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Abstract Microbial communities are not the easiest to manipulate experimentally in natural ecosystems. However, leaf litter—topmost layer of surface soil—is uniquely suitable to investigate the complexities of community assembly. Here, we reflect on over a decade of collaborative work to address this topic using leaf litter as a model system in Southern California ecosystems. By leveraging a number of methodological advantages of the system, we have worked to demonstrate how four processes—selection, dispersal, drift, and diversification—contribute to bacterial and fungal community assembly and ultimately impact community functioning. Although many dimensions remain to be investigated, our initial results demonstrate that both ecological and evolutionary processes occur simultaneously to influence microbial community assembly. We propose that the development of additional and experimentally tractable microbial systems will be enormously valuable to test the role of eco-evolutionary processes in natural settings and their implications in the face of rapid global change. 

Abstract Plasmids are so closely associated with pathogens and antibiotic resistance that their potential for conferring other traits is often overlooked. Few studies consider how the full suite of traits encoded by plasmids is related to a host’s environmental adaptation, particularly for Gram-positive bacteria. To investigate the role that plasmid traits might play in microbial communities from natural ecosystems, we identified plasmids carried by isolates of Curtobacterium (phylum Actinomycetota) from a variety of soil environments. We found that plasmids were common, but not ubiquitous, in the genus and varied greatly in their size and genetic diversity. There was little evidence of phylogenetic conservation among Curtobacterium plasmids even for closely related bacterial strains within the same ecotype, indicating that horizontal transmission of plasmids is common. The plasmids carried a wide diversity of traits that were not a random subset of the host chromosome. Furthermore, the composition of these plasmid traits was associated with the environmental context of the host bacterium. Together, the results indicate that plasmids contribute substantially to the microdiversity of a soil bacterium and that this diversity may play a role in niche differentiation and a bacterium’s adaptation to its local environment. 

Global changes such as increased drought and atmospheric nitrogen deposition perturb both the microbial and plant communities that mediate terrestrial ecosystem functioning. However, few studies consider how microbial responses to global changes may be influenced by interactions with plant communities. To begin to address the role of microbial–plant interactions, we tested the hypothesis that the response of microbial communities to global change depends on the plant community. We characterized bacterial and fungal communities from 395 plant litter samples taken from the Loma Ridge Global Change Experiment, a decade-long global change experiment in Southern California that manipulates rainfall and nitrogen levels across two adjacent ecosystems, a grassland and a coastal sage scrubland. The differences in bacterial and fungal composition between ecosystems paralleled distinctions in plant community composition. In addition to the direct main effects, the global change treatments altered microbial composition in an ecosystem-dependent manner, in support of our hypothesis. The interaction between the drought treatment and ecosystem explained nearly 5% of the variation in bacterial community composition, similar to the variation explained by the ecosystem-independent effects of drought. Unexpectedly, we found that the main effect of drought was approximately four times as strong on bacterial composition as that of nitrogen addition, which did not alter fungal or plant composition. Overall, the findings underscore the importance of considering plant–microbe interactions when considering the transferability of the results of global change experiments across ecosystems. 

ABSTRACT Theory, simulation, and experimental evolution demonstrate that diversified CRISPR-Cas immunity to lytic viruses can lead to stochastic virus extinction due to a limited number of susceptible hosts available to each potential new protospacer escape mutation. Under such conditions, theory predicts that to evade extinction, viruses evolve toward decreased virulence and promote vertical transmission and persistence in infected hosts. To better understand the evolution of host-virus interactions in microbial populations with active CRISPR-Cas immunity, we studied the interaction between CRISPR-immune Sulfolobus islandicus cells and immune-deficient strains that are infected by the chronic virus SSV9. We demonstrate that Sulfolobus islandicus cells infected with SSV9, and with other related SSVs, kill uninfected, immune strains through an antagonistic mechanism that is a protein and is independent of infectious virus. Cells that are infected with SSV9 are protected from killing and persist in the population. We hypothesize that this infection acts as a form of mutualism between the host and the virus by removing competitors in the population and ensuring continued vertical transmission of the virus within populations with diversified CRISPR-Cas immunity. IMPORTANCE Multiple studies, especially those focusing on the role of lytic viruses in key model systems, have shown the importance of viruses in shaping microbial populations. However, it has become increasingly clear that viruses with a long host-virus interaction, such as those with a chronic lifestyle, can be important drivers of evolution and have large impacts on host ecology. In this work, we describe one such interaction with the acidic crenarchaeon Sulfolobus islandicus and its chronic virus Sulfolobus spindle-shaped virus 9. Our work expands the view in which this symbiosis between host and virus evolved, describing a killing phenotype which we hypothesize has evolved in part due to the high prevalence and diversity of CRISPR-Cas immunity seen in natural populations. We explore the implications of this phenotype in population dynamics and host ecology, as well as the implications of mutualism between this virus-host pair. 

