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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 Disturbances, here defined as events that directly alter microbial community composition, are commonly studied in host‐associated and engineered systems. In spite of global change both altering environmental averages and increasing extreme events, there has been relatively little research into the causes, persistence and population‐level impacts of disturbance in the dynamic coastal ocean. Here, we utilize 3 years of observations from a coastal time series to identify disturbances based on the largest week‐over‐week changes in the microbiome (i.e. identifying disturbance as events that alter the community composition). In general, these microbiome disturbances were not clearly linked to specific environmental factors and responsive taxa largely differed, aside from SAR11, which generally declined. However, several disturbance metagenomes identified increased phage‐associated genes, suggesting that unexplained community shifts might be caused by increased mortality. Furthermore, a category 1 hurricane, the only event that would likely be classifieda priorias an environmental disturbance, was not an outlier in microbiome composition, but did enhance a bloom in seasonally abundant phytoplankton. Thus, as extreme environmental changes intensify, assumptions of what constitutes a disturbance should be re‐examined in the context of ecological history and microbiome responses. 

Summary Microbial enzymes often occur as distinct variants that share the same substrate but differ in substrate affinity, sensitivity to environmental conditions, or phylogenetic ancestry. Determining where variants occur in the environment helps identify thresholds that constrain microbial cycling of key chemicals, including the greenhouse gas nitrous oxide (N₂O). To understand the enzymatic basis of N₂O cycling in the ocean, we mined metagenomes to characterize genes encoding bacterial nitrous oxide reductase (NosZ) catalyzing N₂O reduction to N₂. We examined data sets from diverse biomes but focused primarily on those from oxygen minimum zones where N₂O levels are often elevated. With few exceptions, marinenosZdata sets were dominated by ‘atypical’ clade II gene variants. AtypicalnosZhas been associated with low oxygen, enhanced N₂O affinity, and organisms lacking enzymes for complete denitrification, i.e., non‐denitrifiers. AtypicalnosZ often occurred in metagenome‐assembled genomes (MAGs) with nitrate or nitrite respiration genes, although MAGs with genes for complete denitrification were rare. We identified atypicalnosZ in several taxa not previously associated with N₂O consumption, in addition to known N₂O‐associated groups. The data suggest that marine environments generally select for high N₂O‐scavenging ability across diverse taxa and have implications for how N₂O concentration may affect N₂O removal rates. 

Summary Recent advances in sequencing technology and bioinformatic pipelines have allowed unprecedented access to the genomes of yet‐uncultivated microorganisms from diverse environments. However, the catalogue of freshwater genomes remains limited, and most genome recovery attempts in freshwater ecosystems have only targeted specific taxa. Here, we present a genome recovery pipeline incorporating iterative subtractive binning, and apply it to a time series of 100 metagenomic datasets from seven connected lakes and estuaries along the Chattahoochee River (Southeastern USA). Our set of metagenome‐assembled genomes (MAGs) represents >400 yet‐unnamed genomospecies, substantially increasing the number of high‐quality MAGs from freshwater lakes. We propose names for two novel species: ‘CandidatusElulimicrobium humile’ (‘Ca. Elulimicrobiota’, ‘Patescibacteria’) and ‘CandidatusAquidulcis frankliniae’ (‘Chloroflexi’). Collectively, our MAGs represented about half of the total microbial community at any sampling point. To evaluate the prevalence of these genomospecies in the chronoseries, we introduce methodologies to estimate relative abundance and habitat preference that control for uneven genome quality and sample representation. We demonstrate high degrees of habitat‐specialization and endemicity for most genomospecies in the Chattahoochee lakes. Wider ecological ranges characterized smaller genomes with higher coding densities, indicating an overall advantage of smaller, more compact genomes for cosmopolitan distributions. 

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.