Variation in Sulfide Tolerance of Photosystem II in Phylogenetically Diverse Cyanobacteria from Sulfidic Habitats

Abstract

Physiological and molecular phylogenetic approaches were used to investigate variation among 12 cyanobacterial strains in their tolerance of sulfide, an inhibitor of oxygenic photosynthesis. Cyanobacteria from sulfidic habitats were found to be phylogenetically diverse and exhibited an approximately 50-fold variation in photosystem II performance in the presence of sulfide. Whereas the degree of tolerance was positively correlated with sulfide levels in the environment, a strain's phenotype could not be predicted from the tolerance of its closest relatives. These observations suggest that sulfide tolerance is a dynamic trait primarily shaped by environmental variation. Despite differences in absolute tolerance, similarities among strains in the effects of sulfide on chlorophyll fluorescence induction indicated a common mode of toxicity. Based on similarities with treatments known to disrupt the oxygen-evolving complex, it was concluded that sulfide toxicity resulted from inhibition of the donor side of photosystem II.Understanding how evolutionary processes, environmental variation, and geography shape the distribution of genetic and ecological diversity of microorganisms is a fundamental challenge in microbial ecology. Cyanobacteria provide an excellent natural system for investigating the evolution of ecological differences, because these oxygenic phototrophs have diversified to exploit a wide variety of aquatic and terrestrial environments, including hot springs, polar ponds, hot and cold deserts, and hypersaline lagoons (38). By combining physiological experiments with molecular phylogenetics, it has become possible to study the origins of this ecological variation within an evolutionary framework. This integration of approaches has been used to identify several examples of the physiological adaptation of unique cyanobacterial lineages in response to major environmental variables, including salinity (14), light (25), and temperature (23).Another key variable that can vary greatly across cyanobacterial habitats is sulfide, an inhibitor of oxygenic photosynthesis (27). While it is absent from stably oxygenated environments, sulfide is either permanently or periodically present in many ecosystems where cyanobacteria are found, as a result of its presence in source water and/or biological sulfate reduction. These include benthic microbial mat communities that are commonly found in hot springs and both hypersaline and marine sediments (29). Cyanobacteria likewise vary in sulfide tolerance, and strains that typically are not exposed to sulfide in nature, including most planktonic and heterocystous cyanobacteria, are extremely sensitive to and are irreversibly poisoned by this toxin (6,10,15,27). In contrast, those from sulfidic habitats exhibit one or more adaptations for maintaining their photoautotrophic metabolism under such conditions. These include the maintenance of oxygenic photosynthesis by the resistance of photosystem (PS) II to sulfide (6, 10) and the ability to perform PS II-independent, anoxygenic pho...

Unexpected Diversity and Complexity of the Guerrero Negro Hypersaline Microbial Mat

“…6D). The depth location of the association and physiological experiments (9) have suggested a cometabolism of sulfur: the Chloroflexi bacteria may draw down levels of H 2 S stressful for the cyanobacterium (38), which excretes organic carbon used by the Chloroflexi bacteria. However, we observed that M. chthonoplastes filaments were often disrupted when Chloroflexi bacteria were present (Fig.…”

“…All profiles were made within the same 0.25-m 2 area from which the mat cores were taken. The Clark-type oxygen microelectrode and amperometric sulfide microelectrode were calibrated as previously described (3,38). A three-point calibration (pHs 4, 7, and 10) was performed for the pH microelectrode.…”

Influence of hydrogen sulfide on the composition of cell wall proteins of Saccharomyces cerevisiae yeast

“…Встановлено, що в порівняно невисоких концентраціях він пригнічує лю-мінесценцію в бактерій Vibrio fischeri (більше 0,1 мМ) [21], оксигенний фотосинтез у ціанобактерій (від 5 мкМ) [14,15,24]. Гідроген сульфід знижує швидкість погли-нання кисню, що може свідчити про інгібування дихального метаболізму цією спо-лукою, та пригнічує активність ізоцитратдегідрогенази (КФ 1.1.1.41) у клітинах дріжджів Saccharomyces cerevisiae та Pichia guilliermondii [1].…”

Periodic sulfide irruptions impact microbial community structure and diversity in the water column of a hypersaline lake

“…Because water samples collected in the present study were pre-filtered (20 µm), filamentous and larger-celled Cyanobacteria may have been excluded in samples used for PCR amplification. Although sulfide can inhibit oxygenic photosynthesis, sulfide tolerance of Cyanobacteria is shaped to some degree by environmental exposure (Miller & Bebout 2004), and sulfide may also be utilized during anoxygenic growth, thus contributing to the oxidation of sulfide in some environments (Luo & Mitsui 1996). Another consequence of increased Cyanobacteria abundance after sulfide irruption events may be elevated exposure of bird populations to cyanotoxins (i.e.…”