonkers,et al.  In situ fluctuations of oxygen and sulphide in marine microbial sediment ecosystems , 1989 .

[13]  P. Caumette,et al.  Microbial mats in the hypersaline ponds of Mediterranean salterns (Salins-de-Giraud, France) , 1994 .

[14]  Steven Emerson,et al.  A model of oxygen reduction, denitrification, and organic matter mineralization in marine sediments1 , 1982 .

[15]  H. Gemerden,et al.  Chemolithotrophic growth of the phototrophic sulfur bacterium Thiocapsa roseopersicina , 1987 .

[16]  B. Jørgensen,et al.  Competition for sulfide among colorless and purple sulfur bacteria in cyanobacterial mats. , 1986, FEMS microbiology ecology.

[17]  L. V. Bogorov [The properties of Thiocapsa roseopersicina, strain BBS, isolated from an estuary of the White Sea]. , 1974, Mikrobiologiia.

[18]  H. Gemerden,et al.  Growth and metabolism of the purple sulfur bacterium Thiocapsa roseopersicina under combined light/dark and oxic/anoxic regimens , 1990 .

[19]  W. Helder,et al.  Rapid redistribution of oxygen in a sandy sediment induced by changes in the flow velocity of the overlying water , 1991 .

[20]  R. Dewit,et al.  Oxidation of sulfide to thiosulfate by , 1987 .

[21]  D. Canfield,et al.  Aerobic sulfate reduction in microbial mats. , 1991, Science.

[22]  H. Gemerden,et al.  Sulfide oxidation under oxygen limitation by a thiobacillus thioparus isolated from a marine microbial mat , 1993 .

[23]  H. Gemerden,et al.  Simultaneous phototrophic and chemotrophic growth in the purple sulfur bacterium Thiocapsa roseopersicina M1 , 1994 .

[24]  E. Padan,et al.  Occurrence of facultative anoxygenic photosynthesis among filamentous and unicellular cyanobacteria , 1977, Journal of bacteriology.

[25]  B. Jørgensen,et al.  Spectral light measurements in microbenthic phototrophic communities with a fiber‐optic microprobe coupled to a sensitive diode array detector , 1992 .

[26]  H. Gemerden,et al.  Microbial Interactions among Aerobic and Anaerobic Sulfur-Oxidizing Bacteria , 1985 .

[27]  B. Jørgensen,et al.  Growth Pattern and Yield of a Chemoautotrophic Beggiatoa sp. in Oxygen-Sulfide Microgradients , 1986, Applied and environmental microbiology.

[28]  B. Jørgensen,et al.  Adaptation to Hydrogen Sulfide of Oxygenic and Anoxygenic Photosynthesis among Cyanobacteria , 1986, Applied and environmental microbiology.

[29]  H. Gemerden Microbial mats: A joint venture , 1993 .

[30]  John F. Stolz,et al.  Structure of a microbiol mat at Great Sippewissett Marsh, Cape Cod, Massachusetts , 1987 .

[31]  H. Gemerden,et al.  Growth of the phototrophic purple sulfur bacterium Thiocapsaroseopersicina under oxic/anoxic regimens in the light , 1990 .

[32]  L. Baas-Becking Studies on the Sulphur Bacteria , 1925 .

[33]  N. Pfennig,et al.  Chemoautotrophic growth of Thiocystis violacea, Chromatium gracile and C. vinosum in the dark at various O2‐concentrations , 1986 .

[34]  E. Rosenberg,et al.  Microbial mats : physiological ecology of benthic microbial communities , 1989 .

[35]  T. Blackburn,et al.  A reaction diffusion model of C-N-S-O species in a stratified sediment , 1993 .

[36]  B. Pierson,et al.  Spectral Irradiance and Distribution of Pigments in a Highly Layered Marine Microbial Mat , 1990, Applied and environmental microbiology.

[37]  B. Jørgensen,et al.  Microelectrode studies of the photosynthesis and O2, H2S, and pH profiles of a microbial mat1 , 1983 .

[38]  B. Jørgensen,et al.  Light penetration and light intensity in sandy marine sediments measured with irradiance and scalar irradiance fiber-optic microprobes , 1994 .

[39]  L. R. Mur,et al.  Growth Kinetics of Oscillatoria agardhii Gomont in Continuous Culture, Limited in its Growth by the Light Energy Supply , 1979 .

[40]  R. Wit Interactions between phototrophic bacteria in marine sediments , 1989 .

[41]  E. Padan,et al.  Facultative anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica , 1975, Journal of bacteriology.

[42]  R. Guerrero,et al.  Vertical stratification and microbial assemblage of a microbial mat in the Ebro Delta (Spain) , 1991 .

[43]  John F. Andrews,et al.  A mathematical model for the continuous culture of microorganisms utilizing inhibitory substrates , 1968 .

[44]  H. Gemerden,et al.  Growth of the cyanobacterium Microcoleus chtonoplastes on sulfide , 1988 .