Adaptation of cyanobacteria to the sulfide-rich microenvironment of black band disease of coral

Black band disease (BBD) is a cyanobacteria-dominated microbial mat that migrates across living coral colonies lysing coral tissue and leaving behind exposed coral skeleton. The mat is sulfide-rich due to the presence of sulfate-reducing bacteria, integral members of the BBD microbial community, and the sulfide they produce is lethal to corals. The effect of sulfide, normally toxic to cyanobacteria, on the photosynthetic capabilities of five BBD cyanobacterial isolates of the genera Geitlerinema (3), Leptolyngbya (1), and Oscillatoria (1) and six non-BBD cyanobacteria of the genera Leptolyngbya (3), Pseudanabaena (2), and Phormidium (1) was examined. Photosynthetic experiments were performed by measuring the photoincorporation of [¹⁴C] NaHCO₃ under the following conditions: (1) aerobic (no sulfide), (2) anaerobic with 0.5 mM sulfide, and (3) anaerobic with 0.5 mM sulfide and 10 μM 3-(3',4'-dichlorophenyl)-1,1-dimethylurea (DCMU). All five BBD cyanobacterial isolates tolerated sulfide by conducting sulfide-resistant oxygenic photosynthesis. Five of the non-BBD cyanobacterial isolates did not tolerate sulfide, although one Pseudanabaena isolate continued to photosynthesize in the presence of sulfide at a considerably reduced rate. None of the isolates conducted anoxygenic photosynthesis with sulfide as an electron donor. This is the first report on the physiology of a culture of Oscillatoria sp. found globally in BBD.     

Adaptation to Hydrogen Sulfide of Oxygenic and Anoxygenic Photosynthesis among Cyanobacteria

Four different types of adaptation to sulfide among cyanobacteria are described based on the differential toxicity to sulfide of photosystems I and II and the capacity for the induction of anoxygenic photosynthesis. Most cyanobacteria are highly sensitive to sulfide toxicity, and brief exposures to low concentrations cause complete and irreversible cessation of CO₂ photoassimilation. Resistance of photosystem II to sulfide toxicity, allowing for oxygenic photosynthesis under sulfide, is found in cyanobacteria exposed to low H₂S concentrations in various hot springs. When H₂S levels exceed 200 μM another type of adaptation involving partial induction of anoxygenic photosynthesis, operating in concert with partially inhibited oxygenic photosynthesis, is found in cyanobacterial strains isolated from both hot springs and hypersaline cyanobacterial mats. The fourth type of adaptation to sulfide is found at H₂S concentrations higher than 1 mM and involves a complete replacement of oxygenic photosynthesis by an effective sulfide-dependent, photosystem II-independent anoxygenic photosynthesis. The ecophysiology of the various sulfide-adapted cyanobacteria may point to their uniqueness within the division of cyanobacteria.     

Cyanobacterial life at low O(2): community genomics and function reveal metabolic versatility and extremely low diversity in a Great Lakes sinkhole mat

Cyanobacteria are renowned as the mediators of Earth's oxygenation. However, little is known about the cyanobacterial communities that flourished under the low-O(2) conditions that characterized most of their evolutionary history. Microbial mats in the submerged Middle Island Sinkhole of Lake Huron provide opportunities to investigate cyanobacteria under such persistent low-O(2) conditions. Here, venting groundwater rich in sulfate and low in O(2) supports a unique benthic ecosystem of purple-colored cyanobacterial mats. Beneath the mat is a layer of carbonate that is enriched in calcite and to a lesser extent dolomite. In situ benthic metabolism chambers revealed that the mats are net sinks for O(2), suggesting primary production mechanisms other than oxygenic photosynthesis. Indeed, (14)C-bicarbonate uptake studies of autotrophic production show variable contributions from oxygenic and anoxygenic photosynthesis and chemosynthesis, presumably because of supply of sulfide. These results suggest the presence of either facultatively anoxygenic cyanobacteria or a mix of oxygenic/anoxygenic types of cyanobacteria. Shotgun metagenomic sequencing revealed a remarkably low-diversity mat community dominated by just one genotype most closely related to the cyanobacterium Phormidium autumnale, for which an essentially complete genome was reconstructed. Also recovered were partial genomes from a second genotype of Phormidium and several Oscillatoria. Despite the taxonomic simplicity, diverse cyanobacterial genes putatively involved in sulfur oxidation were identified, suggesting a diversity of sulfide physiologies. The dominant Phormidium genome reflects versatile metabolism and physiology that is specialized for a communal lifestyle under fluctuating redox conditions and light availability. Overall, this study provides genomic and physiologic insights into low-O(2) cyanobacterial mat ecosystems that played crucial geobiological roles over long stretches of Earth history.     

