Light intensity and temperature drive growth investment strategies during resuscitation in desert biocrust communities

Drylands cover ~46%% of Earth's surface and support diverse life forms despite water scarcity. In such a harsh environment, living organisms, including microorganisms, lichens, algae, and mosses, form a few mm-thick structure called biological soil crusts (biocrusts), that prevent soil erosion and play a crucial role in ecosystem stability. Biocrusts host microbial communities that survive desiccation by entering a dormant state, reducing metabolic activity. Upon rehydration, the reactivation of these organisms, followed by energy-generating metabolisms and DNA repair, sustains their survival. Previously, we studied microbial activation after a rain event in the daytime at 27 °C¹, while nighttime responses at cooler temperatures remained unexplored. Here, we investigate whether microbial reactivation dynamics vary under contrasting light and temperature regimes, and whether these differences are reflected in resource allocation strategies during early rehydration.

A rehydration experiment was conducted in the dark with biocrusts sampled at the LTER Avdat site in the Negev Desert, Israel. Biocrusts were rehydrated (to 75% water-holding capacity) in a climate-controlled chamber, followed by 12 h of night condition at 19°C and 10 h of day at 27 °C with a 2 h transition. The previously conducted light incubation resulted in desiccation of the biocrusts within 39 hours, whereas nighttime incubation resulted in desiccation within 55 hours. Samples were collected at multiple time points during this experiment for metatranscriptome sequencing. RNA reads were mapped to metagenome-assembled genomes (MAGs) from the same samples for differential gene expression analysis.

Metatranscriptomic analyses revealed a rapid reactivation pattern in both conditions. In the dark, about 70% of MAGs showed significant differential gene expression within 15 minutes of rehydration, increasing to 93% of MAGs between 15 minutes and 3 hours. At daytime, 85% of MAGs reactivated in the first 15 minutes and increased to 95% in three hours. During the early hydration stage, dark-incubated samples exhibited a delayed but increasing transcriptional response, with a higher number of differentially expressed genes per MAG between 30 minutes and 3 hours compared to the light-incubated samples. The light-incubated samples exhibited a stronger initial response within the first 30 minutes, followed by fewer changes at later time points. Consistent with this pattern, a ribosomal-protein-based growth index, calculated as the mean normalized expression of ribosomal protein genes per MAG, remained higher during the first 3 hours under dark-incubated conditions but peaked earlier and declined by 3 hours under light-incubated conditions, despite comparable water availability. Together, these results indicate that hydration at dark and cooler conditions supports a more prolonged and gradual transcriptional adjustment, accompanied by sustained investment in translational capacity, whereas daylight and warmer conditions promote a rapid early response followed by earlier stabilization of core cellular functions.

• Imminger, S. et al. Survival and rapid resuscitation permit limited productivity in desert microbial communities. Nat. Commun. 15, 3056 (2024).