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Key Points Surveys of closely related bacteria and archaea reveal that they have a high degree of genomic diversity, which manifests as single-nucleotide polymorphisms and gene-content variation. To meaningfully interpret the underlying causes of such diversity, it is necessary to clearly define populations — that is, groups of organisms that share a common gene pool and exhibit ecological associations within the same environment and are hence subject to similar selection pressures. High gene frequencies reflect stable selective pressures at the population level, whereas flexible gene content can be partitioned into medium and low gene frequencies to distinguish between different forms of frequency-dependent selection. Such gene categorization enables the generation of hypotheses relating to ecological and evolutionary dynamics. Low-frequency genes often encode different variants of surface structures and have fast rates of turnover, which enables evasion from predators and host immunity; however, the high rate of gene turnover also means that there is low linkage with other genes in the genome, which makes scenarios such as 'kill-the-winner' unlikely explanations for limiting the spread of adaptive clones within populations. Frequency-dependent selection, such as that which arises from social interactions or metabolic trade-offs, can explain the emergence of medium-frequency genes. Moreover, a comparison with animal and plant populations suggests that another role of phenotypic diversity among individuals is population-level synergism, which results from niche complementation. The fact that populations of bacteria and archaea can be regarded as interacting units is also suggested by several studies that have shown asymmetry in the way in which organisms interact within and between populations. Within populations, signalling seems to be increased and antagonism is reduced. Wild populations of bacteria and archaea show high levels of genotypic diversity. In this Review, Cordero and Polz discuss recent studies that show that this diversity arises owing to social and ecological interactions, which have important consequences for microbial ecology and population dynamics. Comparisons of closely related microorganisms have shown that individual genomes can be highly diverse in terms of gene content. In this Review, we discuss several studies showing that much of this variation is associated with social and ecological interactions, which have an important role in the population biology of wild populations of bacteria and archaea. These interactions create frequency-dependent selective pressures that can either stabilize gene frequencies at intermediate levels in populations or promote fast gene turnover, which presents as low gene frequencies in genome surveys. Thus, interpretation of gene-content diversity requires the delineation of populations according to cohesive gene flow and ecology, as micro-evolutionary changes arise in response to local selection pressures and population dynamics.

As one of the largest biotechnological applications, activated sludge (AS) systems in wastewater treatment plants (WWTPs) harbor enormous viruses, with 10-1,000-fold higher concentrations than in natural environments. However, the compositional variation and host-connections of AS viruses remain poorly explored. Here, we report a catalogue of ~50,000 prokaryotic viruses from six WWTPs, increasing the number of described viral species of AS by 23-fold, and showing the very high viral diversity which is largely unknown (98.4-99.6% of total viral contigs). Most viral genera are represented in more than one AS system with 53 identified across all. Viral infection widely spans 8 archaeal and 58 bacterial phyla, linking viruses with aerobic/anaerobic heterotrophs, and other functional microorganisms controlling nitrogen/phosphorous removal. Notably, Mycobacterium, notorious for causing AS foaming, is associated with 402 viral genera. Our findings expand the current AS virus catalogue and provide reference for the phage treatment to control undesired microorganisms in WWTPs. Activated sludge (AS) systems in wastewater treatment plants (WWTPs) contain high concentration of viruses. Here, the authors apply a systematic metagenomic pipeline and retrieve a catalogue of around 50,000 prokaryotic viruses from samples of six WWTPs, revealing a large and uncharacterized viral diversity in AS communities.

In the ocean, organic particles harbour diverse bacterial communities, which collectively digest and recycle essential nutrients. Traits like motility and exo-enzyme production allow individual taxa to colonize and exploit particle resources, but it remains unclear how community dynamics emerge from these individual traits. Here we track the taxon and trait dynamics of bacteria attached to model marine particles and demonstrate that particle-attached communities undergo rapid, reproducible successions driven by ecological interactions. Motile, particle-degrading taxa are selected for during early successional stages. However, this selective pressure is later relaxed when secondary consumers invade, which are unable to use the particle resource but, instead, rely on carbon from primary degraders. This creates a trophic chain that shifts community metabolism away from the particle substrate. These results suggest that primary successions may shape particle-attached bacterial communities in the ocean and that rapid community-wide metabolic shifts could limit rates of marine particle degradation. Particles of organic matter in the ocean harbour microbial communities that digest and recycle essential nutrients. Here, Datta et al. use model marine particles to show that the attached bacterial communities undergo rapid, reproducible successions driven by ecological interactions.