Sulfide inhibition of photosystem II in cyanobacteria (blue-green algae) and tobacco chloroplasts.

The present study shows that in the presence of 600 nm light, sulfide acts as a specific inhibitor of photosynthetic electron transport between water and Photosystem II in the cyanobacteria Aphanothece halophytica and Synechococcus 6311 as well as in tobacco chloroplasts. In the presence of 600 nm light sulfied affects the fast fluorescence transients as does a low concentration (10 mM) of hydroxylamine; the fluorescence yield decreases in the presence of either chemical and can be restored by the addition of 3-(3,4-dichlorophenyl)-1,1-dimethylurea. In chloroplasts, however, NH2OH, an electron donor at high concentrations (40 mM), relieves the sulfide effect. In the dark, sulfide affects the cyanobacterial fluorescence transients through decrease of oxygen tension. The fluorescence yield increases in a similar pattern to that observed under nitrogen flushing. Upon omission of sulfide in A. halophytica, the characteristic aerobic fluorescence transients return, consistent with the ease of alternation between oxygenic and sulfide-dependent anoxygenic photosynthesis in many cyanobacteria.     

Induction of anaerobic, photoautotrophic growth in the cyanobacterium Oscillatoria limnetica.

Anaerobic photoautotrophic growth of the cyanobacterium Oscillatoria limnetica was demonstrated under nitrogen in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea (5micron), a constant concentration of Na2S (2.5 mM), and constant pH (7.3). The photoanaerobic growth rate (2 days doubling time) was similar to that obtained under oxygenic photoautotrophic growth conditions. The potential of oxygenic photosynthesis is constitutive in the cells; that of anoxygenic photosynthesis is rapidly (2 h) induced in the presence of Na2S in the light in a process requiring protein synthesis. The facultative anaerobic phototrophic growth physiology exhibited by O. limnetica would seem to represent an intermediate physiological pattern between the obligate anaerobic one of photosynthetic bacteria and the oxygenic one of eucaryotic algae.     

Facultative anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica.

An isolate from H2S-rich layers of the Solar Lake, the cyanobacterium Oscillatoria limnetica, exhibits both oxygenic and anoxygenic photosynthesis. It can use Na2S as an electron donor for CO2 photoassimilation (photosystem I supplies the energy) in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea or 700-nm light. A stoichiometric ratio of approximately 2 is observed between the Na2S consumed and the photoassimilated CO2. The anoxygenic phototrophic capability of this cyanobacterium explains its growth in nature in high sulfide concentrations and indicates a selective advantage.     

Occurrence of facultative anoxygenic photosynthesis among filamentous and unicellular cyanobacteria.

Eleven of 21 cyanobacteria strains examined are capable of facultative anoxygenic photosynthesis, as shown by their ability to photoassimilate CO2 in the presence of Na2S, 3-(3,4-dichlorophenyl)-1,1-dimethylurea and 703-nm light. These include different cyanobacterial types (filamentous and unicellular) of different growth histories (aerobic, anaerobic, and marine and freshwater). Oscillatoria limnetica, Aphanothece halophytica (7418), and Lyngbya (7104) have different optimal concentrations of Na2S permitting CO2 photoassimilation, above which the rate decreases: 3.5, 0.7, and 0.1 mM, respectively. In A. halophytica, for each CO2 molecule photoassimilated two sulfide molecules are oxidized to elemental sulfur, which is excreted from the cells.The ecological and evolutionary significance of anoxygenic photosynthesis in the cyanobacteria is discussed.     

