Energetic Basis of Microbial Growth and Persistence in Desert Ecosystems

Abstract

Microbial life is surprisingly abundant and diverse in global desert ecosystems. In these environments, microorganisms endure a multitude of physicochemical stresses, including low water potential, carbon and nitrogen starvation, and extreme temperatures. In this review, we summarize our current understanding of the energetic mechanisms and trophic dynamics that underpin microbial function in desert ecosystems. Accumulating evidence suggests that dormancy is a common strategy that facilitates microbial survival in response to water and carbon limitation. Whereas photoautotrophs are restricted to specific niches in extreme deserts, metabolically versatile heterotrophs persist even in the hyper-arid topsoils of the Atacama Desert and Antarctica. At least three distinct strategies appear to allow such microorganisms to conserve energy in these oligotrophic environments: degradation of organic energy reserves, rhodopsin- and bacteriochlorophyll-dependent light harvesting, and oxidation of the atmospheric trace gases hydrogen and carbon monoxide. In turn, these principles are relevant for understanding the composition, functionality, and resilience of desert ecosystems, as well as predicting responses to the growing problem of desertification.

Distribution of Mixotrophy and Desiccation Survival Mechanisms across Microbial Genomes in an Arid Biological Soil Crust Community

“…Recent studies have shown that the oxidation of atmospheric trace gases can be an alternative energy source for soil microorganisms ( 39 , 68 , 69 ), and it has been hypothesized that it might be widely used to generate maintenance energy during dormancy ( 11 ). We detected MAGs with the potential for H 2 oxidation in the phyla Actinobacteriota and Chloroflexota , consistent with previous investigations ( 70 ), and H 2 oxidation was recently detected in BSCs from the same sampling site ( 133 ).…”

“…Yet, dryland soils are inhabited by a variety of other microbial clades ( 3 , 10 ) whose mechanisms of surviving desiccation are unknown. It was recently suggested that many soil microorganisms might rely on inorganic energy sources such as light and oxidation of atmospheric trace gases (e.g., dihydrogen [H 2 ] and carbon monoxide [CO]) to maintain the cell’s integrity in a dormant state ( 11 ). Furthermore, trace gas oxidation could potentially support primary production, as oxidation of atmospheric H 2 has been shown to sustain CO 2 fixation in an Antarctic desert soil ( 12 ).…”

Hydrogen-Oxidizing Bacteria Are Abundant in Desert Soils and Strongly Stimulated by Hydration

“…Drought limits the abundance and productivity of oxygenic photoautotrophs, namely, cyanobacteria, microalgae, and plants, which require water as an electron donor. Low supplies of organic carbon, combined with impaired substrate diffusion and membrane transport, in turn limit the abundance of chemoheterotrophic microorganisms and fauna ( 6 , 7 ). The extents of nutrient limitation vary: semiarid deserts experience considerable precipitation and subsequent productivity, albeit counterbalanced by evapotranspiration, whereas hyperarid deserts can be deprived of rainfall over decadal scales ( 8 , 9 ).…”

“…KEYWORDS carbon fixation, desert, hydrogen, hydrogenase, primary production, trace gas S panning a third of land surfaces, deserts are extensive terrestrial biomes that are expanding due to multiple anthropogenic pressures (1,2). Organisms residing in these ecosystems endure severe and prolonged drought interspersed with infrequent hydration pulses, often in combination with other physicochemical pressures (3)(4)(5)(6). Drought limits the abundance and productivity of oxygenic photoautotrophs, namely, cyanobacteria, microalgae, and plants, which require water as an electron donor.…”

“…In contrast, these primary producers are low in abundance in exposed surface soils, which are instead dominated by chemoheterotrophs from phyla such as Actinobacteriota, Acidobacteriota, and Proteobacteria (10,15,16). Most of these bacteria are thought to live in dormant states during dry periods (6,7,17); while they have detectable transcriptional and metabolic activity (18)(19)(20), cells primarily expend energy for maintenance rather than growth. Rainfall pulses stimulate microbial activity and succession over short timescales, and the frequency and intensity of these events are thought to be major factors determining the composition and function of desert microbial communities over longer timescales (21)(22)(23)(24)(25)(26)(27)(28).…”