Biological soil crusts (BSCs) are formed on top of arid soils by specific microbial communities, with filamentous cyanobacteria fixing CO2 and providing a matrix for other BSC microbiota to thrive. Thus, BSC communities contain a variety of microbial clades, many with yet unresolved physiologies and lifestyles. However, the common feature of microorganism inhabiting BSC must be the ability to survive extensive drought periods. The goal of this study was to shed light on the ecophysiology of microorganisms inhabiting BSC in the Negev Desert, Israel, by analyzing their genomic potential by a population-resolved metagenomic approach. We compared the encoded functionalities between the obtained population genomes and, for the most abundant taxon, to genomes of characterized isolates from aquatic environments.Besides a high degree of genomic novelty, the data revealed a previously undescribed metabolic versatility of BSC microorganisms. Several populations apart from cyanobacteria encoded CO2-fixation potential. The potential to utilize various inorganic energy sources such as light, atmospheric gases, and even sulfide was found in several taxa. This potential for auto- and mixotrophy portraits a more complex picture of trophic interactions in BSC than commonly assumed, since the mixotrophic populations appear to be less dependent on the carbon input by cyanobacteria. The encoded persistence strategies encompassed storage compounds accumulation, extensive O2-stress protection, unique DNA repair strategies, and the use of atmospheric gases as energy source. Classic spore formation potential was found only in few populations. Taken together, our data suggests that despite appearing “extreme”, arid BSC environments select for a variety of equally successful metabolic strategies.
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