Physiology of sulfide tolerance in a thermophilic Oscillatoria

Oscillatoria amphigranulata is a fast-growing (3 doublings/day) cyanobacterium isolated from sulfide hot springs in New Zealand. Photosynthesis, as measured by incorporation of [¹⁴C]-HCO ₃ ^- , was initially inhibited by 0.3–1.5 mM sulfide at pH 7.9–8.1. However, conversion to sulfide-dependent anoxygenic photosynthesis occurred in about 2 h or less under light intensities of 3–14 klx. Under the stimulation of higher light intensity (8–14 klx) a partial recovery of oxygenic photosynthesis also occurred. It was concluded that oxygenic photosynthesis was responsible for 21–42% of the total incorporation at sulfide concentrations of 1.0–0.3 mM, respectively. This contribution was suppressed at 1.5 mM sulfide and not elicited under lower light intensities (3–7 klx). As judged by the inhibitory effect of 10 g/ml chloramphenicol protein synthesis was required for attainment of both anoxygenic photosynthesis and photosystem II recovery. Sulfide could not be replaced by thiosulfate, elemental sulfur or dithionite as electron donors in photosynthesis, but elemental sulfur could serve as the sole assimilatory source of sulfur. Oxygenic photosynthesis was inhibited by DCMU [3-(3,4-dichlorophenyl)-1,1-dimethylurea] or DBMIB (2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone), but sulfide relieved the effect of either inhibitor in adapted cells, indicating that electrons derived from sulfide enter the photosynthetic electron transport chain at a point beyond plastoquinone.Uncommon abbreviations DCMU 3-(3,4-dichlorophenyl)-1,1-dimethylurea - DBMIB 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone - DSPD disalicyclidene propanediamine - DNP-INT 2-4-dinitrophenyl ether of 2-iodo-4-nitrothymol - TMPD N,N,N,N-tetramethyl-p-phenylenediamine - PPO 2,5-diphenyloxazole - POPOP 1,4-bis-2-(5-phenyl oxzolyl) benzene     

Oxidation of sulfide to thiosulfate by Microcoleus chtonoplastes

Sulfide oxidation and product formation was studied in the cyanobacterium Microcoleus chtonoplastes. Anoxygenic photosynthesis was induced in the presence of sulfide and light. It was demonstrated that thiosulfate was the only product of the 3(3,4-dichlorophenyl)1,1-dimethylurea (DCMU)-insensitive photo-oxidation of sulfide. The affinity of this system for sulfide was shown to be very low.Oxygenic photosynthesis continued in the presence of sulfide. After an induction period of 3 h, oxygenic and anoxygenic photosynthesis were shown to be operating simultaneously.The ecological importance of sulfide oxidation and thiosulfate production by M. chtonoplastes is discussed in the context of laminated microbial ecosystems, where cyanobacteria and purple sulfur bacteria coexist.     

Loss of sulfide adaptation ability in a thermophilic Oscillatoria

A spontaneous variant incapable of anoxygenic photosynthesis was derived from a fully competent strain of Oscillatoria amphigramulata which was originally isolated from a high sulfide-containing hot spring of New Zealand. Although the variant (Oa-2) acquired a slight ability to photosynthesize in the presence of 0.3–0.4 mM sulfide, this was only after a 24 h exposure to sulfide and represented oxygenic photosynthesis only. Unlike the parent strain, the incompetent variant never grew in the presence of sulfide >0.05 mM, nor was there any relief of the inhibition by DCMU [3-(3,4-dichlorophenyl)-1,1-dimethylurea] of CO₂ photoincorporation when sulfide was present. The variant strain has retained all of these characteristics over a 4 year period with monthyl transfers in non-sulfide medium. The wild type, under identical conditions, has retained all of its competence with respect to sulfide.Abbreviations DCMU 3-(3,4-dichlorophenyl)-1,1-dimethylurea     

