Survival, 'dormancy', and resuscitation of microorganisms in water-limited environments: insights from coastal salt flats and desert soil crusts

One of the most fascinating features of microorganisms is their ability to survive extremely hostile conditions such as desiccation, UV radiation, hypersalinity, and prolonged periods of starvation. The term ‘dormancy’ is often used to describe the state of reduced metabolic activity in which microorganisms endure unfavourable conditions. Few specific microbial taxa are known to form dedicated resting stages, e.g. spores or cysts. However, physiological and metabolic strategies associated with ‘dormancy’ and survival can vary dramatically between different habitats and microbial species. For most microbial taxa abundant in natural ecosystems such survival mechanisms remain unknown.
In arid regions, microbial activity in habitats like surface soils or tidal flats can suddenly become limited by one critical parameter – water availability. I will present two studies, where we investigated the functional potential and activity of microorganisms inhabiting two water-limited surface environments, both exposed to high UV radiation and heat: i) biological soil crusts of the Negev Desert and ii) salt-saturated microbial mats at the coast of Oman. In biological soil crusts, resumption of microbial activity during crust rehydration experiments was followed with single-cell measurements of biomass generation and population-resolved transcriptomics. In hypersaline microbial mats, rates of microbial processes such as photosynthesis, respiration and sulfide oxidation were assessed by microsensor measurements at varying salinities ranging from 12% NaCl to salt saturation. Both studies included a detailed analysis of genetic potential of the dominant microbial populations via genome-resolved metagenomics with focus on energy metabolism and stress tolerance mechanisms.
In both habitats, we found microbial communities that are highly adapted to survive the prolonged water availability limitation and resume activity upon stress relief, albeit in different ways. While nearly all microbial activity was paused in dry biological soil crusts resuming sharply within the first hours after rehydration, certain processes were still active at lower rates in salt saturated microbial mats. The differences between stress imposed on microorganisms by hypersalinity and desiccation stress are further mirrored in the different stress tolerance genes of the major photoautotrophic primary producers in both microbial communities, halophilic and desiccation-tolerant cyanobacteria, respectively.
Taken together, the insights gained in these in situ and microcosm studies extend our knowledge of desiccation and hypersalinity survival mechanisms in environmentally relevant microorganisms and help us understand the patterns of microbial activity, a major catalyst of biogeochemical cycles.

• BayCEER Kolloquium Dr. Dimitri Meier