Microbial communities are shaped by viral predators. Yet, resolving which viruses (phages) and bacteria are interacting is a major challenge in the context of natural levels of microbial diversity. Thus, fundamental features of how phage-bacteria interactions are structured and evolve in the wild remain poorly resolved. Here we use large-scale isolation of environmental marine Vibrio bacteria and their phages to obtain estimates of strain-level phage predator loads, and use all-by-all host range assays to discover how phage and host genomic diversity shape interactions. We show that lytic interactions in environmental interaction networks (as observed in agar overlay) are sparse—with phage predator loads being low for most bacterial strains, and phages being host-strain-specific. Paradoxically, we also find that although overlap in killing is generally rare between tailed phages, recombination is common. Together, these results suggest that recombination during cryptic co-infections is an important mode of phage evolution in microbial communities. In the development of phages for bioengineering and therapeutics it is important to consider that nucleic acids of introduced phages may spread into local phage populations through recombination, and that the likelihood of transfer is not predictable based on lytic host range. Understanding the interactions between bacteria and their viruses (phages) in natural communities is a major challenge. Here, the authors isolate and study large numbers of marine Vibrio bacteria and their phages, and find that lytic interactions are sparse and many phages are host-strain-specific, but nevertheless recombination between some phages is common.

Microbial activity mediates the fluxes of greenhouse gases. However, in the global models of the marine and terrestrial biospheres used for climate change projections, typically only photosynthetic microbial activity is resolved mechanistically. To move forward, we argue that global biogeochemical models need a theoretically grounded framework with which to constrain parameterizations of diverse microbial metabolisms. Here, we explain how the key redox chemistry underlying metabolisms provides a path towards this goal. Using this first-principles approach, the presence or absence of metabolic functional types emerges dynamically from ecological interactions, expanding model applicability to unobserved environments. “Nothing is less real than realism. It is only by selection, by elimination, by emphasis, that we get at the real meaning of things.” –Georgia O’Keefe Marine microbial activities fuel biogeochemical cycles that impact the climate, but global models do not account for the myriad physiological processes that microbes perform. Here the authors argue for a model framework that reinterprets the ocean as physics coupled to biologically-driven redox chemistry.

A common strategy among microbes living in iron-limited environments is the secretion of siderophores, which can bind poorly soluble iron and make it available to cells via active transport mechanisms. Such siderophore–iron complexes can be thought of as public goods that can be exploited by local communities and drive diversification, for example by the evolution of “cheating.” However, it is unclear whether bacterial populations in the environment form stable enough communities such that social interactions significantly impact evolutionary dynamics. Here we show that public good games drive the evolution of iron acquisition strategies in wild populations of marine bacteria. We found that within nonclonal but ecologically cohesive genotypic clusters of closely related Vibrionaceae, only an intermediate percentage of genotypes are able to produce siderophores. Nonproducers within these clusters exhibited selective loss of siderophore biosynthetic pathways, whereas siderophore transport mechanisms were retained, suggesting that these nonproducers can act as cheaters that benefit from siderophore producers in their local environment. In support of this hypothesis, these nonproducers in iron-limited media suffer a significant decrease in growth, which can be alleviated by siderophores, presumably owing to the retention of transport mechanisms. Moreover, using ecological data of resource partitioning, we found that cheating coevolves with the ecological specialization toward association with larger particles in the water column, suggesting that these can harbor stable enough communities for dependencies among organisms to evolve.

Prophages are known to encode important virulence factors in the human pathogen Vibrio cholerae . However, little is known about the occurrence and composition of prophage-encoded traits in environmental vibrios. A database of 5,674 prophage-like elements constructed from 1,874 Vibrio genome sequences, covering sixty-four species, revealed that prophage-like elements encoding possible properties such as virulence and antibiotic resistance are widely distributed among environmental vibrios, including strains classified as non-pathogenic. Moreover, we found that 45% of Vibrio species harbored a complete prophage-like element belonging to the Inoviridae family, which encode the zonula occludens toxin (Zot) previously described in the V . cholerae . Interestingly, these zot -encoding prophages were found in a variety of Vibrio strains covering both clinical and marine isolates, including strains from deep sea hydrothermal vents and deep subseafloor sediments. In addition, the observation that a spacer from the CRISPR locus in the marine fish pathogen V . anguillarum strain PF7 had 95% sequence identity with a zot gene from the Inoviridae prophage found in V . anguillarum strain PF4, suggests acquired resistance to inoviruses in this species. Altogether, our results contribute to the understanding of the role of prophages as drivers of evolution and virulence in the marine Vibrio bacteria.