Spatial Dominance and Inorganic Carbon Assimilation by Conspicuous Autotrophic Biofilms in a Physical and Chemical Gradient of a Cold Sulfurous Spring: The Role of Differential Ecological Strategies

The community composition and ecophysiological features of microbial autotrophic biofilms were studied in Fuente Podrida, a cold sulfur spring located in East Spain. We demonstrated how different ecophysiological strategies, such as resistance and/or utilization of sulfide and oxygen, light adaptation, or resistance to high water flow, allow each of the microorganisms described to efficiently colonize several areas within the environmental gradient. In the zone of the spring constantly influenced by sulfide-rich waters, biofilms were formed by purple bacteria, cyanobacteria, and filamentous colorless sulfur bacteria. Purple bacteria showed higher photosynthetic efficiency per pigment unit than cyanobacteria, although they were dominant only in anoxic areas. Two filamentous cyanobacteria, strain UVFP1 and strain UVFP2, were also abundant in the sulfide-rich area. Whereas the cyanobacterial strain UVFP2 shows a strategy based on the resistance to sulfide of oxygenic photosynthesis, strain UVFP1, additionally, has the capacity for sulfide-driven anoxygenic photosynthesis. Molecular phylogenetic analyses cluster the benthic strain UVFP1 with genus Planktothrix, but with no particular species, whereas UVFP2 does not closely cluster with any known cyanobacterial species. The colorless sulfur bacterium Thiothrix sp. extended throughout the zone in which both sulfide and oxygen were present, exhibiting its capacity for chemolithoautotrophic dark carbon fixation. Downstream from the source, where springwater mixes with well-oxygenated stream water and sulfide disappears, autotrophic biofilms were dominated by diatoms showing higher photosynthetic rates than cyanobacteria and, by a lesser extent, by a sulfide-sensitive cyanobacterium (strain UVFP3) well adapted to low light availability, although in the areas of higher water velocity far from the river shore, the dominance shifted to crust-forming cyanobacteria. Both types of microorganisms were highly sensitive to sulfide impeding them from occupying sulfide-rich areas of the spring. Sulfide, oxygen, light availability, and water velocity appear as the main factors structuring the autotrophic community of Fuente Podrida spring. An erratum to this article is availbale at .     

Anoxygenic Photosynthesis Controls Oxygenic Photosynthesis in a Cyanobacterium from a Sulfidic Spring

Before the Earth''s complete oxygenation (0.58 to 0.55 billion years [Ga] ago), the photic zone of the Proterozoic oceans was probably redox stratified, with a slightly aerobic, nutrient-limited upper layer above a light-limited layer that tended toward euxinia. In such oceans, cyanobacteria capable of both oxygenic and sulfide-driven anoxygenic photosynthesis played a fundamental role in the global carbon, oxygen, and sulfur cycle. We have isolated a cyanobacterium, Pseudanabaena strain FS39, in which this versatility is still conserved, and we show that the transition between the two photosynthetic modes follows a surprisingly simple kinetic regulation controlled by this organism''s affinity for H₂S. Specifically, oxygenic photosynthesis is performed in addition to anoxygenic photosynthesis only when H₂S becomes limiting and its concentration decreases below a threshold that increases predictably with the available ambient light. The carbon-based growth rates during oxygenic and anoxygenic photosynthesis were similar. However, Pseudanabaena FS39 additionally assimilated NO₃⁻ during anoxygenic photosynthesis. Thus, the transition between anoxygenic and oxygenic photosynthesis was accompanied by a shift of the C/N ratio of the total bulk biomass. These mechanisms offer new insights into the way in which, despite nutrient limitation in the oxic photic zone in the mid-Proterozoic oceans, versatile cyanobacteria might have promoted oxygenic photosynthesis and total primary productivity, a key step that enabled the complete oxygenation of our planet and the subsequent diversification of life.     

