Marine DNA Viral Macro- and Microdiversity from Pole to Pole.

Microbes drive most ecosystems and are modulated by viruses that impact their lifespan, gene flow, and metabolic outputs. However, ecosystem-level impacts of viral community diversity remain difficult to assess due to classification issues and few reference genomes. Here, we establish an ∼12-fold expanded global ocean DNA virome dataset of 195,728 viral populations, now including the Arctic Ocean, and validate that these populations form discrete genotypic clusters. Meta-community analyses revealed five ecological zones throughout the global ocean, including two distinct Arctic regions. Across the zones, local and global patterns and drivers in viral community diversity were established for both macrodiversity (inter-population diversity) and microdiversity (intra-population genetic variation). These patterns sometimes, but not always, paralleled those from macro-organisms and revealed temperate and tropical surface waters and the Arctic as biodiversity hotspots and mechanistic hypotheses to explain them. Such further understanding of ocean viruses is critical for broader inclusion in ecosystem models.

Interspecies Competition Impacts Targeted Manipulation of Human Gut Bacteria by Fiber-Derived Glycans.

Development of microbiota-directed foods (MDFs) that selectively increase the abundance of beneficial human gut microbes, and their expressed functions, requires knowledge of both the bioactive components of MDFs and the mechanisms underlying microbe-microbe interactions. Here, gnotobiotic mice were colonized with a defined consortium of human-gut-derived bacterial strains and fed different combinations of 34 food-grade fibers added to a representative low-fiber diet consumed in the United States. Bioactive carbohydrates in fiber preparations targeting particular Bacteroides species were identified using community-wide quantitative proteomic analyses of bacterial gene expression coupled with forward genetic screens. Deliberate manipulation of community membership combined with administration of retrievable artificial food particles, consisting of paramagnetic microscopic beads coated with dietary polysaccharides, disclosed the contributions of targeted species to fiber degradation. Our approach, including the use of bead-based biosensors, defines nutrient-harvesting strategies that underlie, as well as alleviate, competition between Bacteroides and control the selectivity of MDF components.

Persistent species relationships characterize migrating bird communities across stopover sites and seasons.

Global migrations of diverse animal species often converge along the same routes, bringing together seasonal assemblages of animals that may compete, prey on each other, and share information or pathogens. These interspecific interactions, when energetic demands are high and the time to complete journeys is short, may influence survival, migratory success, stopover ecology, and migratory routes. Numerous accounts suggest that interspecific co-migrations are globally distributed in aerial, aquatic, and terrestrial systems, although the study of migration to date has rarely investigated species interactions among migrating animals. Here, we test the hypothesis that migrating animals are communities engaged in networks of ecological interactions. We leverage over half a million records of 50 bird species from five bird banding sites collected over 8 to 23 y to test for species associations using social network analyses. We find strong support for persistent species relationships across sites and between spring and fall migration. These relationships may be ecologically meaningful: They are often stronger among phylogenetically related species with similar foraging behaviors and nonbreeding ranges even after accounting for the nonsocial contributions to associations, including overlap in migration timing and habitat use. While interspecific interactions could result in costly competition or beneficial information exchange, we find that relationships are largely positive, suggesting limited competitive exclusion at the scale of a banding station during migratory stopovers. Our findings support an understanding of animal migrations that consist of networked communities rather than random assemblages of independently migrating species, encouraging future studies of the nature and consequences of co-migrant interactions.

A mutant fitness assay identifies bacterial interactions in a model ocean hot spot.

Bacteria that assemble in phycospheres surrounding living phytoplankton cells metabolize a substantial proportion of ocean primary productivity. Yet the type and extent of interactions occurring among species that colonize these micron-scale "hot spot" environments are challenging to study. We identified genes that mediate bacterial interactions in phycosphere communities by culturing a transposon mutant library of copiotrophic bacterium Ruegeria pomeroyi DSS-3 with the diatom Thalassiosira pseudonana CCMP1335 as the sole source of organic matter in the presence or absence of other heterotrophic bacterial species. The function of genes having significant effects on R. pomeroyi fitness indicated explicit cell-cell interactions initiated in the multibacterial phycospheres. We found that R. pomeroyi simultaneously competed for shared substrates while increasing reliance on substrates that did not support the other species' growth. Fitness outcomes also indicated that the bacterium competed for nitrogen in the forms of ammonium and amino acids; obtained purines, pyrimidines, and cofactors via crossfeeding; both initiated and defended antagonistic interactions; and sensed an environment with altered oxygen and superoxide levels. The large genomes characteristic of copiotrophic marine bacteria are hypothesized to enable responses to dynamic ecological challenges occurring at the scale of microns. Here, we discover >200 nonessential genes implicated in the management of fitness costs and benefits of membership in a globally significant bacterial community.

