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Versatile cyanobacteria control the timing and extent of sulfide production in a Proterozoic analog microbial mat.

ABSTRACT: Cyanobacterial mats were hotspots of biogeochemical cycling during the Precambrian. However, mechanisms that controlled O₂ release by these ecosystems are poorly understood. In an analog to Proterozoic coastal ecosystems, the Frasassi sulfidic springs mats, we studied the regulation of oxygenic and sulfide-driven anoxygenic photosynthesis (OP and AP) in versatile cyanobacteria, and interactions with sulfur reducing bacteria (SRB). Using microsensors and stable isotope probing we found that dissolved organic carbon (DOC) released by OP fuels sulfide production, likely by a specialized SRB population. Increased sulfide fluxes were only stimulated after the cyanobacteria switched from AP to OP. O₂ production triggered migration of large sulfur-oxidizing bacteria from the surface to underneath the cyanobacterial layer. The resultant sulfide shield tempered AP and allowed OP to occur for a longer duration over a diel cycle. The lack of cyanobacterial DOC supply to SRB during AP therefore maximized O₂ export. This mechanism is unique to benthic ecosystems because transitions between metabolisms occur on the same time scale as solute transport to functionally distinct layers, with the rearrangement of the system by migration of microorganisms exaggerating the effect. Overall, cyanobacterial versatility disrupts the synergistic relationship between sulfide production and AP, and thus enhances diel O₂ production.

SUBMITTER: Klatt JM

PROVIDER: S-EPMC7784965 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Versatile cyanobacteria control the timing and extent of sulfide production in a Proterozoic analog microbial mat.

Klatt Judith M JM Gomez-Saez Gonzalo V GV Meyer Steffi S Ristova Petra Pop PP Yilmaz Pelin P Granitsiotis Michael S MS Macalady Jennifer L JL Lavik Gaute G Polerecky Lubos L Bühring Solveig I SI

The ISME journal 20200807 12

Cyanobacterial mats were hotspots of biogeochemical cycling during the Precambrian. However, mechanisms that controlled O<sub>2</sub> release by these ecosystems are poorly understood. In an analog to Proterozoic coastal ecosystems, the Frasassi sulfidic springs mats, we studied the regulation of oxygenic and sulfide-driven anoxygenic photosynthesis (OP and AP) in versatile cyanobacteria, and interactions with sulfur reducing bacteria (SRB). Using microsensors and stable isotope probing we found ...[more]

PMID: 32770117

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Project description:Multiple sulphur (S) isotope ratios are powerful proxies to understand the complexity of S biogeochemical cycling through Deep Time. The disappearance of a sulphur mass-independent fractionation (S-MIF) signal in rocks <~2.4 Ga has been used to date a dramatic rise in atmospheric oxygen levels. However, intricacies of the S-cycle before the Great Oxidation Event remain poorly understood. For example, the isotope composition of coeval atmospherically derived sulphur species is still debated. Furthermore, variation in Archaean pyrite δ34 S values has been widely attributed to microbial sulphate reduction (MSR). While petrographic evidence for Archaean early-diagenetic pyrite formation is common, textural evidence for the presence and distribution of MSR remains enigmatic. We combined detailed petrographic and in situ, high-resolution multiple S-isotope studies (δ34 S and Δ33 S) using secondary ion mass spectrometry (SIMS) to document the S-isotope signatures of exceptionally well-preserved, pyritised microbialites in shales from the ~2.65-Ga Lokammona Formation, Ghaap Group, South Africa. The presence of MSR in this Neoarchaean microbial mat is supported by typical biogenic textures including wavy crinkled laminae, and early-diagenetic pyrite containing <26‰ μm-scale variations in δ34 S and Δ33 S = -0.21 ± 0.65‰ (±1σ). These large variations in δ34 S values suggest Rayleigh distillation of a limited sulphate pool during high rates of MSR. Furthermore, we identified a second, morphologically distinct pyrite phase that precipitated after lithification, with δ34 S = 8.36 ± 1.16‰ and Δ33 S = 5.54 ± 1.53‰ (±1σ). We propose that the S-MIF signature of this secondary pyrite does not reflect contemporaneous atmospheric processes at the time of deposition; instead, it formed by the influx of later-stage sulphur-bearing fluids containing an inherited atmospheric S-MIF signal and/or from magnetic isotope effects during thermochemical sulphate reduction. These insights highlight the complementary nature of petrography and SIMS studies to resolve multigenerational pyrite formation pathways in the geological record.

Dataset Information

Versatile cyanobacteria control the timing and extent of sulfide production in a Proterozoic analog microbial mat.

Publications

Versatile cyanobacteria control the timing and extent of sulfide production in a Proterozoic analog microbial mat.

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