Metabolic similarity and the predictability of microbial community assembly.

When microbial communities form, their composition is shaped by selective pressures imposed by the environment. Can we predict which communities will assemble under different environmental conditions? Here, we hypothesize that quantitative similarities in metabolic traits across metabolically similar environments lead to predictable similarities in community composition. To that end, we measured the growth rate and by-product profile of a library of proteobacterial strains in a large number of single nutrient environments. We found that growth rates and secretion profiles were positively correlated across environments when the supplied substrate was metabolically similar. By analyzing hundreds of in-vitro communities experimentally assembled in an array of different synthetic environments, we then show that metabolically similar substrates select for taxonomically similar communities. These findings lead us to propose and then validate a comparative approach for quantitatively predicting the effects of novel substrates on the composition of complex microbial consortia.

Nature, Data, and Power: How Hegemonies Shaped This Special Section.

AbstractSystems of oppression-racism, colonialism, misogyny, cissexism, ableism, heteronormativity, and more-have long shaped the content and practice of science. But opportunities to reckon with these influences are rarely found within academic science, even though such critiques are well developed in the social sciences and humanities. In this special section, we attempt to bring cross-disciplinary conversations among ecology, evolution, behavior, and genetics on the one hand and critical perspectives from the social sciences and humanities on the other into the pages-and in front of the readers-of a scientific journal. In this introduction to the special section, we recount and reflect on the process of running this cross-disciplinary experiment to confront harms done in the name of science and envision alternatives.

Functional attractors in microbial community assembly.

For microbiome biology to become a more predictive science, we must identify which descriptive features of microbial communities are reproducible and predictable, which are not, and why. We address this question by experimentally studying parallelism and convergence in microbial community assembly in replicate glucose-limited habitats. Here, we show that the previously observed family-level convergence in these habitats reflects a reproducible metabolic organization, where the ratio of the dominant metabolic groups can be explained from a simple resource-partitioning model. In turn, taxonomic divergence among replicate communities arises from multistability in population dynamics. Multistability can also lead to alternative functional states in closed ecosystems but not in metacommunities. Our findings empirically illustrate how the evolutionary conservation of quantitative metabolic traits, multistability, and the inherent stochasticity of population dynamics, may all conspire to generate the patterns of reproducibility and variability at different levels of organization that are commonplace in microbial community assembly.

The Macroevolutionary Consequences of Niche Construction in Microbial Metabolism.

Microorganisms display a stunning metabolic diversity. Understanding the origin of this diversity requires understanding how macroevolutionary processes such as innovation and diversification play out in the microbial world. Metabolic networks, which govern microbial resource use, can evolve through different mechanisms, e.g., horizontal gene transfer or de novo evolution of enzymes and pathways. This process is governed by a combination of environmental factors, selective pressures, and the constraints imposed by the genetic architecture of metabolic networks. In addition, many independent results hint that the process of niche construction, by which organisms actively modify their own and each other's niches and selective pressures, could play a major role in microbial innovation and diversification. Yet, the general principles by which niche construction shapes microbial macroevolutionary patterns remain largely unexplored. Here, we discuss several new hypotheses and directions, and suggest metabolic modeling methods that could allow us to explore large-scale empirical genotype-phenotype-(G-P)-environment spaces in order to study the macroevolutionary effects of niche construction. We hope that this short piece will further stimulate a systematic and quantitative characterization of macroevolutionary patterns and processes in microbial metabolism.

Microbial effects on plant phenology and fitness.

Plant development and the timing of developmental events (phenology) are tightly coupled with plant fitness. A variety of internal and external factors determine the timing and fitness consequences of these life-history transitions. Microbes interact with plants throughout their life history and impact host phenology. This review summarizes current mechanistic and theoretical knowledge surrounding microbe-driven changes in plant phenology. Overall, there are examples of microbes impacting every phenological transition. While most studies have focused on flowering time, microbial effects remain important for host survival and fitness across all phenological phases. Microbe-mediated changes in nutrient acquisition and phytohormone signaling can release plants from stressful conditions and alter plant stress responses inducing shifts in developmental events. The frequency and direction of phenological effects appear to be partly determined by the lifestyle and the underlying nature of a plant-microbe interaction (i.e., mutualistic or pathogenic), in addition to the taxonomic group of the microbe (fungi vs. bacteria). Finally, we highlight biases, gaps in knowledge, and future directions. This biotic source of plasticity for plant adaptation will serve an important role in sustaining plant biodiversity and managing agriculture under the pressures of climate change.

