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Unveiling microbial communities along the polyextreme physicochemical gradients of Dallol and its surroundings (Danakil depression, Afar region, Ethiopia)

Abstract : From the vast microbial diversity of the three domains of life, a fraction of microorganisms (in particular some Archaea) have adapted to the most extreme conditions. Since most extreme environments are characterised by multiple stress factors (e.g. hot and acidic hydrothermal springs, saline and alkaline lakes, etc.), some extremophiles are in fact polyextremophiles. Nevertheless, there is no microorganism known to be adapted simultaneously to a very low pH (<1) and high salinity (and possibly high temperature). Either there are no molecular adaptations capable of withstanding certain combinations of pH and salinity, or this absence is related to the rarity of hyperacidic and hypersaline (and hot) environments, leaving them unexplored.The salt desert of the Danakil Depression (Afar region) in Ethiopia lies at the confluence of three tectonic plates in the East African Rift. In the middle of this geologically active zone, the Dallol geothermal dome and its surroundings offer a rare combination of physicochemical parameters, with high salt levels (20 to 78%, rich in Mg2+/Ca2+ or Na+(/Fe2+/3+)) and neutral to negative pH values (~6 to -1.5). Therefore, these sites provide a good model for studying microbial communities along these rare and unique parameter gradients. Over the last four years, we have collected 235 samples (solids, liquids, plankton biomass) from the different sites in and around the Dallol dome. In situ and ex situ physicochemical measurements have enabled us to characterise each environment and estimate its theoretical habitability based on previously known life-limiting conditions. We then proceeded to DNA purification of the samples and amplified and sequenced 16S/18S rRNA genes in order to characterize the microbial diversity, which we compared with databases and classified phylogenetically. We also completed our study by using a flow cytometer (for multiparametric analysis), and microscope observations (optical, scanning electron and confocal laser scanning).Hypersaline (~30% salts, dominated by NaCl) and slightly acidic (pH 4-6) environments showed a very high diversity of microorganisms, dominated by Archaea (at least 80% of the total sequences) in particular Halobacteria and Nanohaloarchaeota, frequently associated in hypersaline environments. We observed that the increase in acidity and salinity was associated with an increase in the proportion of Archaea (especially Nanohaloarchaeota). A better adaptation of halophilic archaea compared to bacteria could explain their prevalence. Concerning nanohaloarchaea, their higher proportion could be linked to their suspected role as haloarchaea ectosymbionts: in the case of a mutualistic relationship, their association could favour the adaptation to more extreme conditions; in the case of a parasitic relationship, the rise of acidity and salinity may weaken the host and increase the parasite prevalence. No trace of microbial life has been found in the most polyextreme environments (salinity 20-78%, pH -1 to 3). For some sites, we interpret that the chaotropicity, water activity and ionic strength values related to the composition and concentration of salts (minimum 50%, rich in Mg2+/Ca2+) are limiting for microbial life. For others, such as the Dallol dome, it could be the combination of hypersalinity and hyperacidity (pH~0) that make it inhospitable, without excluding the possible presence of sterilising chemical compounds. As environments with low or absent biomass are sensitive to biocontamination (local or laboratory), we have also tried to estimate the impact of this biocontamination on the study of the multi-extreme sites of Dallol and its surroundings. We thus propose a rigorous protocol, based on the use of cross-analyses and positive/negative controls in all our experiments in order to separate endogenous and exogenous DNA, and to distinguish cells from abiotic mineral biomorphs in our samples.
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Jodie Belilla. Unveiling microbial communities along the polyextreme physicochemical gradients of Dallol and its surroundings (Danakil depression, Afar region, Ethiopia). Ecosystems. Université Paris-Saclay, 2020. English. ⟨NNT : 2020UPASL043⟩. ⟨tel-03121160⟩

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