Inducible CRISPR-targeted "knockdown" of human gut Bacteroides in gnotobiotic mice discloses glycan utilization strategies.

Understanding how members of the human gut microbiota prioritize nutrient resources is one component of a larger effort to decipher the mechanisms defining microbial community robustness and resiliency in health and disease. This knowledge is foundational for development of microbiota-directed therapeutics. To model how bacteria prioritize glycans in the gut, germfree mice were colonized with 13 human gut bacterial strains, including seven saccharolytic Bacteroidaceae species. Animals were fed a Western diet supplemented with pea fiber. After community assembly, an inducible CRISPR-based system was used to selectively and temporarily reduce the absolute abundance of Bacteroides thetaiotaomicron or B. cellulosilyticus by 10- to 60-fold. Each knockdown resulted in specific, reproducible increases in the abundances of other Bacteroidaceae and dynamic alterations in their expression of genes involved in glycan utilization. Emergence of these "alternate consumers" was associated with preservation of community saccharolytic activity. Using an inducible system for CRISPR base editing in vitro, we disrupted translation of transporters critical for utilizing dietary polysaccharides in Phocaeicola vulgatus, a B. cellulosilyticus knockdown-responsive taxon. In vitro and in vivo tests of the resulting P. vulgatus mutants allowed us to further characterize mechanisms associated with its increased fitness after knockdown. In principle, the approach described can be applied to study utilization of a range of nutrients and to preclinical efforts designed to develop therapeutic strategies for precision manipulation of microbial communities.

Frugivore-mediated seed dispersal in fragmented landscapes: Compositional and functional turnover from forest to matrix.

Seed dispersal by frugivores is a fundamental function for plant community dynamics in fragmented landscapes, where forest remnants are typically embedded in a matrix of anthropogenic habitats. Frugivores can mediate both connectivity among forest remnants and plant colonization of the matrix. However, it remains poorly understood how frugivore communities change from forest to matrix due to the loss or replacement of species with traits that are less advantageous in open habitats and whether such changes ultimately influence the composition and traits of dispersed plants via species interactions. Here, we close this gap by using a unique dataset of seed-dispersal networks that were sampled in forest patches and adjacent matrix habitats of seven fragmented landscapes across Europe. We found a similar diversity of frugivores, plants, and interactions contributing to seed dispersal in forest and matrix, but a high turnover (replacement) in all these components. The turnover of dispersed seeds was smaller than that of frugivore communities because different frugivore species provided complementary seed dispersal in forest and matrix. Importantly, the turnover involved functional changes toward larger and more mobile frugivores in the matrix, which dispersed taller, larger-seeded plants with later fruiting periods. Our study provides a trait-based understanding of frugivore-mediated seed dispersal through fragmented landscapes, uncovering nonrandom shifts that can have cascading consequences for the composition of regenerating plant communities. Our findings also highlight the importance of forest remnants and frugivore faunas for ecosystem resilience, demonstrating a high potential for passive forest restoration of unmanaged lands in the matrix.

Diet-driven differential response of Akkermansia muciniphila modulates pathogen susceptibility.

The erosion of the colonic mucus layer by a dietary fiber-deprived gut microbiota results in heightened susceptibility to an attaching and effacing pathogen, Citrobacter rodentium. Nevertheless, the questions of whether and how specific mucolytic bacteria aid in the increased pathogen susceptibility remain unexplored. Here, we leverage a functionally characterized, 14-member synthetic human microbiota in gnotobiotic mice to deduce which bacteria and functions are responsible for the pathogen susceptibility. Using strain dropouts of mucolytic bacteria from the community, we show that Akkermansia muciniphila renders the host more vulnerable to the mucosal pathogen during fiber deprivation. However, the presence of A. muciniphila reduces pathogen load on a fiber-sufficient diet, highlighting the context-dependent beneficial effects of this mucin specialist. The enhanced pathogen susceptibility is not owing to altered host immune or pathogen responses, but is driven by a combination of increased mucus penetrability and altered activities of A. muciniphila and other community members. Our study provides novel insights into the mechanisms of how discrete functional responses of the same mucolytic bacterium either resist or enhance enteric pathogen susceptibility.

Food web rewiring drives long-term compositional differences and late-disturbance interactions at the community level.