Chasing Ghosts: Race, Racism, and the Future of Microbiome Research.

In this article, we argue that a careful examination of human microbiome science's relationship with race and racism is necessary to foster equitable social and ecological relations in the field. We point to the origins and evolution of the problematic use of race in microbiome literature by demonstrating the increased usage of race both explicitly and implicitly in and beyond the human microbiome sciences. We demonstrate how these uses limit the future of rigorous and just microbiome research. We conclude with an outline of alternative actionable ways to build a more effective, antiracist microbiome science.

Model Systems in Ecology, Evolution, and Behavior: A Call for Diversity in Our Model Systems and Discipline.

AbstractEcologists and evolutionary biologists are fascinated by life's variation but also seek to understand phenomena and mechanisms that apply broadly across taxa. Model systems can help us extract generalities from amid all the wondrous diversity, but only if we choose and develop them carefully, use them wisely, and have a range of model systems from which to choose. In this introduction to the Special Feature on Model Systems in Ecology, Evolution, and Behavior (EEB), we begin by grappling with the question, What is a model system? We then explore where our model systems come from, in terms of the skills and other attributes required to develop them and the historical biases that influence traditional model systems in EEB. We emphasize the importance of communities of scientists in the success of model systems-narrow scientific communities can restrict the model organisms themselves. We also consider how our discipline was built around one type of "model scientist"-a history still reflected in the field. This lack of diversity in EEB is unjust and also narrows the field's perspective, including by restricting the questions asked and talents used to answer them. Increasing diversity, equity, and inclusion will require acting at many levels, including structural changes. Diversity in EEB, in both model systems and the scientists who use them, strengthens our discipline.

Engineering complex communities by directed evolution.

Directed evolution has been used for decades to engineer biological systems at or below the organismal level. Above the organismal level, a small number of studies have attempted to artificially select microbial ecosystems, with uneven and generally modest success. Our theoretical understanding of artificial ecosystem selection is limited, particularly for large assemblages of asexual organisms, and we know little about designing efficient methods to direct their evolution. Here, we have developed a flexible modelling framework that allows us to systematically probe any arbitrary selection strategy on any arbitrary set of communities and selected functions. By artificially selecting hundreds of in silico microbial metacommunities under identical conditions, we first show that the main breeding methods used to date, which do not necessarily let communities reach their ecological equilibrium, are outperformed by a simple screen of sufficiently mature communities. We then identify a range of alternative directed evolution strategies that, particularly when applied in combination, are well suited for the top-down engineering of large, diverse and stable microbial consortia. Our results emphasize that directed evolution allows an ecological structure-function landscape to be navigated in search of dynamically stable and ecologically resilient communities with desired quantitative attributes.

Multi-Replicated Enrichment Communities as a Model System in Microbial Ecology.

Recent advances in robotics and affordable genomic sequencing technologies have made it possible to establish and quantitatively track the assembly of enrichment communities in high-throughput. By conducting community assembly experiments in up to thousands of synthetic habitats, where the extrinsic sources of variation among replicates can be controlled, we can now study the reproducibility and predictability of microbial community assembly at different levels of organization, and its relationship with nutrient composition and other ecological drivers. Through a dialog with mathematical models, high-throughput enrichment communities are bringing us closer to the goal of developing a quantitative predictive theory of microbial community assembly. In this short review, we present an overview of recent research on this growing field, highlighting the connection between theory and experiments and suggesting directions for future work.

Spatially explicit depiction of a floral epiphytic bacterial community reveals role for environmental filtering within petals.

The microbiome of flowers (anthosphere) is an understudied compartment of the plant microbiome. Within the flower, petals represent a heterogeneous environment for microbes in terms of resources and environmental stress. Yet, little is known of drivers of structure and function of the epiphytic microbial community at the within-petal scale. We characterized the petal microbiome in two co-flowering plants that differ in the pattern of ultraviolet (UV) absorption along their petals. Bacterial communities were similar between plant hosts, with only rare phylogenetically distant species contributing to differences. The epiphyte community was highly culturable (75% of families) lending confidence in the spatially explicit isolation and characterization of bacteria. In one host, petals were heterogeneous in UV absorption along their length, and in these, there was a negative relationship between growth rate and position on the petal, as well as lower UV tolerance in strains isolated from the UV-absorbing base than from UV reflecting tip. A similar pattern was not seen in microbes isolated from a second host whose petals had uniform patterning along their length. Across strains, the variation in carbon usage and chemical tolerance followed common phylogenetic patterns. This work highlights the value of petals for spatially explicit explorations of bacteria of the anthosphere.