Members of a family of marine dsDNA non-tailed bacterial viruses have short, 10-kb genomes, infect a broader range of hosts than tailed viruses and belong to the double jelly roll capsid lineage of viruses, which are associated with diverse bacterial and archaeal hosts. Microbial predator found in the ocean Double-stranded DNA (dsDNA) viruses comprise both tailed and non-tailed viruses and are thought to be the most abundant viruses on Earth. Tailed viruses of the Caudovirales dominate sequence and culture collections, whereas non-tailed dsDNA viruses often dominate ocean samples but remain largely uncharacterized. Martin Polz and colleagues describe a family of diverse marine non-tailed viruses, called the Autolykiviridae . Through metagenomics and phylogenetic analyses, the team show that Autolykiviridae represent an ancient lineage of double jelly roll capsid viruses. They also show that these viruses are abundant in the ocean, where they prey on marine bacteria and archaea. This finding was facilitated by updated methods for environmental viral discovery, and represents an important step forwards in our understanding of environmental bacteria–virus interactions. The most abundant viruses on Earth are thought to be double-stranded DNA (dsDNA) viruses that infect bacteria 1 . However, tailed bacterial dsDNA viruses ( Caudovirales ), which dominate sequence and culture collections, are not representative of the environmental diversity of viruses 2 , 3 . In fact, non-tailed viruses often dominate ocean samples numerically 4 , raising the fundamental question of the nature of these viruses. Here we characterize a group of marine dsDNA non-tailed viruses with short 10-kb genomes isolated during a study that quantified the diversity of viruses infecting Vibrionaceae bacteria. These viruses, which we propose to name the Autolykiviridae , represent a novel family within the ancient lineage of double jelly roll (DJR) capsid viruses. Ecologically, members of the Autolykiviridae have a broad host range, killing on average 34 hosts in four Vibrio species, in contrast to tailed viruses which kill on average only two hosts in one species. Biochemical and physical characterization of autolykiviruses reveals multiple virion features that cause systematic loss of DJR viruses in sequencing and culture-based studies, and we describe simple procedural adjustments to recover them. We identify DJR viruses in the genomes of diverse major bacterial and archaeal phyla, and in marine water column and sediment metagenomes, and find that their diversity greatly exceeds the diversity that is currently captured by the three recognized families of such viruses. Overall, these data suggest that viruses of the non-tailed dsDNA DJR lineage are important but often overlooked predators of bacteria and archaea that impose fundamentally different predation and gene transfer regimes on microbial systems than on tailed viruses, which form the basis of all environmental models of bacteria–virus interactions.

Although competition–dispersal tradeoffs are commonly invoked to explain species coexistence for animals and plants in spatially structured environments, such mechanisms for coexistence remain unknown for microorganisms. Here we show that two recently speciated marine bacterioplankton populations pursue different behavioral strategies to exploit nutrient particles in adaptation to the landscape of ephemeral nutrient patches characteristic of ocean water. These differences are mediated primarily by differential colonization of and dispersal among particles. Whereas one population is specialized to colonize particles by attaching and growing biofilms, the other is specialized to disperse among particles by rapidly detecting and swimming toward new particles, implying that it can better exploit short-lived patches. Because the two populations are very similar in their genomic composition, metabolic abilities, chemotactic sensitivity, and swimming speed, this fine-scale behavioral adaptation may have been responsible for the onset of the ecological differentiation between them. These results demonstrate that the principles of spatial ecology, traditionally applied at macroscales, can be extended to the ocean’s microscale to understand how the rich spatiotemporal structure of the resource landscape contributes to the fine-scale ecological differentiation and species coexistence among marine bacteria.

Because microbial plankton in the ocean comprise diverse bacteria, algae, and protists that are subject to environmental forcing on multiple spatial and temporal scales, a fundamental open question is to what extent these organisms form ecologically cohesive communities. Here we show that although all taxa undergo large, near daily fluctuations in abundance, microbial plankton are organized into clearly defined communities whose turnover is rapid and sharp. We analyze a time series of 93 consecutive days of coastal plankton using a technique that allows inference of communities as modular units of interacting taxa by determining positive and negative correlations at different temporal frequencies. This approach shows both coordinated population expansions that demarcate community boundaries and high frequency of positive and negative associations among populations within communities. Our analysis thus highlights that the environmental variability of the coastal ocean is mirrored in sharp transitions of defined but ephemeral communities of organisms. Whether marine microbes form strongly differentiated communities over time remains unknown. Here, Martin-Platero and colleagues develop a time series analysis to characterize marine bacteria and Eukarya communities at a fine temporal grain, revealing cohesive but rapidly changing communities.