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Abstract Understanding how populations respond to disturbances represents a major goal for microbial ecology. While several hypotheses have been advanced to explain microbial community compositional changes in response to disturbance, appropriate data to test these hypotheses is scarce, due to the challenges in delineating rare vs. abundant taxa and generalists vs. specialists, a prerequisite for testing the theories. Here, we operationally define these two key concepts by employing the patterns of coverage of a (target) genome by a metagenome to identify rare populations, and by borrowing the proportional similarity index from macroecology to identify generalists. We applied these concepts to time-series (field) metagenomes from the Piver’s Island Coastal Observatory to establish that coastal microbial communities are resilient to major perturbations such as tropical cyclones and (uncommon) cold or warm temperature events, in part due to the response of rare populations. Therefore, these results provide support for the insurance hypothesis [i.e. the rare biosphere has the buffering capacity to mitigate the effects of disturbance]. Additionally, generalists appear to contribute proportionally more than specialists to community adaptation to perturbations like warming, supporting the disturbance-specialization hypothesis [i.e. disturbance favors generalists]. Several of these findings were also observed in replicated laboratory mesocosms that aimed to simulate disturbances such as a rain-driven washout of microbial cells and a labile organic matter release from a phytoplankton bloom. Taken together, our results advance understanding of the mechanisms governing microbial population dynamics under changing environmental conditions and have implications for ecosystem modeling. 

Abstract Metagenomic surveys have revealed that natural microbial communities are predominantly composed of sequence-discrete, species-like populations but the genetic and/or ecological processes that maintain such populations remain speculative, limiting our understanding of population speciation and adaptation to perturbations. To address this knowledge gap, we sequenced 112 Salinibacter ruber isolates and 12 companion metagenomes from four adjacent saltern ponds in Mallorca, Spain that were experimentally manipulated to dramatically alter salinity and light intensity, the two major drivers of this ecosystem. Our analyses showed that the pangenome of the local Sal. ruber population is open and similar in size (~15,000 genes) to that of randomly sampled Escherichia coli genomes. While most of the accessory (noncore) genes were isolate-specific and showed low in situ abundances based on the metagenomes compared to the core genes, indicating that they were functionally unimportant and/or transient, 3.5% of them became abundant when salinity (but not light) conditions changed and encoded for functions related to osmoregulation. Nonetheless, the ecological advantage of these genes, while significant, was apparently not strong enough to purge diversity within the population. Collectively, our results provide an explanation for how this immense intrapopulation gene diversity is maintained, which has implications for the prokaryotic species concept. 

Summary Bacteriophages encode host‐acquired functional genes known as auxiliary metabolic genes (AMGs). Photosynthesis AMGs are commonly found in marine cyanobacteria‐infectingMyoviridaeandPodoviridaecyanophages, but their ecology remains understudied in freshwater environments. To advance knowledge of this issue, we analysed viral metagenomes collected in the summertime for four years from five lakes and two estuarine locations interconnected by the Chattahoochee River, Southeast USA. Sequences representing ten different AMGs were recovered and found to be prevalent in all sites. Most freshwater AMGs were 10‐fold less abundant than estuarine and marine AMGs and were encoded by novelMyoviridaeandPodoviridaecyanophage genera. Notably, several of the corresponding viral genomes showed endemism to a specific province along the river. This translated intopsbAgene phylogenetic clustering patterns that matched a marine vs. freshwater origin indicating thatpsbAmay serve as a robust classification and source‐tracking biomarker. Genomes classified in a novel viral lineage represented by isolate S‐EIVl containedpsbA, which is unprecedented for this lineage. Collectively, our findings indicated that the acquisition of photosynthesis AMGs is a widespread strategy used by cyanophages in aquatic ecosystems, and further indicated the existence of viral provinces in which certain viral species and/or genotypes are locally abundant.