Assessment of the stoichiometry and efficiency of CO2 fixation coupled to reduced sulfur oxidation

Chemolithoautotrophic sulfur oxidizing bacteria (SOB) couple the oxidation of reduced sulfur compounds to the production of biomass. Their role in the cycling of carbon, sulfur, oxygen, and nitrogen is, however, difficult to quantify due to the complexity of sulfur oxidation pathways. We describe a generic theoretical framework for linking the stoichiometry and energy conservation efficiency of autotrophic sulfur oxidation while accounting for the partitioning of the reduced sulfur pool between the energy generating and energy conserving steps as well as between the main possible products (sulfate vs. zero-valent sulfur). Using this framework, we show that the energy conservation efficiency varies widely among SOB with no apparent relationship to their phylogeny. Aerobic SOB equipped with reverse dissimilatory sulfite reductase tend to have higher efficiency than those relying on the complete Sox pathway, whereas for anaerobic SOB the presence of membrane-bound, as opposed to periplasmic, nitrate reductase systems appears to be linked to higher efficiency. We employ the framework to also show how limited rate measurements can be used to estimate the primary productivity of SOB without the knowledge of the sulfate-to-zero-valent-sulfur production ratio. Finally, we discuss how the framework can help researchers gain new insights into the activity of SOB and their niches

Cyanobacteria in sulfidic spring microbial mats can perform oxygenic and anoxygenic photosynthesis simultaneously during an entire diurnal period

We used microsensors to study the regulation of oxygenic and anoxygenic photosynthesis by light and sulfide in a cyanobacterium dominating microbial mats from cold sulfidic springs. Both photosynthetic modes were performed simultaneously over all H2S concentrations (1–2200 µM) and irradiances (4–52 µmol photons m-2 s-1) tested. Anoxygenic photosynthesis increased with H2S concentration while the sum of oxygenic and anoxygenic photosynthetic rates was constant at each light intensity. Thus, the total photosynthetically driven electron transport rate was solely controlled by the irradiance level. The partitioning between the rates of these two photosynthetic modes was regulated by both light and H2S concentration. The plastoquinone pool (PQ) receives electrons from sulfide:quinone:reductase (SQR) in anoxygenic photosynthesis and from photosystem II (PSII) in oxygenic photosynthesis. It is thus the link in the electron transport chain where both pathways intersect, and the compound that controls their partitioning. We fitted our data with a model of the photosynthetic electron transport that includes the kinetics of plastoquinone reduction and oxidation. The model results confirmed that the observed partitioning between photosynthetic modes can be explained by a simple kinetic control based on the affinity of SQR and PSII towards PQ. The SQR enzyme and PSII have similar affinities towards PQ, which explains the concurrent oxygenic and anoxygenic photosynthesis over an astonishingly wide range of H2S concentrations and irradiances. The elegant kinetic control of activity makes the cyanobacterium successful in the fluctuating spring environment. We discuss how these specific regulation mechanisms may have played a role in ancient H2S-rich oceans

Assessment of the stoichiometry and efficiency of CO2 fixation coupled to reduced sulfur oxidation

Chemolithoautotrophic sulfur oxidizing bacteria (SOB) couple the oxidation of reduced sulfur compounds to the production of biomass. Their role in the cycling of carbon, sulfur, oxygen and nitrogen is, however, difficult to quantify due to the complexity of sulfur oxidation pathways. We describe a generic theoretical framework for linking the stoichiometry and energy conservation efficiency of autotrophic sulfur oxidation while accounting for the partitioning of the reduced sulfur pool between the energy generating and energy conserving steps as well as between the main possible products (sulfate versus elemental sulfur). Using this framework, we show that the energy conservation efficiency varies widely among SOB with no apparent relationship to their phylogeny. Aerobic SOB equipped with reverse dissimilatory sulfite reductase tend to have higher efficiency than those relying on the complete Sox pathway, whereas for anaerobic SOB the presence of membrane-bound, as opposed to periplasmic, nitrate reductase systems appears to be linked to higher efficiency. We employ the framework to also show how limited rate measurements can be used to estimate the primary productivity of SOB without the knowledge of the sulfate-to-elemental-sulfur production ratio. Finally, we discuss how the framework can help researchers gain new insights into the activity of SOB and their niches

Cyanobacteria in sulfidic spring microbial mats can perform oxygenic and anoxygenic photosynthesis simultaneously during an entire diurnal period

We used microsensors to study the regulation of anoxygenic and oxygenic photosynthesis (AP and OP, respectively) by light and sulfide in a cyanobacterium dominating microbial mats from cold sulfidic springs. Both photosynthetic modes were performed simultaneously over all H2S concentrations (1–2200 μM) and irradiances (4–52 μmol photons m-2 s-1) tested. AP increased with H2S concentration while the sum of oxygenic and anoxygenic photosynthetic rates was constant at each light intensity. Thus, the total photosynthetically driven electron transport rate was solely controlled by the irradiance level. The partitioning between the rates of these two photosynthetic modes was regulated by both light and H2S concentration. The plastoquinone pool (PQ) receives electrons from sulfide:quinone:reductase (SQR) in AP and from photosystem II (PSII) in OP. It is thus the link in the electron transport chain where both pathways intersect, and the compound that controls their partitioning. We fitted our data with a model of the photosynthetic electron transport that includes the kinetics of plastoquinone reduction and oxidation. The model results confirmed that the observed partitioning between photosynthetic modes can be explained by a simple kinetic control based on the affinity of SQR and PSII toward PQ. The SQR enzyme and PSII have similar affinities toward PQ, which explains the concurrent OP and AP over an astonishingly wide range of H2S concentrations and irradiances. The elegant kinetic control of activity makes the cyanobacterium successful in the fluctuating spring environment. We discuss how these specific regulation mechanisms may have played a role in ancient H2S-rich oceans