Ecological communities are constantly exposed to multiple natural and anthropogenic disturbances. Multivariate composition (if recovered) has been found to need significantly more time to be regained after pulsed disturbance compared to univariate diversity metrics and functional endpoints. However, the mechanisms driving the different recovery times of communities to single and multiple disturbances remain unexplored. Here, we apply quantitative ecological network analyses to try to elucidate the mechanisms driving long-term community-composition dissimilarity and late-stage disturbance interactions at the community level. For this, we evaluate the effects of two pesticides, nutrient enrichment, and their interactions in outdoor mesocosms containing a complex freshwater community. We found changes in interactions strength to be strongly related to compositional changes and identified postdisturbance interaction-strength rewiring to be responsible for most of the observed compositional changes. Additionally, we found pesticide interactions to be significant in the long term only when both interaction strength and food-web architecture are reshaped by the disturbances. We suggest that quantitative network analysis has the potential to unveil ecological processes that prevent long-term community recovery.

Environmental control of marine phytoplankton stoichiometry in the North Atlantic Ocean.

The stoichiometric coupling of carbon to limiting nutrients in marine phytoplankton regulates the magnitude of biological carbon sequestration in the ocean. While clear links between plankton C:N ratios and environmental drivers have been identified, the nature and direction of these links, as well as their underlying physiological and ecological controls, remain uncertain. We show, with a well-constrained mechanistic model of plankton ecophysiology, that while nitrogen availability and temperature emerge as the main drivers of phytoplankton C:N stoichiometry in the North Atlantic, the biological mechanisms involved vary depending on the spatiotemporal scale and region considered. We find that phytoplankton C:N stoichiometry is overall controlled by nitrogen availability below 40° N, predominantly driven by ecoevolutionary shifts in the functional composition of the phytoplankton communities, while phytoplankton stoichiometric plasticity in response to dropping temperatures and increased grazing pressure dominates at higher latitudes. Our findings highlight the potential of "organisms-to-ecosystems" modeling approaches based on mechanistic models of plankton biology accounting for physiology, ecology, and trait evolution to explore and explain complex observational data and ultimately improve the predictions of global ocean models.

A taxonomy of multiple stable states in complex ecological communities.

Natural systems are built from multiple interconnected units, making their dynamics, functioning and fragility notoriously hard to predict. A fragility scenario of particular relevance concerns so-called regime shifts: abrupt transitions from healthy to degraded ecosystem states. An explanation for these shifts is that they arise as transitions between alternative stable states, a process that is well-understood in few-species models. However, how multistability upscales with system complexity remains a debated question. Here, we identify that four different multistability regimes generically emerge in models of species-rich communities and other archetypical complex biological systems assuming random interactions. Across the studied models, each regime consistently emerges under a specific interaction scheme and leaves a distinct set of fingerprints in terms of the number of observed states, their species richness and their response to perturbations. Our results help clarify the conditions and types of multistability that can be expected to occur in complex ecological communities.

Cooperative interactions between invader and resident microbial community members weaken the negative diversity-invasion relationship.

The negative diversity-invasion relationship observed in microbial invasion studies is commonly explained by competition between the invader and resident populations. However, whether this relationship is affected by invader-resident cooperative interactions is unknown. Using ecological and mathematical approaches, we examined the survival and functionality of Aminobacter niigataensis MSH1 to mineralize 2,6-dichlorobenzamide (BAM), a groundwater micropollutant affecting drinking water production, in sand microcosms when inoculated together with synthetic assemblies of resident bacteria. The assemblies varied in richness and in strains that interacted pairwise with MSH1, including cooperative and competitive interactions. While overall, the negative diversity-invasion relationship was retained, residents engaging in cooperative interactions with the invader had a positive impact on MSH1 survival and functionality, highlighting the dependency of invasion success on community composition. No correlation existed between community richness and the delay in BAM mineralization by MSH1. The findings suggest that the presence of cooperative residents can alleviate the negative diversity-invasion relationship.

Asymmetric Biotic Interactions Cannot Be Inferred Without Accounting for Priority Effects.

Understanding biotic interactions is a crucial goal in community ecology and species distribution modelling, and large strides have been made towards improving multivariate computational methods with the aim of quantifying biotic interactions and improving predictions of species occurrence. Yet, while considerable attention has been given to computational approaches and the interpretation of these quantitative tools, the importance of sampling design to reveal these biotic interactions has received little consideration. This study explores the influential role of priority effects, that is, the order of habitat colonisation, in shaping our ability to detect biotic interactions. Using a simple set of simulations, we demonstrate that commonly used cross-sectional co-occurrence data alone cannot be used to make reliable inferences on asymmetric biotic interactions, even if they perform well in predicting the occurrence of species. We then show how sampling designs that consider priority effects can recover the asymmetric effects that are lost when priority effects are ignored. Based on these findings, we urge for caution when drawing inferences on biotic interactions from cross-sectional binary co-occurrence data, and provide guidance on sampling designs that may provide the necessary data to tackle this longstanding challenge.

