Halophilic microbial community compositional shift after a rare rainfall in the Atacama Desert

Abstract

Understanding the mechanisms underlying microbial resistance and resilience to perturbations is essential to predict the impact of climate change on Earth’s ecosystems. However, the resilience and adaptation mechanisms of microbial communities to natural perturbations remain relatively unexplored, particularly in extreme environments. The response of an extremophile community inhabiting halite (salt rocks) in the Atacama Desert to a catastrophic rainfall provided the opportunity to characterize and de-convolute the temporal response of a highly specialized community to a major disturbance. With shotgun metagenomic sequencing, we investigated the halite microbiome taxonomic composition and functional potential over a 4-year longitudinal study, uncovering the dynamics of the initial response and of the recovery of the community after a rainfall event. The observed changes can be recapitulated by two general modes of community shifts—a rapid Type 1 shift and a more gradual Type 2 adjustment. In the initial response, the community entered an unstable intermediate state after stochastic niche re-colonization, resulting in broad predicted protein adaptations to increased water availability. In contrast, during recovery, the community returned to its former functional potential by a gradual shift in abundances of the newly acquired taxa. The general characterization and proposed quantitation of these two modes of community response could potentially be applied to other ecosystems, providing a theoretical framework for prediction of taxonomic and functional flux following environmental changes.

Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community

“…Salt-in strategists accumulate KCl to balance the high osmotic pressure of their environment, hence the need to actively pump potassium into the cell. In contrast, we did not find any significant positive regulation between asRNAs and their cognate genes (upregulation of both), which might be due to the inherent quality of our data set, i.e., no ribodepletion and heterogeneity across replicates (14). Alternatively, it might also reflect promiscuous transcription processes as argued when considering the functionality of asRNAs (33).…”

“…We used metatranscriptomics data from multiple replicate samples collected in the field in 2016 and 2017 (21 and 24 replicates for 2016 and 2017, respectively) (see Table S1). Using SnapT, we aligned reads from stranded RNA sequencing (RNA-seq) libraries to our reference coassembled metagenome from a previous study (14) (See Fig. S1).…”

“…We carried out a differential expression analysis and found that 109 (18%) of the regulatory itsRNAs were significantly differentially expressed (false-discovery rate [FDR] Ͻ 5%) between samples collected in 2016 and 2017 ( Fig. 3 and Data Set S1), 3 and 15 months after a major rain event in the desert, respectively (14). Of these, 72% were annotated as archaea and 28% as bacteria, and 16 were conserved in multiple genomes (14 from Halobacteria and 2 from Cyanobacteria).…”

“…One major difficulty in obtaining metatranscriptomic data from natural microbial communities, in particular, from extreme environments, is the small amount of biomass that can be collected, resulting in low RNA yields (14). This, in turn, prevents attempts at ribodepletion, resulting in a decreased number of non-rRNA reads available for analysis.…”

“…This paucity of knowledge suggests that an abundance of sRNAs remain to be discovered with potentially essential roles in stress response (10), interspecies communication, and/or cross-species RNA interference (11)(12)(13). This might be relevant to extreme environments where microbial communities are specifically adapted to a narrow set of environmental conditions, i.e., high salt and low pH, and are particularly sensitive to perturbations (14).…”