Discovery of the first light‐dependent protochlorophyllide oxidoreductase in anoxygenic phototrophic bacteria

In all photosynthetic organisms, chlorophylls function as light‐absorbing photopigments allowing the efficient harvesting of light energy. Chlorophyll biosynthesis recurs in similar ways in anoxygenic phototrophic proteobacteria as well as oxygenic phototrophic cyanobacteria and plants. Here, the biocatalytic conversion of protochlorophyllide to chlorophyllide is catalysed by evolutionary and structurally distinct protochlorophyllide reductases (PORs) in anoxygenic and oxygenic phototrophs. It is commonly assumed that anoxygenic phototrophs only contain oxygen‐sensitive dark‐operative PORs (DPORs), which catalyse protochlorophyllide reduction independent of the presence of light. In contrast, oxygenic phototrophs additionally (or exclusively) possess oxygen‐insensitive but light‐dependent PORs (LPORs). Based on this observation it was suggested that light‐dependent protochlorophyllide reduction first emerged as a consequence of increased atmospheric oxygen levels caused by oxygenic photosynthesis in cyanobacteria. Here, we provide experimental evidence for the presence of an LPOR in the anoxygenic phototrophic α‐proteobacterium Dinoroseobacter shibae DFL12^T. In vitro and in vivo functional assays unequivocally prove light‐dependent protochlorophyllide reduction by this enzyme and reveal that LPORs are not restricted to cyanobacteria and plants. Sequence‐based phylogenetic analyses reconcile our findings with current hypotheses about the evolution of LPORs by suggesting that the light‐dependent enzyme of D. shibae DFL12^T might have been obtained from cyanobacteria by horizontal gene transfer.     

Comparative anoxygenic photosynthetic capacity in 7 strains of a thermophilic cyanobacterium

The capacity for anoxygenic photosynthesis and other physiological traits related to sulfide tolerance were compared in several strains of the thermophilic cyanobacterium Oscillatoria amphigranulata. Strains were isolated from hot springs in which the environmental sulfide over O. amphigranulata microbial mats spanned a range from 0.2 to 1 mM. Great differences in the capacity for anoxygenic photosynthesis existed among the isolates but these correlated in a predictable manner with the sulfide content of the springs. The time required for commencement of anoxygenic photosynthesis and the degree of initial sensitivity of Photosystem II to sulfide did not correlate with environmental sulfide levels. Kinetic parameters of sulfide consumption indicate uniformly low affinities for sulfide (K_m of about 1 mM) but differences among strains in V_max.Abbreviations CAM Chloramphenicol - DCMU 3-(3,4-dichlorophenyl)-1,1-dimethylurea - PC phycocyanin - PE phycoerythrin - PSII photosystem II     

Characterization of functional bacterial groups in a hypersaline microbial mat community (Salins-de-Giraud, Camargue, France)

A photosynthetic microbial mat was investigated in a large pond of a Mediterranean saltern (Salins-de-Giraud, Camargue, France) having water salinity from 70 per thousand to 150 per thousand (w/v). Analysis of characteristic biomarkers (e.g., major microbial fatty acids, hydrocarbons, alcohols and alkenones) revealed that cyanobacteria were the major component of the pond, in addition to diatoms and other algae. Functional bacterial groups involved in the sulfur cycle could be correlated to these biomarkers, i.e. sulfate-reducing, sulfur-oxidizing and anoxygenic phototrophic bacteria. In the first 0.5 mm of the mat, a high rate of photosynthesis showed the activity of oxygenic phototrophs in the surface layer. Ten different cyanobacterial populations were detected with confocal laser scanning microscopy: six filamentous species, with Microcoleus chthonoplastes and Halomicronema excentricum as dominant (73% of total counts); and four unicellular types affiliated to Microcystis, Chroococcus, Gloeocapsa, and Synechocystis (27% of total counts). Denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA gene fragments confirmed the presence of Microcoleus, Oscillatoria, and Leptolyngbya strains (Halomicronema was not detected here) and revealed additional presence of Phormidium, Pleurocapsa and Calotrix types. Spectral scalar irradiance measurements did not reveal a particular zonation of cyanobacteria, purple or green bacteria in the first millimeter of the mat. Terminal-restriction fragment length polymorphism analysis of PCR-amplified 16S rRNA gene fragments of bacteria depicted the community composition and a fine-scale depth-distribution of at least five different populations of anoxygenic phototrophs and at least three types of sulfate-reducing bacteria along the microgradients of oxygen and light inside the microbial mat.     

