Archaeal overdominance close to life‐limiting conditions in geothermally influenced hypersaline lakes at the Danakil Depression, Ethiopia

Abstract

T he Dallol protovolcanic area on the Danakil Depres s ion (Afar region, E thiopia) exhibits unique hydrothermal manifes tations in hypers aline context, yielding varied polyextreme phys icochemical conditions . P revious s tudies identified a wide archaeal divers ity in les s extreme brines but failed to identify microorganis ms thriving in either high-chaotropicity, low-wateractivity brines or hyperacidic-hypers aline Na-F e-rich brines . R ecently, we acces s ed s everal s mall lakes under intens e degas s ing activity adjacent to the R ound Mountain, wes t to the Dallol dome (Wes tern C anyon Lakes ; WC L1-5). T hey exhibited intermediate parameter combinations (pH~5, 34-41% NaC l-dominated s alts with relatively high levels of chaotropic Mg-C a s alts ) that s hould allow to better cons train life limits . T hes e lakes were overwhelmingly dominated by Archaea, encompas s ing up to 99% of prokaryotic 16S rR NA gene amplicon s equences in metabarcoding s tudies . T he majority belonged to Halobacteriota and Nanohaloarchaeota, the latter repres enting up to half of prokaryotic s equences . Optical and epifluores cence micros copy s howed active cells in natural s amples and divers e morphotypes in enrichment cultures . S canning electron micros copy coupled with energy-dis pers ive x-ray s pectros copy revealed tiny cells (200-300 nm diameter) epibiotically as s ociated with s omewhat larger cells (0.6-1 µm) but als o the pres ence of s ilica-dominated precipitates of s imilar s ize and s hape, highlighting the difficulty of dis tinguis hing microbes from mineral biomorphs in this kind of low-biomas s s ys tems .

Active Microbial Airborne Dispersal and Biomorphs as Confounding Factors for Life Detection in the Cell-Degrading Brines of the Polyextreme Dallol Geothermal Field

“…Although amplicons could not be produced from a neighboring pond, fluorescent in situ hybridization (FISH) seemingly indicated the specific presence of those archaea ( 57 ). In contrast, in our own 16S rRNA gene PCR amplification studies ( 48 , 51 ), samples from the Black and Yellow lakes and Dallol failed to yield amplicons. Nonetheless, in several cases, after nested PCR reamplification, amplicons were produced from brines but only when first-PCR-negative controls yielded amplicons as well.…”

“…The load of eukaryotes in aerosols seemed to be proportionally higher than in some local extreme ecosystems, as we were unable to amplify eukaryotes from the selected WCLs as well as, in some years, from Gt samples. The latter was possibly due to differences in the cave reservoir level affecting physicochemical parameters and/or in lower sampled volumes (sampled volumes were 5 to 25 L, but they were lower in Gt 2016 and PS samples [ 48 , 51 ]). In the case of Gt 2016 and PS3, where fungal and choanoflagellate sequences appeared dominant in proportion ( Fig.…”

“…This generates diverse hydrothermal manifestations on and around the dome of Dallol. This also influences the local hydrochemistry, leading to unique polyextreme conditions that, depending on the zone, combine hypersalinity (20 to >50% [wt/vol]), low pH (≤0 to 6.0), and high temperature (25 to 108°C) ( 39 , 45 – 51 ).…”

“…Previous studies have unequivocally shown the presence of diverse microbial communities largely dominated by archaea in the hydrothermally influenced Lake Assale, the salt plain at the Dallol dome base, a salt-karst cave reservoir on the Dallol western canyons’ flank, and a series of small lakes located at the base of the Round Mountain (Western Canyon Lakes). These NaCl-dominated ecosystems, with ∼35% salinity, moderate temperature (∼30°C), and moderate pH (∼4 to 6), were largely enriched (85 to 99%) in highly diverse archaea, notably Halobacteriota and Nanohaloarchaeota ( 48 , 51 ). In contrast, various lines of evidence on dozens of samples (cultures, 16S/18S rRNA gene metabarcoding, fluorescence-activated cell sorting, and optical and electron microscopy) failed to unambiguously identify microbial life thriving in two other types of brines in the Dallol area.…”

“…In this study, we aimed at testing whether airborne microbial dispersal and mineral biomorphs, which are observed in many Danakil brines ( 48 , 51 ), are confounding factors leading to the potentially mistaken detection of life in the Dallol ponds. We show not only that aerosols over the dome bear widely diverse cells but also that cells are rapidly destroyed by Dallol brines upon arrival.…”