With a pinch of salt: metagenomic insights into Namib Desert salt pan microbial mats and halites reveal functionally adapted and competitive communities

Abstract

ABSTRACT Salt pans or playas, which are saline-rich springs surrounded by halite evaporates in arid environments, have played an essential role in landscape erosion during the formation of the Namib Desert and are numerous in its central region. In this study, we used shotgun metagenomics to investigate the phylogenetic and functional capacities of the microbial communities from two salt pans (namely, Eisefeld and Hosabes) located in central Namib Desert, located in Southwest Africa. We studied the source and sink sediment mat communities of the saline streams, as well as those from two halites (crystallized structures on the stream margins). The microbial assemblages and potential functions were distinct in both niches. Independently from their localization (Eisfeld vs Hosabes and source vs sink), the sediment mat communities were dominated by members of the Alpha- and Gamma-proteobacteria classes, while halites were Archaea dominated and also contained high abundances of the extremely halophilic bacterium Salinibacter sp. (phylum Bacteroidota ). Photoheterotrophy and chemoheterotrophy were the principal lifestyles in both niches, with halite communities having a reduced diversity of metabolic pathways. Intense microbial-virus interactions in both niches were implied by the widespread detection of CRISPR-Cas defense systems. We identified a putatively novel clade of type II CRISPR-Cas systems, as well as novel candidate viral lineages of the class Caudoviricetes and of Halobacteriales - infecting haloviruses. Putative gene transfer agent-like sequences within the Alphaproteobacteria were identified in the sediment mat communities. These horizontal gene transfer elements have the potential to drive genome plasticity and evolution of the Alphaproteobacteria in the Namib Desert salt pan microbiomes. IMPORTANCE The hyperarid Namib Desert is one of the oldest deserts on Earth. It contains multiple clusters of playas which are saline-rich springs surrounded by halite evaporites. Playas are of great ecological importance, and their indigenous (poly)extremophilic microorganisms are potentially involved in the precipitation of minerals such as carbonates and sulfates and have been of great biotechnological importance. While there has been a considerable amount of microbial ecology research performed on various Namib Desert edaphic microbiomes, little is known about the microbial communities inhabiting its multiple playas. In this work, we provide a comprehensive taxonomic and functional potential characterization of the microbial, including viral, communities of sediment mats and halites from two distant salt pans of the Namib Desert, contributing toward a better understanding of the ecology of this biome.