Directed Evolution of Microbial Communities.

Directed evolution is a form of artificial selection that has been used for decades to find biomolecules and organisms with new or enhanced functional traits. Directed evolution can be conceptualized as a guided exploration of the genotype-phenotype map, where genetic variants with desirable phenotypes are first selected and then mutagenized to search the genotype space for an even better mutant. In recent years, the idea of applying artificial selection to microbial communities has gained momentum. In this article, we review the main limitations of artificial selection when applied to large and diverse collectives of asexually dividing microbes and discuss how the tools of directed evolution may be deployed to engineer communities from the top down. We conceptualize directed evolution of microbial communities as a guided exploration of an ecological structure-function landscape and propose practical guidelines for navigating these ecological landscapes.

Polyploid plants obtain greater fitness benefits from a nutrient acquisition mutualism.

Polyploidy is a key driver of ecological and evolutionary processes in plants, yet little is known about its effects on biotic interactions. This gap in knowledge is especially profound for nutrient acquisition mutualisms, despite the fact that they regulate global nutrient cycles and structure ecosystems. Generalism in mutualistic interactions depends on the range of potential partners (niche breadth), the benefits obtained and ability to maintain benefits across a variety of partners (fitness plasticity). Here, we determine how each of these is influenced by polyploidy in the legume-rhizobium mutualism. We inoculated a broad geographic sample of natural diploid and autotetraploid alfalfa (Medicago sativa) lineages with a diverse panel of Sinorhizobium bacterial symbionts. To analyze the extent and mechanism of generalism, we measured host growth benefits and functional traits. Autotetraploid plants obtained greater fitness enhancement from mutualistic interactions and were better able to maintain this across diverse rhizobial partners (i.e. low plasticity in fitness) relative to diploids. These benefits were not attributed to increases in niche breadth, but instead reflect increased rewards from investment in the mutualism. Polyploid plants displayed greater generalization in bacterial mutualisms relative to diploids, illustrating another axis of advantage for polyploids over diploids.

Why Evolve Reliance on the Microbiome for Timing of Ontogeny?

The timing of life history events has important fitness consequences. Since the 1950s, researchers have combined first principles and data to predict the optimal timing of life history transitions. Recently, a striking mystery has emerged. Such transitions can be shaped by a completely different branch of the tree of life: species in the microbiome. Probing these interactions using testable predictions from evolutionary theory could illuminate whether and how host-microbiome integrated life histories can evolve and be maintained. Beyond advancing fundamental science, this research program could yield important applications. In an age of microbiome engineering, understanding the contexts that lead to microbiota signaling shaping ontogeny could offer novel mechanisms for manipulations to increase yield in agriculture by manipulating plant responses to stressful environments, or to reduce pathogen transmission by affecting vector efficiency. We combine theory and evidence to illuminate the essential questions underlying the existence of microbiome-dependent ontogenetic timing (MiDOT) to fuel research on this emerging topic.

Floral organs act as environmental filters and interact with pollinators to structure the yellow monkeyflower (Mimulus guttatus) floral microbiome.

Assembly of microbial communities is the result of neutral and selective processes. However, the relative importance of these processes is still debated. Microbial communities of flowers, in particular, have gained recent attention because of their potential impact to plant fitness and plant-pollinator interactions. However, the role of selection and dispersal in the assembly of these communities remains poorly understood. Here, we evaluated the role of pollinator-mediated dispersal on the contribution of neutral and selective processes in the assembly of floral microbiomes of the yellow monkeyflower (Mimulus guttatus). We sampled floral organs from flowers in the presence and absence of pollinators within five different serpentine seeps in CA and obtained 16S amplicon data on the epiphytic bacterial communities. Consistent with strong microenvironment selection within flowers we observed significant differences in community composition across floral organs and only a small effect of geographic distance. Pollinator exposure affected the contribution of environmental selection and depended on the rate and intimacy of interactions with flower visitors. This study provides evidence of the importance of dispersal and within-flower heterogeneity in shaping epiphytic bacterial communities of flowers, and highlights the complex interplay between pollinator behaviour, environmental selection and additional abiotic factors in shaping the epiphytic bacterial communities of flowers.

