Exploring Microbiome Functional Dynamics Through Space and Time with Trait-Based Theory

Microbiomes play essential roles in the health and function of animal and plant hosts and drive nutrient cycling across ecosystems. Integrating novel trait-based approaches with ecological theory can facilitate the prediction of microbial functional traits important for ecosystem functioning and health. In particular, the yield-acquisition-stress (Y-A-S) framework considers dominant microbial life history strategies across gradients of resource availability and stress. However, microbiomes are dynamic, and spatial and temporal shifts in taxonomic and trait composition can affect ecosystem functions. We posit that extending the Y-A-S framework to microbiomes during succession and across biogeographic gradients can lead to generalizable rules for how microbiomes and their functions respond to resources and stress across space, time, and diverse ecosystems. We demonstrate the potential of this framework by applying it to the microbiomes hosted by the carnivorous pitcher plant Sarracenia purpurea, which have clear successional trajectories and are distributed across a broad climatic gradient

Characterization and Comparison of Convergence Among \u3cem\u3eCephalotus follicularis\u3c/em\u3e Pitcher Plant-Associated Communities with Those of \u3cem\u3eNepenthes\u3c/em\u3e and \u3cem\u3eSarracenia\u3c/em\u3e Found Worldwide

The Albany pitcher plant, Cephalotus follicularis, has evolved cup-shaped leaves and a carnivorous habit completely independently from other lineages of pitcher plants. It is the only species in the family Cephalotaceae and is restricted to a small region of Western Australia. Here, we used metabarcoding to characterize the bacterial and eukaryotic communities living in C. follicularis pitchers at two different sites. Bacterial and eukaryotic communities were correlated in both richness and composition; however, the factors associated with richness were not the same across bacteria and eukaryotes, with bacterial richness differing with fluid color, and eukaryotic richness differing with the concentration of DNA extracted from the fluid, a measure roughly related to biomass. For turnover in composition, the variation in both bacterial and eukaryotic communities primarily differed with fluid acidity, fluid color, and sampling site. We compared C. follicularis-associated community diversity with that of Australian Nepenthes mirabilis, as well as a global comparison of Southeast Asian Nepenthes and North American Sarracenia. Our results showed similarity in richness with communities from other pitcher plants, and specific bacterial taxa shared among all three independent lineages of pitcher plants. Overall, we saw convergence in richness and particular clades colonizing pitcher plants around the world, suggesting that these highly specialized habitats select for certain numbers and types of inhabitants

Dissecting host-associated communities with DNA barcodes

DNA barcoding and metabarcoding methods have been invaluable in the study of interactions between host organisms and their symbiotic communities. Barcodes can help identify individual symbionts that are difficult to distinguish using morphological characters, and provide a way to classify undescribed species. Entire symbiont communities can be characterized rapidly using barcoding and especially metabarcoding methods, which is often crucial for isolating ecological signal from the substantial variation among individual hosts. Furthermore, barcodes allow the evolutionary histories of symbionts and their hosts to be assessed simultaneously and in reference to one another. Here, we describe three projects illustrating the utility of barcodes for studying symbiotic interactions: first, we consider communities of arthropods found in the ant-occupied domatia of the East African ant-plant Vachellia (Acacia) drepanolobium; second, we examine communities of arthropod and protozoan inquilines in three species of Nepenthes pitcher plant in South East Asia; third, we investigate communities of gut bacteria of South American ants in the genus Cephalotes. Advances in sequencing and computation, and greater database connectivity, will continue to expand the utility of barcoding methods for the study of species interactions, especially if barcoding can be approached flexibly by making use of alternative genetic loci, metagenomes and whole-genome data. This article is part of the themed issue ‘From DNA barcodes to biomes’

Exploring Microbiome Functional Dynamics through Space and Time with Trait-Based Theory

Microbiomes play essential roles in the health and function of animal and plant hosts and drive nutrient cycling across ecosystems. Integrating novel trait-based approaches with ecological theory can facilitate the prediction of microbial functional traits important for ecosystem functioning and health. In particular, the yield-acquisition-stress (Y-A-S) framework considers dominant microbial life history strategies across gradients of resource availability and stress. However, microbiomes are dynamic, and spatial and temporal shifts in taxonomic and trait composition can affect ecosystem functions. We posit that extending the Y-A-S framework to microbiomes during succession and across biogeographic gradients can lead to generalizable rules for how microbiomes and their functions respond to resources and stress across space, time, and diverse ecosystems. We demonstrate the potential of this framework by applying it to the microbiomes hosted by the carnivorous pitcher plant Sarracenia purpurea, which have clear successional trajectories and are distributed across a broad climatic gradient

