Nutrient Acquisition, Rather Than Stress Response Over Diel Cycles, Drives Microbial Transcription in a Hyper-Arid Namib Desert Soil

Abstract

Hot desert surface soils are characterized by extremely low water activities for large parts of any annual cycle. It is widely assumed that microbial processes in such soils are very limited. Here we present the first metatranscriptomic survey of microbial community function in a low water activity hyperarid desert soil. Sequencing of total mRNA revealed a diverse and active community, dominated by Actinobacteria. Metatranscriptomic analysis of samples taken at different times over 3 days indicated that functional diel variations were limited at the whole community level, and mostly affected the eukaryotic subpopulation which was induced during the cooler night hours. High levels of transcription of chemoautotrophic carbon fixation genes contrasted with limited expression of photosynthetic genes, indicating that chemoautotrophy is an important alternative to photosynthesis for carbon cycling in desiccated desert soils. Analysis of the transcriptional levels of key N-cycling genes provided strong evidence that soil nitrate was the dominant nitrogen input source. Transcriptional network analyses and taxon-resolved functional profiling suggested that nutrient acquisition processes, and not diurnal environmental variation, were the main drivers of community activity in hyperarid Namib Desert soil. While we also observed significant levels of expression of common stress response genes, these genes were not dominant hubs in the co-occurrence network.

Nutrient parsimony shapes diversity and functionality in hyper-oligotrophic Antarctic soils

“…Soil nitrate is depleted of 15 N in Antarctic soils [13], and our data support previous findings that soil nitrate in the desert sub-surface may be an essential reservoir of bioavailable nitrogen used by microorganisms to overcome nitrogen deficiency [69]. Interestingly, a recent metatranscriptomic study of microbial functionality in desiccated hot desert soils [70] showed high levels of nitrate reductase gene expression but little or no nitrogenase gene expression, suggesting that nitrate was also the primary source of metabolic N in this edaphic environment.…”

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

“…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).…”

Functional Traits Co-Occurring with Mobile Genetic Elements in the Microbiome of the Atacama Desert

“…In the present study, we detected several stress response genes associated with cold-shock, heat-shock and osmotic pressure, though only a small fraction was co-occurring with MGEs. The stress response is highly transcribed in potentially active microbial communities from desert soils but it seems that nutrient acquisition is a more critical factor [4]. Even so, rpoE co-occurring with MGEs was the most abundant gene identified with GhostKOALA in the present study.…”

“…For example, the gene coding for dihydrolipoyl dehydrogenase was the most abundant gene related to energy production co-occurring with MGEs. This enzyme, involved in the TCA cycle, has been recognized as a central step in the carbohydrate metabolism in the Nabim Desert [4]. The authors of this study suggested that nutrients acquisition (nitrogen, phosphorus and sulfur assimilation and carbon fixation) rather than the stress response has a central role in the transcriptional activity.…”

“…A recent polyphasic study gave evidence for metabolically active microbial communities in the Atacama Desert, even in the hyperarid region where the water activity is often below the metabolic needs [3]. Likewise, transcriptional data showed active microbial communities in desert soil from the Namib Desert [4]. Some studies have indicated that Mobile Genetic Elements (MGEs) are enriched in the microbiomes of extreme environments, which could facilitate an enhanced evolution and adaptation of the microbiome to environmental stressors [5].…”