Temporal dynamics of microbial transcription in wetted hyperarid desert soils

Abstract

Rainfall is rare in hyperarid deserts but, when it occurs, it triggers large biological responses which are considered to be essential for the long-term maintenance of biodiversity. In such environments, microbial communities have major roles in nutrient cycling, but their functional responses to short-lived resource opportunities are poorly understood. We used whole community metatranscriptomic data to demonstrate structured and sequential functional responses in desiccated desert soils to a simulated rainfall event over a seven-day time frame. Rapid transcriptional activation of Actinobacteria, Alpha-proteobacteria and phage transcripts was followed by a marked increase in protist and myxobacterial activity, before returning to the original state. In functional terms, motility systems were activated in the early phases, whereas competition-toxicity systems increased in parallel to the activity from predators and the drying of soils. The dispersal-predation dynamic was identified as a central driver of microbial community responses to watering. Carbon fixation mechanisms that were active under dry condition were rapidly down-regulated in wetted soils, and only reactivated on a return to a near-dry state, suggesting a reciprocal balance between carbon fixation and fixed-carbon acquisition processes. Water addition induced a general reduction in the transcription of stress response genes, most prominently HSP20, indicating that this chaperone is particularly important for life in desiccated ecosystems. Based on these data, we propose a rainfall response model for desert soil microbiomes.

Water inputs across the Namib Desert: implications for dryland edaphic microbiology

“…In addition, only limited data are available on the limits of metabolic processes in relation to water activity and, where available, often come from laboratory studies of single organisms. While acknowledging the weakness of extrapolating single-organism data to entire microbial communities, the implication from these estimates is that the capacity for microbial community growth is severely constrained in all Namib Desert soils and active growth may only occur during the brief, and intermittent, rain events and for relatively short periods thereafter (León-Sobrino et al 2021).…”

“…Water inputs have been shown to dramatically alter the composition of Namib Desert soil microbial communities over the short term, both in ex-situ microcosm experiments (Frossard et al 2015) and in in-situ field studies (Jacobson 1997, Armstrong et al 2016, León-Sobrino et al 2021. Similarly, exposure to wetting alters both the activity (Jacobson and Jacobson 1998, Rajeev et al 2013, Jordaan et al 2020) and spatial organisation (Garcia-Pichel and Pringault 2001) of desert soil microbial communities globally.…”

“…Similarly, exposure to wetting alters both the activity (Jacobson and Jacobson 1998, Rajeev et al 2013, Jordaan et al 2020) and spatial organisation (Garcia-Pichel and Pringault 2001) of desert soil microbial communities globally. The central Namib Desert soil microbiome has been shown to respond very rapidly to the addition of liquid water, with substantial up-regulation of key functional genes (particularly motility and transport process genes) within minutes of water addition (León-Sobrino et al 2021). However, the sporadic and erratic nature of rainwater input in desert regions inevitably means that desert soils are, for a very large part of any annual cycle, fully desiccated (i.e., have gravimetric water content values of 0.5-2%) as seen in both the Negev (Agam (Ninari) and Berliner 2004) and Namib (Li et al 2018) deserts.…”

“…The non-zero respiration of dry soils is assumed to be mostly of biotic origin with the caveat that soil respiration in arid environments actually may be underestimated due to abiotic CO 2 fixation (Fa et al 2018). There is also strong molecular evidence for continued microbial functionality in desiccated soils, based on transcriptomic and proteomic analyses (Gunnigle et al 2014, Gunnigle et al 2017, Schulze-Makuch et al 2018, León-Sobrino et al 2021).…”

Microbial anhydrobiosis

“…motility genes, transporter genes) and downregulation (e.g. stress‐response genes, autotrophic carbon‐acquisition genes) were observed only 10 min after the addition of water to desiccated soils (León‐Sobrino et al ., 2021).…”