The environment,diversity and activity of microbial communities in submarine freshwater springs in the Dead Sea

Abstract

The Dead Sea, located at the border between Jordan, Israel and the Palestinian authority is one of the most hypersaline lakes on earth. Its waters contain a total dissolved salt concentration of up to 348 g L-1, which is about 10 times higher than regular sea water. The lake is characterized by elevated concentrations of divalent cations (~2 M Mg2 and ~0.5 M Ca2 ), which, in addition to the high salinity, form an extreme environment where only highly adapted microorganisms can survive. This doctoral thesis describes the environment, diversity and activity of microbial communities in a novel ecosystem of submarine freshwater springs in the Dead Sea. These springs allow for the formation of diverse microbial mats in an otherwise hostile environment. Water chemistry analysis showed that these springs originate from the Judean Group Aquifer. However, their chemistry is altered along the subsurface flow path from the Aquifer to the Dead Sea due to microbial activity, mixing with interstitial brine in the sediment and dissolution and precipitation of minerals. Pyrosequencing of the 16S rRNA gene and community fingerprinting methods revealed that most of the spring sediment community originates from the Dead Sea sediments and not from the spring water. Using a novel salinity mini-sensor and a flume system that simulates the spring water flow into the Dead Sea it was demonstrated in the second study, that microenvironments of reduced salinity are formed in sediments and around rocks in the springs. The presence of microbial mats in these unique microenvironments led to the conclusion that one of the main drivers of the abundant microbial life is a local salinity reduction. However, as shown by flow and salinity microsensor measurements, the locally decreased salinity is unstable due to frequent fluctuations in the spring water flow. Therefore, although the microorganisms inhabiting these environments are exposed to an overall reduced salinity, they have to cope with large and rapid salinity fluctuations in the range of minutes to hours. The results of the third study showed that some of the microbial mats found in the spring area are either dominated by diatoms or unicellular cyanobacteria and are spatially separated. Growth experiments showed that the local salinity reduction is sufficient to allow for growth of these phototrophs, however, the salinity fluctuations directly affect their distribution. This could be deduced from the observation that diatoms and cyanobacteria had different in-vitro recovery rates of photosynthetic activity following rapid salinity shifts. Furthermore, the high energy demand which is expected to result from the salinity fluctuations, limits phototrophic life to shallow water depths, where enough light is available, in this case less than 10 meters. As shown in the fourth study, other microbial mats in the spring ecosystems were dominated by sulfide oxidizing bacteria (SOB), which were fueled by a flux of sulfide from the sediment below. However, sulfate reduction rates (SRR) in the spring surface sediment (<2.8 nmol cm3 day-1), were too low to account for the sulfide flux determined by in situ microsensor measurements. In fact, isotopic analysis of coexisting sulfide and sulfate in the spring water showed that the reduced sulfur compounds are instead produced along the flow path. The sulfide flux, in combination with a locally reduced salinity and O2 supply from the Dead Sea water column are the driving factors for the abundant microbial biomass of SOB encountered in the springs. Microbial mats in the Dead Sea are dominated by different types of microorganisms, ranging from different SOB genera, to cyanobacteria or diatoms. Differences in the availability of light, the mean salinity and the scale of salinity fluctuations at different spots are the main factors determining the dominating community and their spatial distribution. As reduced salinity in the spring ecosystems was shown to play an extremely important role in supporting life, it was surprising to discover that SRR in the Dead Sea sediment were higher than in the less-saline springs (up to 10 nmol cm3 day-1). While this indicates the presence of an unexpectedly active, extremely halophilic community of sulfate reducing bacteria (SRB) in the Dead Sea sediments, it also suggests that the extensive salinity fluctuations within the springs may limit the SRB populations due to the high energetic cost of osmoregulation in the dynamic system. Therefore while this thesis shows that the low salinity environment of the Dead Sea springs is advantageous for microbial life, the fluctuations within the environment bring their own set of challenges.