Arrive and wait: Inactive bacterial taxa contribute to perceived soil microbiome resilience after a multidecadal press disturbance.

Long-term (press) disturbances like the climate crisis and other anthropogenic pressures are fundamentally altering ecosystems and their functions. Many critical ecosystem functions, such as biogeochemical cycling, are facilitated by microbial communities. Understanding the functional consequences of microbiome responses to press disturbances requires ongoing observations of the active populations that contribute to functions. This study leverages a 7-year time series of a 60-year-old coal seam fire (Centralia, Pennsylvania, USA) to examine the resilience of soil bacterial microbiomes to a press disturbance. Using 16S rRNA and 16S rRNA gene amplicon sequencing, we assessed the interannual dynamics of the active subset and the 'whole' bacterial community. Contrary to our hypothesis, the whole communities demonstrated greater resilience than active subsets, suggesting that inactive members contributed to overall structural resilience. Thus, in addition to selection mechanisms of active populations, perceived microbiome resilience is also supported by mechanisms of dispersal, persistence, and revival from the local dormant pool.

Plant interaction networks reveal the limits of our understanding of diversity maintenance.

Species interactions are key drivers of biodiversity and ecosystem stability. Current theoretical frameworks for understanding the role of interactions make many assumptions which unfortunately, do not always hold in natural, diverse communities. This mismatch extends to annual plants, a common model system for studying coexistence, where interactions are typically averaged across environmental conditions and transitive competitive hierarchies are assumed to dominate. We quantify interaction networks for a community of annual wildflowers in Western Australia across a natural shade gradient at local scales. Whilst competition dominated, intraspecific and interspecific facilitation were widespread in all shade categories. Interaction strengths and directions varied substantially despite close spatial proximity and similar levels of local species richness, with most species interacting in different ways under different environmental conditions. Contrary to expectations, all networks were predominantly intransitive. These findings encourage us to rethink how we conceive of and categorize the mechanisms driving biodiversity in plant systems.

Consequences of Local Conspecific Density Effects for Plant Diversity and Community Dynamics.

Conspecific density dependence (CDD) in plant populations is widespread, most likely caused by local-scale biotic interactions, and has potentially important implications for biodiversity, community composition, and ecosystem processes. However, progress in this important area of ecology has been hindered by differing viewpoints on CDD across subfields in ecology, lack of synthesis across CDD-related frameworks, and misunderstandings about how empirical measurements of local CDD fit within the context of broader ecological theories on community assembly and diversity maintenance. Here, we propose a conceptual synthesis of local-scale CDD and its causes, including species-specific antagonistic and mutualistic interactions. First, we compare and clarify different uses of CDD and related concepts across subfields within ecology. We suggest the use of local stabilizing/destabilizing CDD to refer to the scenario where local conspecific density effects are more negative/positive than heterospecific effects. Second, we discuss different mechanisms for local stabilizing and destabilizing CDD, how those mechanisms are interrelated, and how they cut across several fields of study within ecology. Third, we place local stabilizing/destabilizing CDD within the context of broader ecological theories and discuss implications and challenges related to scaling up the effects of local CDD on populations, communities, and metacommunities. The ultimate goal of this synthesis is to provide a conceptual roadmap for researchers studying local CDD and its implications for population and community dynamics.

A quantitative framework for identifying the role of individual species in Nature's Contributions to People.

It is widely acknowledged that biodiversity change is affecting human well-being by altering the supply of Nature's Contributions to People (NCP). Nevertheless, the role of individual species in this relationship remains obscure. In this article, we present a framework that combines the cascade model from ecosystem services research with network theory from community ecology. This allows us to quantitatively link NCP demanded by people to the networks of interacting species that underpin them. We show that this "network cascade" framework can reveal the number, identity and importance of the individual species that drive NCP and of the environmental conditions that support them. This information is highly valuable in demonstrating the importance of biodiversity in supporting human well-being and can help inform the management of biodiversity in social-ecological systems.

The Genetic Architecture of Adaptation to Leaf and Root Bacterial Microbiota in Arabidopsis thaliana.

