Cyanobacteria in Sulfidic Spring Microbial Mats Can Perform Oxygenic and Anoxygenic Photosynthesis Simultaneously during an Entire Diurnal Period

Abstract

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.

Mercury geochemistry and microbial diversity in meromictic Glacier Lake, Jamesville, NY

“…Facultative anoxygenic photosynthesis in the presence of sulphidic conditions has been documented, however, in several genera of cyanobacteria (Klatt et al . ; Grim and Dick ; Nagy et al . ; Garlick et al .…”

“…While most Chlorobi are known obligate anoxygenic phototrophs, Synechococcus is generally abundant in oxic conditions. Facultative anoxygenic photosynthesis in the presence of sulphidic conditions has been documented, however, in several genera of cyanobacteria (Klatt et al 2016;Grim and Dick 2016;Fig. 2.…”

Oxygenic and anoxygenic photosynthesis in a microbial mat from an anoxic and sulfidic spring

“…Most in situ radiation is between 500 and 600 nm, a wavelength range that forms a minimum in the photosynthetic action spectrum of both oxygenic and anoxygenic phototrophs (McConnell et al ., ; Falkowski and Raven, ). Cyanobacteria use the accessory pigments phycoerythrin, phycocyanin and allophycocyanin (Klatt, ) to harvest radiation in the 500–650 nm range (Nichols and Bogorad, ; Glazer, ). The found antennae pigment isorenieratene allow the GSB to harvest radiation between 350 and 500 nm (Overmann et al ., ) which overlaps somewhat with the light quality we observed.…”

“…Multicellular organisms developed following the GOE and as a result, mats became limited to the uncommon environments where grazers are excluded. The most intensively investigated mats are found in hypersaline or hot environments (Stolz and Margulis, ; Bateson and Ward, ; Jørgensen and Des Marais, ; Canfield and Des Marais, ; Ferris et al ., ; Ramsing et al ., ; Wieland and Kühl, ; Hoehler et al ., ; Nübel et al ., ; Wieland et al ., ; Klatt, ). More recently, an interest has developed for hypoxic or anoxic environments at the bottom of sinkholes that are influenced by seeping groundwater (Hamilton et al ., ; Voorhies et al ., ).…”

“…A recent study (Hamilton et al ., ) showed that these are dominated by Cyanobacteria and GSB ( Chlorobium spp). Remarkably, the most common Cyanobacteria could be cultivated and several of its physiological characteristics were determined, showing that they can perform both oxygenic photosynthesis and anoxygenic photosynthesis and that sulfide inhibits oxygenic photosynthesis (Klatt, ). Our aim was to assess if these characteristics are reflected in the behavior of the consortium from which they were isolated.…”