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ABSTRACT AimEcological theory suggests that dispersal limitation and selection by climatic factors influence bacterial community assembly at a continental scale, yet the conditions governing the relative importance of each process remains unclear. The carnivorous pitcher plantSarracenia purpureaprovides a model aquatic microecosystem to assess bacterial communities across the host plant's north–south range in North America. This study determined the relative influences of dispersal limitation and environmental selection on the assembly of bacterial communities inhabitingS. purpureapitchers at the continental scale. LocationEastern United States and Canada. Time Period2016. Major Taxa StudiedBacteria inhabitingS. purpureapitchers. MethodsPitcher morphology, fluid, inquilines and prey were measured, and pitcher fluid underwent DNA sequencing for bacterial community analysis. Null modelling of β‐diversity provided estimates for the contributions of selection and dispersal limitation to community assembly, complemented by an examination of spatial clustering of individuals. Phylogenetic and ecological associations of co‐occurrence network module bacteria was determined by assessing the phylogenetic diversity and habitat preferences of member taxa. ResultsDispersal limitation was evident from between‐site variation and spatial aggregation of individual bacterial taxa in theS. purpureapitcher system. Selection pressure was weak across the geographic range, yet network module analysis indicated environmental selection within subgroups. A group of aquatic bacteria held traits under selection in warmer, wetter climates, and midge abundance was associated with selection for traits held by a group of saprotrophs. Processes that increased pitcher fluid volume weakened selection in one module, possibly by supporting greater bacterial dispersal. ConclusionDispersal limitation governed bacterial community assembly inS. purpureapitchers at a continental scale (74% of between‐site comparisons) and was significantly greater than selection across the range. Network modules showed evidence for selection, demonstrating that multiple processes acted concurrently in bacterial community assembly at the continental scale. 

ABSTRACT Across diverse ecosystems, bacteria and their hosts engage in complex relationships having negative, neutral, or positive interactions. However, the specific effects of leaf-associated bacterial community functions on plant growth are poorly understood. Although microbes can promote plant growth through various biochemical mechanisms, investigating the community’s functional contributions to plant growth remains to be explored. To address this gap, we characterized the relationships between bacterial community function and host plant growth in the purple pitcher plant (Sarracenia purpurea). The main aim of our research was to investigate how different bacterial community functions affect the growth and nutrient content in the plant. Previous research has suggested that microbial communities aid in prey decomposition and subsequent nutrient acquisition in carnivorous plants, includingS. purpurea. However, the specific functional roles of bacterial communities in plant growth and nutrient uptake are not well known. In this study, sterile, freshly opened pitchers were inoculated with three functionally distinct, pre-assembled bacterial communities. Bacterial community composition and function were measured over 8 weeks using physiological assays, metagenomics, and metatranscriptomics. Distinct community functions affected plant traits; a bacterial community enriched in decomposition was associated with larger leaves with almost double the biomass of control pitchers. Physiological differences in bacterial communities were supported by metatranscriptomics; for example, the bacterial community with the highest chitinase activity had greater expression of transcripts associated with chitinase enzymes. The relationship between bacterial community function and plant growth observed here indicates potential mechanisms, such as chitinase activity, for host-associated bacterial functions to support pitcher plant growth. IMPORTANCEThis study addresses a gap in understanding the relationships between bacterial community function and plant growth. We inoculated sterile, freshly opened pitcher plant leaves with three functionally distinct bacterial communities to uncover potential mechanisms through which bacterial functions support plant health and growth. Our findings demonstrate that distinct community functions significantly influence plant traits, with some bacterial communities supporting more plant growth than in control pitchers. These results highlight the ecological roles of microbial communities in plants and thus ecosystems and suggest that nutrient cycling is an important pathway through which microbes support host plant health. This research provides valuable insights into plant-microbe interactions and the effects of diverse microbial community functions. 

