Survival and rapid resuscitation permit limited productivity in desert soil microbial communities

Despite drylands constituting the largest terrestrial biome, key information such as microbial productivity in desert soil is lacking. However, rapid growth would be needed to maintain the microbial community, if, as proposed, desiccation and rehydration via rain causes widespread cell death due to osmotic stress. Further, major microbially-mediated ecosystem processes are confined to rare and short periods of rain, but it is unknown how desert soil microorganisms maintain ecosystem processes in such narrow activity time. We addressed these knowledge gaps on rain-mediated microbial resuscitation and associated activities in biological soil crusts from the Negev Desert, Israel. We investigated changes in gene transcription of individual microbial populations and single-cell biomass generation during a controlled rehydration experiment. Simulating rain with ²H₂O followed by single-cell NanoSIMS, we showed that the desert biocrust microbial community is characterized by limited productivity, considering median replication times of 6 to 19 days and restricted number of days in the Negev Desert allowing growth. Genome-resolved metatranscriptomics revealed that nearly all microbial populations resuscitate within minutes after simulated rain, independent of taxonomy or encoded physiology. We observed distinct temporal phases of cellular processes, beginning with DNA repair powered by storage compound oxidation and only later followed by uptake of external carbon sources and resumption of main metabolism. Together, our data reveal a community that makes optimal use of short activity phases by fast and universal resuscitation enabling the maintenance of key ecosystem functions. This community is highly adapted to surviving rapid changes in soil moisture and solute concentrations, resulting in high persistence that balances limited productivity. These findings have important implications considering preservation of soil microbial communities that are critical for soil stabilization.