Sulfide and pH effects on variable fluorescence of photosystem II in two strains of the cyanobacterium Oscillatoria amphigranulata

Changes in fluorescence of photosystem II (PS II) chlorophyll were used to monitor the in vivo effects of sulfide and pH on photosynthesis by the cyanobacterium Oscillatoria amphigranulata. O. amphigranulata is capable of both oxygenic photosynthesis and sulfide dependent anoxygenic photosynthesis. A genetic variant of O. amphigranulata which photosynthesizes oxygenically at normal rates, but is incapable of anoxygenic photosynthesis and cannot tolerate sulfide, was also used to explore the mode of action of sulfide. In vivo fluorescence responses of PS II chlorophyll in the first few seconds of exposure to light (Kautsky transients) reflected the electrochemical states of PS II and associated electron donors and acceptors. Kautsky transients showed a distinct difference between PS II of the wild type and the variant, but sulfide lowered fluorescence in both. Kautsky transients with sulfide were similar to transients with addition of NH₂OH, NH₄ ⁺ or HCN, indicating sulfide interacts with a protein on the donor side of PS II. The fluorescence steady-state (after 2 min) was measured in the presence of sulfide, cyanide and ammonium with pH ranging from 7.2–8.7. Sulfide and cyanide had the most impact at pH 7.2, ammonium at pH 8.7. This suggests that the uncharged forms (HCN, NH₃ and H₂S) had the strongest effect on PS II, possibly because of increased membrane permeability.Abbreviations DCMU 3(3,4-dichlorophenyl)-1,1-dimethyl-urea - Oa-wt Oscillatoria amphigranulata (wild type) - Oa-2 Oscillatoria amphigranulata (genetic variant)     

Transition from Anoxygenic to Oxygenic Photosynthesis in a Microcoleus chthonoplastes Cyanobacterial Mat

Benthic cyanobacterial mats with the filamentous Microcoleus chthonoplastes as the dominant phototroph grow in oxic hypersaline environments such as Solar Lake, Sinai. The cyanobacteria are in situ exposed to chemical variations between 200 μmol of sulfide liter⁻¹ at night and 1 atm pO₂ during the day. During experimental H₂S to O₂ transitions the microbial community was shown to shift from anoxygenic photosynthesis, with H₂S as the electron donor, to oxygenic photosynthesis. Microcoleus filaments could carry out both types of photosynthesis concurrently. Anoxygenic photosynthesis dominated at high sulfide levels, 500 μmol liter⁻¹, while the oxygenic reaction became dominant when the sulfide level was reduced below 100 to 300 μmol liter⁻¹ (25 to 75 μmol of H₂S liter⁻¹). An increasing inhibition of the oxygenic photosynthesis was observed upon transition to oxic conditions from increasing sulfide concentrations. Oxygen built up within the Microcoleus layer of the mat even under 5 mmol of sulfide liter⁻¹ (500 μmol of H₂S liter⁻¹) in the overlying water. The implications of such a localized O₂ production in a highly reducing environment are discussed in relation to the evolution of oxygenic photosynthesis during the Proterozoic era.     

