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, 12 (6), 1414-1426

Life on the Edge: Active Microbial Communities in the Kryos MgCl 2-brine Basin at Very Low Water Activity

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Life on the Edge: Active Microbial Communities in the Kryos MgCl 2-brine Basin at Very Low Water Activity

Lea Steinle et al. ISME J.

Abstract

The Kryos Basin is a deep-sea hypersaline anoxic basin (DHAB) located in the Eastern Mediterranean Sea (34.98°N 22.04°E). It is filled with brine of re-dissolved Messinian evaporites and is nearly saturated with MgCl2-equivalents, which makes this habitat extremely challenging for life. The strong density difference between the anoxic brine and the overlying oxic Mediterranean seawater impedes mixing, giving rise to a narrow chemocline. Here, we investigate the microbial community structure and activities across the seawater-brine interface using a combined biogeochemical, next-generation sequencing, and lipid biomarker approach. Within the interface, we detected fatty acids that were distinctly 13C-enriched when compared to other fatty acids. These likely originated from sulfide-oxidizing bacteria that fix carbon via the reverse tricarboxylic acid cycle. In the lower part of the interface, we also measured elevated rates of methane oxidation, probably mediated by aerobic methanotrophs under micro-oxic conditions. Sulfate reduction rates increased across the interface and were highest within the brine, providing first evidence that sulfate reducers (likely Desulfovermiculus and Desulfobacula) thrive in the Kryos Basin at a water activity of only ~0.4 Aw. Our results demonstrate that a highly specialized microbial community in the Kryos Basin has adapted to the poly-extreme conditions of a DHAB with nearly saturated MgCl2 brine, extending the known environmental range where microbial life can persist.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
a Overview map of DHABs in the Eastern Mediterranean. The position of the Kryos Basin is indicated with a red star, the other basins with green dots. b Bathymetry of the Kryos Basin and the adjacent seafloor (resolution = 30 m). The extent of the Kryos brine basin is delimited with a dark orange line, and the depth of the basin is indicated by the colored scale bar
Fig. 2
Fig. 2
Scheme for high-resolution sampling across the seawater–brine interface with Niskin Bottles. Interface sampling was conducted during very calm weather conditions with minimal pitch/roll of the ship, preventing erratic up and down movement of the water sampler. The strong density difference impeded mixing of seawater and brine in the closed Niskin bottles during recovery. Immediately upon recovery, each Niskin bottle was sampled repeatedly (5–7 cycles) for different parameters resulting in a vertical resolution of the water column of ~20 cm. Vertical depth profiles were aligned based on chlorinity. Separate bottles were taken for 16S rRNA and biomarker analyses
Fig. 3
Fig. 3
Geochemical profiles and rate measurements across the seawater–brine interface. Concentrations of a chloride (filled symbols) and sulfate (open symbols), b magnesium (filled symbols) and sodium (open symbols), c oxygen, d ammonium (filled symbols) and sulfide (open symbols), and e methane. f Isotopic composition of methane −δD (filled symbols) and δ13C (open symbols). Rates of g sulfate reduction (SR), and h methane oxidation (MOx). i Fraction of oxidized methane-C incorporated into biomass. Values in af represent single measurements. Error bars in gi represent standard deviations of quadruplicates. The dashed horizontal line indicates the border between upper and lower interface, and the continuous horizontal line the beginning of the brine. Note the different depth scales for the interface and brine. We vertically resolved the interface with four, substantially overlapping Niskin bottle samplings (represented by different symbols: circle, square, upward-, and downward triangle). The profiles from these bottles were aligned based on chlorinity
Fig. 4
Fig. 4
Relative abundances of bacterial and archaeal genera and unclassified clades in the Kryos brine and interface based on sequencing of 16S RNA genes (V3–V4 region for Bacteria, V3-V6 region for Archaea). Taxonomy is based on SILVAngs, release 123.1. Sequence abundances are given in per cent of total classified Bacteria and Archaea, respectively. Only taxa that made up >1% of total archaeal or bacterial sequences in any given sample are shown. Archaeal sequence abundances shown in this figure are based on unassembled reverse sequence reads. Forward reads showed a nearly congruent community composition
Fig. 5
Fig. 5
Fatty-acid fingerprints across the seawater–brine interface. Fractional abundance (black bars) and compound-specific δ13C-values (diamonds, gray line) of fatty acids (C14—C22) from a the seawater, b the upper interface, c the lower interface, and d the brine. The fingerprint comprised fatty acids with methyl groups at the iso (i) or anteiso (ai) position, or at carbon atom position 10 (10 Me). In several cases, we could not determine the position of the methyl branch in the alkyl chain. Chain isomerism was then denoted by sequential numbers in parentheses (e.g., MeC14:0(1) and MeC14:0(2)). Mass traces of C16:1ω8 were detected as DMDS-derivate in interface and brine samples. Concentration-weighted averages of bulk fatty-acid δ13C-values are −28.9‰ (seawater), −29‰ (upper interface), −28.6‰ (lower interface), −26.6‰ (brine)

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