ABSTRACT Viral infection exerts selection pressure on marine microbes, as virus-induced cell lysis causes 20 to 50% of cell mortality, resulting in fluxes of biomass into oceanic dissolved organic matter. Archaeal and bacterial populations can defend against viral infection using the clustered regularly interspaced short palindromic repeat (CRISPR)-associated (Cas) system, which relies on specific matching between a spacer sequence and a viral gene. If a CRISPR spacer match to any gene within a viral genome is equally effective in preventing lysis, no viral genes should be preferentially matched by CRISPR spacers. However, if there are differences in effectiveness, certain viral genes may demonstrate a greater frequency of CRISPR spacer matches. Indeed, homology search analyses of bacterioplankton CRISPR spacer sequences against virioplankton sequences revealed preferential matching of replication proteins, nucleic acid binding proteins, and viral structural proteins. Positive selection pressure for effective viral defense is one parsimonious explanation for these observations. CRISPR spacers from virioplankton metagenomes preferentially matched methyltransferase and phage integrase genes within virioplankton sequences. These virioplankton CRISPR spacers may assist infected host cells in defending against competing phage. Analyses also revealed that half of the spacer-matched viral genes were unknown, some genes matched several spacers, and some spacers matched multiple genes, a many-to-many relationship. Thus, CRISPR spacer matching may be an evolutionary algorithm, agnostically identifying those genes under stringent selection pressure for sustaining viral infection and lysis. Investigating this subset of viral genes could reveal those genetic mechanisms essential to virus-host interactions and provide new technologies for optimizing CRISPR defense in beneficial microbes. IMPORTANCE The CRISPR-Cas system is one means by which bacterial and archaeal populations defend against viral infection which causes 20 to 50% of cell mortality in the ocean. We tested the hypothesis that certain viral genes are preferentially targeted for the initial attack of the CRISPR-Cas system on a viral genome. Using CASC, a pipeline for CRISPR spacer discovery, and metagenome data from oceanic microbes and viruses, we found a clear subset of viral genes with high match frequencies to CRISPR spacers. Moreover, we observed a many-to-many relationship of spacers and viral genes. These high-match viral genes were involved in nucleotide metabolism, DNA methylation, and viral structure. It is possible that CRISPR spacer matching is an evolutionary algorithm pointing to those viral genes most important to sustaining infection and lysis. Studying these genes may advance the understanding of virus-host interactions in nature and provide new technologies for leveraging CRISPR-Cas systems in beneficial microbes. 

Abstract Microorganisms are the primary engines of biogeochemical processes and foundational to the provisioning of ecosystem services to human society. Free‐living microbial communities (microbiomes) and their functioning are now known to be highly sensitive to environmental change. Given microorganisms' capacity for rapid evolution, evolutionary processes could play a role in this response. Currently, however, few models of biogeochemical processes explicitly consider how microbial evolution will affect biogeochemical responses to environmental change. Here, we propose a conceptual framework for explicitly integrating evolution into microbiome–functioning relationships. We consider how microbiomes respond simultaneously to environmental change via four interrelated processes that affect overall microbiome functioning (physiological acclimation, demography, dispersal and evolution). Recent evidence in both the laboratory and the field suggests that ecological and evolutionary dynamics occur simultaneously within microbiomes; however, the implications for biogeochemistry under environmental change will depend on the timescales over which these processes contribute to a microbiome's response. Over the long term, evolution may play an increasingly important role for microbially driven biogeochemical responses to environmental change, particularly to conditions without recent historical precedent.