Understanding the role of the host genome in modulating microbiota variation is a need to shed light on the holobiont theory and overcome the current limits on the description of host-microbiota interactions at the genomic and molecular levels. However, the host genetic architecture structuring microbiota is only partly described in plants. In addition, most association genetic studies on microbiota are often carried out outside the native habitats where the host evolves and the identification of signatures of local adaptation on the candidate genes has been overlooked. To fill these gaps and dissect the genetic architecture driving adaptive plant-microbiota interactions, we adopted a genome-environment association (GEA) analysis on 141 whole-genome sequenced natural populations of Arabidopsis thaliana characterized in situ for their leaf and root bacterial communities in fall and spring, and a large range of nonmicrobial ecological factors (i.e., climate, soil, and plant communities). A much higher fraction of among-population microbiota variance was explained by the host genetics than by nonmicrobial ecological factors. Importantly, the relative importance of host genetics and nonmicrobial ecological factors in explaining the presence of particular operational taxonomic units (OTUs) differs between bacterial families and genera. In addition, the polygenic architecture of adaptation to bacterial communities was highly flexible between plant compartments and seasons. Relatedly, signatures of local adaptation were stronger on quantitative trait loci (QTLs) of the root microbiota in spring. Finally, plant immunity appears as a major source of adaptive genetic variation structuring bacterial assemblages in A. thaliana.

Parameter Sensitivity of Transient Community Dynamics.

AbstractTransient dynamics have always intrigued ecologists, but current rapid environmental change (inducing transients even in previously undisturbed systems) has highlighted their importance more than ever. Here, I introduce a method for analyzing the sensitivity of transient ecological dynamics to parameter perturbations. The question the method answers is: how would the community dynamics have unfolded for some time horizon had the parameters been slightly different? I apply the method to three empirically parameterized models: competition between native forbs and exotic grasses in California, a host-parasitoid system, and an experimental chemostat predator-prey model. These applications showcase the ecological insights one can gain from models using transient sensitivity analysis. First, one can find parameters and their combinations whose perturbations disproportionately affect a system. Second, one can identify particular windows of time during which the predicted deviation from the unperturbed trajectories is especially large and utilize this information for management purposes. Third, there is an inverse relationship between transient and long-term sensitivities whenever the interacting populations are ecologically similar; paradoxically, the smaller the immediate response of the system, the more extreme its long-term response will be.

Assembly, Persistence, and Disassembly Dynamics of Quaternary Caribbean Frugivore Communities.

AbstractHow communities assemble and restructure is of critical importance to ecological theory, evolutionary theory, and conservation, but long-term perspectives on the patterns and processes of community assembly are rarely integrated into traditional community ecology, and the utility of communities as an ecological concept has been repeatedly questioned in part because of a lack of temporal perspective. Through a synthesis of paleontological and neontological data, I reconstruct Caribbean frugivore communities over the Quaternary (2.58 million years ago to present). Numerous Caribbean frugivore lineages arise during periods coincident with the global origins of plant-frugivore mutualisms. The persistence of many of these lineages into the Quaternary is indicative of long-term community stability, but an analysis of Quaternary extinctions reveals a nonrandom loss of large-bodied mammalian and reptilian frugivores. Anthropogenic impacts, including human niche construction, underlie the recent reorganization of frugivore communities, setting the stage for continued declines and evolutionary responses in plants that have lost mutualistic partners. These impacts also support ongoing and future introductions of invader complexes: introduced plants and frugivores that further exacerbate native biodiversity loss by interacting more strongly with one another than with native plants or frugivores. This work illustrates the importance of paleontological data and perspectives in conceptualizing ecological communities, which are dynamic and important entities.

Environmental drivers of Arctic communities based on metabarcoding of marine sediment eDNA.

Our ability to assess biodiversity at relevant spatial and temporal scales for informing management is of increasing importance given this is foundational to identify and mitigate the impacts of global change. Collecting baseline information and tracking ecological changes are particularly important for areas experiencing rapid changes and representing data gaps such as Arctic marine ecosystems. Environmental DNA has the potential to provide such data. We extracted environmental DNA from 90 surface sediment samples to assess eukaryote diversity around Greenland and Svalbard using two separate primer pairs amplifying different sections of the 18S rRNA gene. We detected 27 different phyla and 99 different orders and found that temperature and the change in temperature explained the most variation in the community in a single linear model, while latitude, sea ice cover and change in temperature explained the most variation in the community when assessed by individual non-linear models. We identified potential indicator taxa for Arctic climate change, including a terebellid annelid worm. In conclusion, our study demonstrates that environmental DNA offers a feasible method to assess biodiversity and identifies warming as a key driver of differences in biodiversity across these remote ecosystems.