Origin and Examination of a Leafhopper Facultative Endosymbiont

Eukaryotes engage in intimate interactions with microbes that range in age and type of association. Although many conspicuous examples of ancient insect associates are studied (e.g., Buchneraaphidicola), fewer examples of younger associations are known. Here, we further characterize a recently evolved bacterial endosymbiont of the leafhopper Euscelidius variegatus (Hemiptera, Cicadellidae), called BEV. We found that BEV, continuously maintained in E. variegatus hosts at UC Berkeley since 1984, is vertically transmitted with high fidelity. Unlike many vertically transmitted, ancient endosymbioses, the BEV–E. variegatus association is not obligate for either partner, and BEV can be cultivated axenically. Sufficient BEV colonies were grown and harvested to estimate its genome size and provide a partial survey of the genome sequence. The BEV chromosome is about 3.8 Mbp, and there is evidence for an extrachromosomal element roughly 53 kb in size (e.g., prophage or plasmid). We sequenced 438 kb of unique short-insert clones, representing about 12% of the BEV genome. Nearly half of the gene fragments were similar to mobile DNA, including 15 distinct types of insertion sequences (IS). Analyses revealed that BEV not only shares virulence genes with plant pathogens, but also is closely related to the plant pathogenic genera Dickeya, Pectobacterium, and Brenneria. However, the slightly reduced genome size, abundance of mobile DNA, fastidious growth in culture, and efficient vertical transmission suggest that symbiosis with E. variegatus has had a significant impact on genome evolution in BEV

Context-Dependent Dynamics Lead to the Assembly of Functionally Distinct Microbial Communities

Niche construction through interspecific interactions can condition future community states on past ones. However, the extent to which such history dependency can steer communities towards functionally different states remains a subject of active debate. Using bacterial communities collected from wild pitchers of the carnivorous pitcher plant, Sarracenia purpurea, we test the effects of history on composition and function across communities assembled in synthetic pitcher plant microcosms. We find that the diversity of assembled communities is determined by the diversity of the system at early, pre-assembly stages. Species composition is also contingent on early community states, not only because of differences in the species pool, but also because the same species have different dynamics in different community contexts. Importantly, compositional differences are proportional to differences in function, as profiles of resource use are strongly correlated with composition, despite convergence in respiration rates. Early differences in community structure can thus propagate to mature communities, conditioning their functional repertoire

Tropical Pitcher Plants (\u3cem\u3eNepenthes\u3c/em\u3e) Act as Ecological Filters by Altering Properties of Their Fluid Microenvironments

Characteristics of host species can alter how other, interacting species assemble into communities by acting as ecological filters. Pitchers of tropical pitcher plants (Nepenthes) host diverse communities of aquatic arthropods and microbes in nature. This plant genus exhibits considerable interspecific diversity in morphology and physiology; for example, different species can actively control the pH of their pitcher fluids and some species produce viscoelastic fluids. Our study investigated the extent to which Nepenthes species differentially regulate pitcher fluid traits under common garden conditions, and the effects that these trait differences had on their associated communities. Sixteen species of Nepenthes were reared together in the controlled environment of a glasshouse using commonly-sourced pH 6.5 water. We analyzed their bacterial and eukaryotic communities using metabarcoding techniques, and found that different plant species differentially altered fluid pH, viscosity, and color, and these had strong effects on the community structure of their microbiota. Nepenthes species can therefore act as ecological filters, cultivating distinctive microbial communities despite similar external conditions, and blurring the conceptual line between biotic and abiotic filters

Quantifying the Relative Importance of Variation in Predation and the Environment for Species Coexistence

Coexistence and food web theory are two cornerstones of the long‐standing effort to understand how species coexist. Although competition and predation are known to act simultaneously in communities, theory and empirical study of these processes continue to be developed largely independently. Here, we integrate modern coexistence theory and food web theory to simultaneously quantify the relative importance of predation and environmental fluctuations for species coexistence. We first examine coexistence in a theoretical, multitrophic model, adding complexity to the food web using machine learning approaches. We then apply our framework to a stochastic model of the rocky intertidal food web, partitioning empirical coexistence dynamics. We find the main effects of both environmental fluctuations and variation in predator abundances contribute substantially to species coexistence. Unexpectedly, their interaction tends to destabilise coexistence, leading to new insights about the role of bottom‐up vs. top‐down forces in both theory and the rocky intertidal ecosystem