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.
Highlights
Microbial communities are essential to the functioning and evolution of our planet and their dynamics greatly affect
The response and recovery of natural communities following environmental disasters, rather than manipulative experiments, remain largely unexplored mechanistically because of the difficulty in avoiding multiple compounding environmental factors [11, 12]. These gaps in the understanding of microbial community behavior limits our ability to effectively model and predict the responses of microbiomes to major perturbations, such as those resulting from climate change and natural or man-made ecological disasters. To address this knowledge gap, and to build a conceptual model for modeling microbial community responses to extreme stress, we examined the temporal dynamics in response to a disastrous climate perturbation of a unique microbial ecosystem found in the Atacama Desert, Chile
The surviving community was comprised of organisms with higher average isoelectric points of their predicted proteins and lower potassium uptake potential
Summary
Each halite nodule represents a near-closed miniature ecosystem and can be treated as true independent biological replicates in longitudinal studies, allowing community changes to be tracked without external factors compounding the results Combined with their sensitivity to changing osmotic conditions and slow growth rates, this makes halite microbiomes ideal for studying temporal dynamics of microbial communities and their ability to adapt to major environmental changes. The previous notable precipitation in the area occurred in 2002 (4.1 mm) [25] Such rain events have been observed to be devastating to the specialized hyper-arid microbiomes of the Atacama Desert [26], in communities adapted to survive in saturated salt conditions, such as those found in halite nodules. Our longitudinal study over 4 years captured the microbiome’s short-term adaptations to this major natural disaster and its recovery in the subsequent years, revealing two strikingly different community response mechanisms
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