Pollen on Stigmas of Herbarium Specimens: A Window into the Impacts of a Century of Environmental Disturbance on Pollen Transfer.

Pollination is necessary for plant reproduction but often highly susceptible to disruption, for example, by habitat fragmentation and climate change. Here, we indirectly evaluated on a century timescale pollination interactions for species in one of the historically most disturbed habitats on earth-tropical dry forests of Hawai'i. We employed a novel method for acquiring a historical perspective on temporal change in pollination by characterizing pollen on stigmas of herbarium specimens from six remnant native species collected from 1909-2002. We determine whether temporal shifts occurred in (1) pollination quantity and quality or (2) the composition of species interacting via pollen transfer. While pollen quantity remained constant, these remnant species interact with different species in modern times via pollen transfer than they did nearly 100 years ago. Species that are resilient to long-term environmental change may also be the ones subject to changes in pollination interactions.

Gazing into the anthosphere: considering how microbes influence floral evolution.

The flower is the hallmark of angiosperms and its evolution is key to their diversification. As knowledge of ecological interactions between flowers and their microbial communities (the anthosphere) expands, it becomes increasingly important to consider the evolutionary impacts of these associations and their potential eco-evolutionary dynamics. In this Viewpoint we synthesize current knowledge of the anthosphere within a multilevel selection framework and illustrate the potential for the extended floral phenotype (the phenotype expressed from the genes of the plant and its associated flower microbes) to evolve. We argue that flower microbes are an important, but understudied, axis of variation that shape floral trait evolution and angiosperm reproductive ecology. We highlight knowledge gaps and discuss approaches that are critical for gaining a deeper understanding of the role microbes play in mediating plant reproduction, ecology, and evolution.

Adaptation, chance, and history in experimental evolution reversals to unicellularity.

Evolution is often deemed irreversible. The evolution of complex traits that require many mutations makes their reversal unlikely. Even in simpler traits, reversals might become less likely as neutral or beneficial mutations, with deleterious effects in the ancestral context, become fixed in the novel background. This is especially true in changes that involve large reorganizations of the organism and its interactions with the environment. The evolution of multicellularity involves the reorganization of previously autonomous cells into a more complex organism; despite the complexity of this change, single cells have repeatedly evolved from multicellular ancestors. These repeated reversals to unicellularity undermine the generality of Dollo's law. In this article, we evaluated the dynamics of reversals to unicellularity from recently evolved multicellular phenotypes of the brewers yeast Saccharomyces cerevisae. Even though multicellularity in this system evolved recently, it involves the evolution of new levels of selection. Strong selective pressures against multicellularity lead to rapid reversibility to single cells in all of our replicate lines, whereas counterselection favoring multicellularity led to minimal reductions to the rates of reversal. History and chance played an important role in the tempo and mode of reversibility, highlighting the interplay of deterministic and stochastic events in evolutionary reversals.

The Cost of Being Big: Local Competition, Importance of Dispersal, and Experimental Evolution of Reversal to Unicellularity.

Multicellularity provides multiple benefits. Nonetheless, unicellularity is ubiquitous, and there have been multiple cases of evolutionary reversal to a unicellular organization. In this article, we explore some of the costs of multicellularity as well as the possibility and dynamics of evolutionary reversals to unicellularity. We hypothesize that recently evolved multicellular organisms would face a high cost of increased competition for local resources in spatially structured environments because of larger size and increased cell densities. To test this hypothesis we conducted competition assays, computer simulations, and selection experiments using isolates of Saccharomyces cerevisiae that recently evolved multicellularity. In well-mixed environments, multicellular isolates had lower growth rates relative to their unicellular ancestor because of limitations of space and resource acquisition. In structured environments with localized resources, cells in both multicellular and unicellular isolates grew at a similar rate. Despite similar growth, higher local density of cells in multicellular groups led to increased competition and higher fitness costs in spatially structured environments. In structured environments all of the multicellular isolates rapidly evolved a predominantly unicellular life cycle, while in well-mixed environments reversal was more gradual. Taken together, these results suggest that a lack of dispersal, leading to higher local competition, might have been one of the main constraints in the evolution of early multicellular forms.