Data_Sheet_1_Low-Light Anoxygenic Photosynthesis and Fe-S-Biogeochemistry in a Microbial Mat.DOCX

<p>We report extremely low-light-adapted anoxygenic photosynthesis in a thick microbial mat in Magical Blue Hole, Abaco Island, The Bahamas. Sulfur cycling was reduced by iron oxides and organic carbon limitation. The mat grows below the halocline/oxycline at 30 m depth on the walls of the flooded sinkhole. In situ irradiance at the mat surface on a sunny December day was between 0.021 and 0.084 μmol photons m^-2 s^-1, and UV light (<400 nm) was the most abundant part of the spectrum followed by green wavelengths (475–530 nm). We measured a light-dependent carbon uptake rate of 14.5 nmol C cm^-2 d^-1. A 16S rRNA clone library of the green surface mat layer was dominated (74%) by a cluster (>97% sequence identity) of clones affiliated with Prosthecochloris, a genus within the green sulfur bacteria (GSB), which are obligate anoxygenic phototrophs. Typical photopigments of brown-colored GSB, bacteriochlorophyll e and (β-)isorenieratene, were abundant in mat samples and their absorption properties are well-adapted to harvest light in the available green and possibly even UV-A spectra. Sulfide from the water column (3–6 μmol L^-1) was the main source of sulfide to the mat as sulfate reduction rates in the mats were very low (undetectable-99.2 nmol cm^-3 d^-1). The anoxic water column was oligotrophic and low in dissolved organic carbon (175–228 μmol L^-1). High concentrations of pyrite (FeS₂; 1–47 μmol cm^-3) together with low microbial process rates (sulfate reduction, CO₂ fixation) indicate that the mats function as net sulfide sinks mainly by abiotic processes. We suggest that abundant Fe(III) (4.3–22.2 μmol cm^-3) is the major source of oxidizing power in the mat, and that abiotic Fe-S-reactions play the main role in pyrite formation. Limitation of sulfate reduction by low organic carbon availability along with the presence of abundant sulfide-scavenging iron oxides considerably slowed down sulfur cycling in these mats.</p

Hydrogen sulfide can inhibit and enhance oxygenic photosynthesis in a cyanobacterium from sulfidic springs

We used microsensors to investigate the combinatory effect of hydrogen sulfide (H2S) and light on oxygenic photosynthesis in biofilms formed by a cyanobacterium from sulfidic springs. We found that photosynthesis was both positively and negatively affected by H2S: (i) H2S accelerated the recovery of photosynthesis after prolonged exposure to darkness and anoxia. We suggest that this is possibly due to regulatory effects of H2S on photosystem I components and/or on the Calvin cycle. (ii) H2S concentrations of up to 210μM temporarily enhanced the photosynthetic rates at low irradiance. Modelling showed that this enhancement is plausibly based on changes in the light-harvesting efficiency. (iii) Above a certain light-dependent concentration threshold H2S also acted as an inhibitor. Intriguingly, this inhibition was not instant but occurred only after a specific time interval that decreased with increasing light intensity. That photosynthesis is most sensitive to inhibition at high light intensities suggests that H2S inactivates an intermediate of the oxygen evolving complex that accumulates with increasing light intensity. We discuss the implications of these three effects of H2S in the context of cyanobacterial photosynthesis under conditions with diurnally fluctuating light and H2S concentrations, such as those occurring in microbial mats and biofilms

Hydrogen sulfide can inhibit and enhance oxygenic photosynthesis in a cyanobacterium from sulfidic springs

We used microsensors to investigate the combinatory effect of hydrogen sulfide (H2S) and light on oxygenic photosynthesis in biofilms formed by a cyanobacterium from sulfidic springs. We found that photosynthesis was both positively and negatively affected by H2S: (i) H2S accelerated the recovery of photosynthesis after prolonged exposure to darkness and anoxia. We suggest that this is possibly due to regulatory effects of H2S on photosystem I components and/or on the Calvin cycle. (ii) H2S concentrations of up to 210μM temporarily enhanced the photosynthetic rates at low irradiance. Modelling showed that this enhancement is plausibly based on changes in the light-harvesting efficiency. (iii) Above a certain light-dependent concentration threshold H2S also acted as an inhibitor. Intriguingly, this inhibition was not instant but occurred only after a specific time interval that decreased with increasing light intensity. That photosynthesis is most sensitive to inhibition at high light intensities suggests that H2S inactivates an intermediate of the oxygen evolving complex that accumulates with increasing light intensity. We discuss the implications of these three effects of H2S in the context of cyanobacterial photosynthesis under conditions with diurnally fluctuating light and H2S concentrations, such as those occurring in microbial mats and biofilms