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Unveiling microbial activities along the halocline of Thetis, a deep-sea hypersaline anoxic basin.

ABSTRACT: Deep-sea hypersaline anoxic basins (DHABs) in the Eastern Mediterranean Sea are considered some of the most hostile environments on Earth. Little is known about the biochemical adaptations of microorganisms living in these habitats. This first metatranscriptome analysis of DHAB samples provides significant insights into shifts in metabolic activities of microorganisms as physicochemical conditions change from deep Mediterranean sea water to brine. The analysis of Thetis DHAB interface indicates that sulfate reduction occurs in both the upper (7.0-16.3% salinity) and lower (21.4-27.6%) halocline, but that expression of dissimilatory sulfate reductase is reduced in the more hypersaline lower halocline. High dark-carbon assimilation rates in the upper interface coincided with high abundance of transcripts for ribulose 1,5-bisphosphate carboxylase affiliated to sulfur-oxidizing bacteria. In the lower interface, increased expression of genes associated with methane metabolism and osmoregulation is noted. In addition, in this layer, nitrogenase transcripts affiliated to uncultivated putative methanotrophic archaea were detected, implying nitrogen fixation in this anoxic habitat, and providing evidence of linked carbon, nitrogen and sulfur cycles.

SUBMITTER: Pachiadaki MG

PROVIDER: S-EPMC4260694 | biostudies-literature | 2014 Dec

REPOSITORIES: biostudies-literature

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Unveiling microbial activities along the halocline of Thetis, a deep-sea hypersaline anoxic basin.

Pachiadaki Maria G MG Yakimov Michail M MM LaCono Violetta V Leadbetter Edward E Edgcomb Virginia V

The ISME journal 20140620 12

Deep-sea hypersaline anoxic basins (DHABs) in the Eastern Mediterranean Sea are considered some of the most hostile environments on Earth. Little is known about the biochemical adaptations of microorganisms living in these habitats. This first metatranscriptome analysis of DHAB samples provides significant insights into shifts in metabolic activities of microorganisms as physicochemical conditions change from deep Mediterranean sea water to brine. The analysis of Thetis DHAB interface indicates ...[more]

PMID: 24950109

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Project description:The deep-sea hypersaline anoxic basins (DHABs) of the Mediterranean (water depth ~3500 m) are some of the most extreme oceanic habitats known. Brines of DHABs are nearly saturated with salt, leading many to suspect they are uninhabitable for eukaryotes. While diverse bacterial and protistan communities are reported from some DHAB haloclines and brines, loriciferans are the only metazoan reported to inhabit the anoxic DHAB brines. Our goal was to further investigate metazoan communities in DHAB haloclines and brines.We report observations from sediments of three DHAB (Urania, Discovery, L'Atalante) haloclines, comparing these to observations from sediments underlying normoxic waters of typical Mediterranean salinity. Due to technical difficulties, sampling of the brines was not possible. Morphotype analysis indicates nematodes are the most abundant taxon; crustaceans, loriciferans and bryozoans were also noted. Among nematodes, Daptonema was the most abundant genus; three morphotypes were noted with a degree of endemicity. The majority of rRNA sequences were from planktonic taxa, suggesting that at least some individual metazoans were preserved and inactive. Nematode abundance data, in some cases determined from direct counts of sediments incubated in situ with CellTracker(TM) Green, was patchy but generally indicates the highest abundances in either normoxic control samples or in upper halocline samples; nematodes were absent or very rare in lower halocline samples. Ultrastructural analysis indicates the nematodes in L'Atalante normoxic control sediments were fit, while specimens from L'Atalante upper halocline were healthy or had only recently died and those from the lower halocline had no identifiable organelles. Loriciferans, which were only rarely encountered, were found in both normoxic control samples as well as in Discovery and L'Atalante haloclines. It is not clear how a metazoan taxon could remain viable under this wide range of conditions.We document a community of living nematodes in normoxic, normal saline deep-sea Mediterranean sediments and in the upper halocline portions of the DHABs. Occurrences of nematodes in mid-halocline and lower halocline samples did not provide compelling evidence of a living community in those zones. The possibility of a viable metazoan community in brines of DHABs is not supported by our data at this time.

Project description:The adaptation of sporeformers to extreme environmental conditions is frequently questioned due to their capacity to produce highly resistant endospores that are considered as resting contaminants, not representing populations adapted to the system. In this work, in order to gain a better understanding of bacterial adaptation to extreme habitats, we investigated the phenotypic and genomic characteristics of the halophile Virgibacillus sp. 21D isolated from the seawater-brine interface (SBI) of the MgCl2-saturated deep hypersaline anoxic basin Discovery located in the Eastern Mediterranean Sea. Vegetative cells of strain 21D showed the ability to grow in the presence of high concentrations of MgCl2, such as 14.28% corresponding to 1.5 M. Biolog phenotype MicroArray (PM) was adopted to investigate the strain phenotype, with reference to carbon energy utilization and osmotic tolerance. The strain was able to metabolize only 8.4% of 190 carbon sources provided in the PM1 and PM2 plates, mainly carbohydrates, in accordance with the low availability of nutrients in its habitat of origin. By using in silico DNA-DNA hybridization the analysis of strain 21D genome, assembled in one circular contig, revealed that the strain belongs to the species Virgibacillus dokdonensis. The genome presented compatible solute-based osmoadaptation traits, including genes encoding for osmotically activated glycine-betaine/carnitine/choline ABC transporters, as well as ectoine synthase enzymes. Osmoadaptation of the strain was then confirmed with phenotypic assays by using the osmolyte PM9 Biolog plate and growth experiments. Furthermore, the neutral isoelectric point of the reconstructed proteome suggested that the strain osmoadaptation was mainly mediated by compatible solutes. The presence of genes involved in iron acquisition and metabolism indicated that osmoadaptation was tailored to the iron-depleted saline waters of the Discovery SBI. Overall, both phenomics and genomics highlighted the potential capability of V. dokdonensis 21D vegetative cells to adapt to the environmental conditions in Discovery SBI.

Dataset Information

Unveiling microbial activities along the halocline of Thetis, a deep-sea hypersaline anoxic basin.

Publications

Unveiling microbial activities along the halocline of Thetis, a deep-sea hypersaline anoxic basin.

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