How the diverse bacterial communities inhabiting desert soils maintain energy and carbon needs is much debated. Traditionally, most bacteria are thought to persist by using organic carbon synthesized by photoautotrophs following transient hydration events. Recent studies focused on Antarctic desert soils have revealed, however, that some bacteria use atmospheric trace gases, such as hydrogen (H2), to conserve energy and fix carbon independently of photosynthesis. In this study, we investigated whether atmospheric H2 oxidation occurs in four nonpolar desert soils and compared this process to photosynthesis. To do so, we first profiled the distribution, expression, and activities of hydrogenases and photosystems in surface soils collected from the South Australian desert over a simulated hydration-desiccation cycle. Hydrogenase-encoding sequences were abundant in the metagenomes and metatranscriptomes and were detected in actinobacterial, acidobacterial, and cyanobacterial metagenome-assembled genomes. Native dry soil samples mediated H2 oxidation, but rates increased 950-fold following wetting. Oxygenic and anoxygenic phototrophs were also detected in the community but at lower abundances. Hydration significantly stimulated rates of photosynthetic carbon fixation and, to a lesser extent, dark carbon assimilation. Hydrogenase genes were also widespread in samples from three other climatically distinct deserts, the Namib, Gobi, and Mojave, and atmospheric H2 oxidation was also greatly stimulated by hydration at these sites. Together, these findings highlight that H2 is an important, hitherto-overlooked energy source supporting bacterial communities in desert soils. Contrary to our previous hypotheses, however, H2 oxidation occurs simultaneously rather than alternately with photosynthesis in such ecosystems and may even be mediated by some photoautotrophs. IMPORTANCE Desert ecosystems, spanning a third of the earth’s surface, harbor remarkably diverse microbial life despite having a low potential for photosynthesis. In this work, we reveal that atmospheric hydrogen serves as a major previously overlooked energy source for a large proportion of desert bacteria. We show that both chemoheterotrophic and photoautotrophic bacteria have the potential to oxidize hydrogen across deserts sampled across four continents. Whereas hydrogen oxidation was slow in native dry deserts, it increased by three orders of magnitude together with photosynthesis following hydration. This study revealed that continual harvesting of atmospheric energy sources may be a major way that desert communities adapt to long periods of water and energy deprivation, with significant ecological and biogeochemical ramifications.

Bacteria have been inferred to exhibit relatively weak biogeographic patterns. To what extent such findings reflect true biological phenomena or methodological artifacts remains unclear. Here, we addressed this question by analyzing the turnover of soil bacterial communities from three data sets. We applied three methodological innovations: (i) design of a hierarchical sampling scheme to disentangle environmental from spatial factors driving turnover; (ii) resolution of 16S rRNA gene amplicon sequence variants to enable higher-resolution community profiling; and (iii) application of the new metric zeta diversity to analyze multisite turnover and drivers. At fine taxonomic resolution, rapid compositional turnover was observed across multiple spatial scales. Turnover was overwhelmingly driven by deterministic processes and influenced by the rare biosphere. The communities also exhibited strong distance decay patterns and taxon-area relationships, with z values within the interquartile range reported for macroorganisms. These biogeographical patterns were weakened upon applying two standard approaches to process community sequencing data: clustering sequences at 97% identity threshold and/or filtering the rare biosphere (sequences lower than 0.05% relative abundance). Comparable findings were made across local, regional, and global data sets and when using shotgun metagenomic markers. Altogether, these findings suggest that bacteria exhibit strong biogeographic patterns, but these signals can be obscured by methodological limitations. We advocate various innovations, including using zeta diversity, to advance the study of microbial biogeography. IMPORTANCE It is commonly thought that bacterial distributions show lower spatial variation than for multicellular organisms. In this article, we present evidence that these inferences are artifacts caused by methodological limitations. Through leveraging innovations in sampling design, sequence processing, and diversity analysis, we provide multifaceted evidence that bacterial communities in fact exhibit strong distribution patterns. This is driven by selection due to factors such as local soil characteristics. Altogether, these findings suggest that the processes underpinning diversity patterns are more unified across all domains of life than previously thought, which has broad implications for the understanding and management of soil biodiversity.

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Abstract. In drylands, microbes that colonize rock surfaces have been linked to erosion because water scarcity excludes traditional weathering mechanisms. We studied the origin and role of rock biofilms in geomorphic processes of hard lime and dolomitic rocks that feature comparable weathering morphologies, although these two rock types originate from arid and hyperarid environments, respectively. We hypothesized that weathering patterns are fashioned by salt erosion and mediated by the rock biofilms that originate from the adjacent soil and dust. We used a combination of microbial and geological techniques to characterize rock morphologies and the origin and diversity of their biofilms. Amplicon sequencing of the SSU rRNA gene suggested that bacterial diversity is low and dominated by Proteobacteria and Actinobacteria. These phyla only formed laminar biofilms on rock surfaces that were exposed to the atmosphere and burrowed up to 6 mm beneath the surface, protected by sedimentary deposits. Unexpectedly, the microbial composition of the biofilms differed between the two rock types and was also distinct from the communities identified in the adjacent soil and settled dust, showing a habitat-specific filtering effect. Moreover, the rock bacterial communities were shown to secrete extracellular polymeric substances (EPSs) that form an evaporation barrier, reducing water loss rates by 65 %–75 %. The reduced water transport rates through the rock also limit salt transport and its crystallization in surface pores, which is thought to be the main force for weathering. Concomitantly, the biofilm layer stabilizes the rock surface via coating and protects the weathered front. Our hypothesis contradicts common models, which typically consider biofilms to be agents that promote weathering. In contrast, we propose that the microbial colonization of mineral surfaces acts to mitigate geomorphic processes in hot, arid environments.

In drylands, microbes that colonise rock surfaces were linked to erosion because water scarcity excludes traditional weathering mechanisms. We studied the origin and role of rock biofilms in geomorphic processes of hard lime and dolomitic rocks that feature comparable weathering morphologies though originating from arid and hyperarid environments, respectively. We hypothesised that weathering patterns are fashioned by salt erosion and mediated by the rock biofilms that originate from the adjacent soil and dust. We used a combination of microbial and geological techniques to characterise rocks morphologies and the origin and diversity of their biofilm. Amplicon sequencing of the SSU rRNA gene suggested that bacterial diversity is low and dominated by Proteobacteria and Actinobacteria. These phyla formed laminar biofilms only on rock surfaces that were exposed to the atmosphere and burrowed up to 6 mm beneath the surface, protected by sedimentary deposits. Unexpectedly, the microbial composition of the biofilms differed between the two rock types and was also distinct from the communities identified in the adjacent soil and settled dust, showing a habitat-specific filtering effect. Moreover, the rock bacterial communities were shown to secrete extracellular polymeric substances that form an evaporation barrier, reducing water loss rates by 65-75%. The reduced water transport rates through the rock also limit salt transport and its crystallisation in surface pores, which is thought to be the main force for weathering. Concomitantly, the biofilm layer stabilises the rock surface via coating and protects the weathered front. Our hypothesis contradicts common models, which typically consider biofilms as weathering-promoting agents. In contrast, we propose the microbial colonisation of mineral surfaces acts to mitigate geomorphic processes in hot, arid environments.