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.

Keywords: desert; dormancy; energetics; energy reserve; photosynthesis; trace gas.

FIG 1

Microbial community structure of global desert soils. The map is generated by ArcGIS 10.6 and shaded by global aridity index, a ratio of mean annual precipitation to potential evapotranspiration (160) modeled by Antonio Trabucco and Robert Zomer (161). The relative abundances of major microbial groups in 20 desert (nonbiocrust) soils from Africa (162, 163), Antarctica (77, 132, 164), Asia (165–170), Australia (171), Europe (172), North America (47, 77, 173), and South America (13) are displayed in pie charts and in Table S1 in the supplemental material. Phyla with a <1% relative abundance were grouped into the category “Other.” Actinobacteria is the most abundant phylum detected in bare soils (25.5%), followed by Proteobacteria (21%), Acidobacteria (6.5%), Bacteroidetes (6%), Chloroflexi (2.5%), and Firmicutes (2%) (median values of the 20 samples are shown in Table S1). Cyanobacteria, though abundant in soil biocrusts and lithic niches, are present in less than 1% in most bare soil samples.

FIG 2

Conceptual diagram representing the model lifestyle of a microbial community in a desert in response to hydration-desiccation cycles. It is proposed that organic carbon reserves (energy reserve hypothesis), light (light-dependent continual-energy-harvesting hypothesis), and trace gases (air-dependent continual-energy-harvesting hypothesis) are the major energy sources that allow dormant microorganisms to persist during prolonged desiccation. Abbreviations: CODH, carbon monoxide dehydrogenase; Hyd, group 1h [NiFe] hydrogenase; pMMO, particulate methane monooxygenase; PS, photosystem of aerobic anoxygenic phototroph; Rho, microbial rhodopsin; and Cox, terminal oxidase.