Anaerobic heterotrophic dark metabolism in the cyanobacterium Oscillatoria limnetica: Sulfur respiration and lactate fermentation

The cyanobacterium Oscillatoria limnetica, capable of anoxygenic photosynthesis in the light with sulfide as electron donor can anaerobically break down its intracellular polyglucose in the dark. In the absence of elemental sulfur, the organism carries out lactate fermentation; in its presence, anaerobic respiration occurs in which sulfur is reduced to sulfide. Induction of anoxygenic photosynthesis or synthesis of new proteins is not necessary for either process. Cells adapted in the dark to sulfur reduction are capable of anoxygenic photosynthesis during a subsequent light period, unless protein synthesis has been inhibited during the dark incubation period.Abbreviations DCMU 3-(3,4-dichlorophenyl)-1,1-dimethylurea - FCCP Carbonylcyanide p-trifluoromethoxyphenylhydrazone - mgat milligramatom - OD optical density     

Monitoring of oxygenic and anoxygenic photosynthesis in a unicyanobacterial biofilm, grown in benthic gradient chamber

In order to assess the role of cyanobacteria in the formation and dynamics of microenvironments in microbial mats, we studied an experimental biofilm of a benthic, halotolerant strain, belonging to the Halothece cluster of cyanobacteria. The 12-week-old biofilm developed in a sand core incubated in a benthic gradient chamber under opposing oxygen and sulfide vertical concentration gradients. At the biofilm surface, and as a response to high light irradiances, specific accumulation of myxoxanthophyll was detected in the cells, consistent with the typical vertical distribution of sun versus shade species in nature. The oxygen turn-over in terms of gross photosynthesis and net productivity rates was comparable to oxygen dynamics in natural microbial mats. Sulfide blocked O(2) production at low irradiances in deep biofilm layers but the dynamics of H(2)S and pH demonstrated that sulfide removal by anoxygenic photosynthesis was taking place. At higher irradiances, as soon as H(2)S was depleted, the cells switched to oxygenic photosynthesis as has been postulated for natural communities. The similarities between this experimental biofilm and natural benthic microbial mats demonstrate the central role of cyanobacteria in shaping microenvironmental gradients and processes in other complex microbial communities.     

Distribution of phototrophic microbes in the flat laminated microbial mat at Laguna Figueroa, Baja California, Mexico

The microbial mat community in the saltmarsh/evaporate flat interface at Laguna Figueroa involved in the deposition of laminated sediments was investigated. Pigment analysis, light microscopy and transmission electron microscopy were used to determine the relative abundance and distribution of phototrophic species. The community is vertically stratified into four distinct phototrophic populations. The layering could be distinguished by pigment and species composition. The two layers closest to the surface contained mostly oxygenic phototrophs and chlorophyll a as the primary photosynthetic pigment. Anoxic phototrophs predominated in the bottom two layers with bacteriochlorophylls a and c in the third layer and bacteriochlorophyll a and b in the bottom layer. The surface yellow layer was composed primarily of Navicula, Rhopalodia and other diatom species as well as the cyanobacteria Aphanothece sp. and Phormidium sp. Microcoleus chthonoplasces and Chroococcidiopsis sp. were the major cyanobacteria in the green colored second layer. In the third layer, pinkish-purple in color, purple photographs (Chromatium sp., Thiocapsa roseoparsicina) and filamentous green phototrophs (Chloroflexus sp., Oscillochloris sp.) were abundant. The fourth and deepest photosynthetic layer was salmon colored and composed primarily of Thiocapsa pfennigii, and other purple sulfur phototrophs. The pattern of alternating light (oxygenic community) and dark (anoxygenic community) layering preserved in older laminae is a consequence of this community structure. Study of the flat laminated mat over the 10-year period (1978-1988) including and after its destruction by catastrophic flooding events in 1978 and 1980, showed a succession of stratified communities culminating in the return of Microcoleus and the full compliment of layers by the fall of 1984.