Abstract
Microbial communities inhabiting the deep-sea salt-saturated anoxic lakes of the Eastern Mediterranean operate under harsh physical-chemical conditions that are incompatible with the lifestyle of common marine microorganisms. Here, we investigated a stable three-component microbial consortium obtained from the brine of the recently discovered deep-sea salt-saturated Lake Thetis. The trophic network of this consortium, established at salinities up to 240, relies on fermentative decomposition of common osmoprotectant glycine betaine (GB). Similarly to known extreme halophilic anaerobic GB-degrading enrichments, the initial step of GB degradation starts with its reductive cleavage to trimethylamine and acetate, carried out by the fermenting member of the Thetis enrichment, Halobacteroides lacunaris TB21. In contrast to acetate, which cannot be easily oxidized in salt-saturated anoxic environments, trimethylamine represents an advantageous C1-substrate for methylotrophic methanogenic member of the Thetis enrichment, Methanohalophilus sp. TA21. This second member of the consortium likely produces hydrogen via methylotrophic modification of reductive acetyl-CoA pathway because the initial anaerobic GB cleavage reaction requires the consumption of reducing equivalents. Ecophysiological role of the third member of the Thetis consortium, Halanaerobium sp. TB24, which lacks the capability of either GB or trimethylamine degradation, remains yet to be elucidated. As it is true for cultivated members of family Halanaerobiaceae, the isolate TB24 can obtain energy primarily by fermenting simple sugars and producing hydrogen as one of the end products. Hence, by consuming of TB21 and TA21 metabolites, Halanaerobium sp. TB24 can be an additional provider of reducing equivalents required for reductive degradation of GB. Description of the Thetis GB-degrading consortium indicated that anaerobic degradation of osmoregulatory molecules may play important role in the overall turnover of organic carbon in anoxic hypersaline biotopes.
Highlights
Since the discovery on the Mediterranean seabed of two deep-sea hypersaline anoxic lakes (DHALs) [1,2,3], yet more are being discovered and currently there are eight such hydrological formations known [4,5,6]
Was not examined as a result of reductive degradation of glycine betaine (GB) followed by TMA fermentation
Enrichment cultures and no active methanogens were obtained with salinities exceeding 240. This finding neatly corroborates with the upper limit of in vitro salinity reported for growth of all known halophilic methanogenic species isolated from hypersaline sediments [15,18]
Summary
Since the discovery on the Mediterranean seabed of two deep-sea hypersaline anoxic lakes (DHALs) [1,2,3], yet more are being discovered and currently there are eight such hydrological formations known [4,5,6] The surface of these brine lakes lies 3.0–3.5 km below sea level and the salinity of the brines is five to thirteen times higher than that of seawater. The most halophilic and halotolerant aerobic microorganisms meet the osmolarity challenge by synthesis and maintaining high intracellular concentrations of osmoprotectants or compatible solutes that act as osmolytes This type of haloadaptation, known as “salt out” strategy, requires high energetic costs and, limits the number of organisms that can thrive in dark, anoxic, salt-saturated, and energy-impoverished environments where photosynthesis, aerobic respiration, and other highly exergonic processes cannot be operative
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