Abstract Leaves of the carnivorous sundew plants (Droseraspp.) secrete mucilage that hosts microorganisms, but whether this microbiota contributes to prey digestion is unclear. We identified the acidophilic fungusAcrodontium crateriformeas the dominant species in the mucilage microbial communities, thriving in multiple sundew species across the global range. The fungus grows and sporulates on sundew glands as its preferred acidic environment, and its presence in traps increased the prey digestion process.A. crateriformehas a reduced genome similar to other symbiotic fungi. DuringA. crateriforme–Drosera spatulatacoexistence and digestion of prey insects, transcriptomes revealed significant gene co-option in both partners. Holobiont expression patterns during prey digestion further revealed synergistic effects in several gene families including fungal aspartic and sedolisin peptidases, facilitating prey digestion in leaves, as well as nutrient assimilation and jasmonate signalling pathway expression. This study establishes that botanical carnivory is defined by adaptations involving microbial partners and interspecies interactions. 

Understanding microbial roles in ecosystem function requires integrating microscopic processes into food webs. The carnivorous pitcher plant, Sarracenia purpurea, offers a tractable study system where diverse food webs of macroinvertebrates and microbes facilitate digestion of captured insect prey, releasing nutrients supporting the food web and host plant. However, how interactions between these macroinvertebrate and microbial communities contribute to ecosystem functions remains unclear. We examined the role of the pitcher plant mosquito, Wyeomyia smithii, in top-down control of the composition and function of pitcher plant microbial communities. Mosquito larval abundance was enriched or depleted across a natural population of S. purpurea pitchers over a 74-day field experiment. Bacterial community composition and microbial community function were characterized by 16S rRNA amplicon sequencing and profiling of carbon substrate use, bulk metabolic rate, hydrolytic enzyme activity, and macronutrient pools. Bacterial communities changed from pitcher opening to maturation, but larvae exerted minor effects on high-level taxonomic composition. Higher larval abundance was associated with lower diversity communities with distinct functions and elevated nitrogen availability. Treatment-independent clustering also supported roles for larvae in curating pitcher microbial communities through shifts in community diversity and function. These results demonstrate top-down control of microbial functions in an aquatic microecosystem. 

Processes influencing recruitment of diverse bacteria to plant microbiomes remain poorly understood. In the carnivorous pitcher plant Sarracenia purpurea model system, individual pitchers open to collect rainwater, invertebrates and a diverse microbial community, and this detrital food web is sustained by captured insect prey. This study examined how potential sources of bacteria affect the development of the bacterial community within pitchers, how the host plant tissue affects community development and how established vs. assembling communities differ. In a controlled greenhouse experiment, seven replicate pitchers were allocated to five treatments to exclude specific bacterial sources or host tissue: milliQ water only, milliQ + insect prey, rainwater + prey, established communities + prey, artificial pitchers with milliQ + prey. Community composition and functions were examined over 8–40 weeks using bacterial gene sequencing and functional predictions, measurements of cell abundance, hydrolytic enzyme activity and nutrient transformations. Distinct community composition and functional differences between artificial and real pitchers confirm an important influence of host plant tissue on community development, but also suggest this could be partially related to host nutrient uptake. Significant recruitment of bacteria to pitchers from air was evident from many taxa common to all treatments, overlap in composition between milliQ, milliQ + prey, and rainwater + prey treatments, and few taxa unique to milliQ only pitchers. Community functions measured as hydrolytic enzyme (chitinase, protease) activity suggested a strong influence of insect prey additions and were linked to rapid transformation of insect nutrients into dissolved and inorganic sources. Bacterial taxa found in 6 of 7 replicate pitchers within treatments, the “core microbiome” showed tighter successional trajectories over 8 weeks than all taxa. Established pitcher community composition was more stable over 8 weeks, suggesting a diversity-stability relationship and effect of microinvertebrates on bacteria. This study broadly demonstrates that bacterial composition in host pitcher plants is related to both stochastic and specific bacterial recruitment and host plants influence microbial selection and support microbiomes through capture of insect prey. 

ABSTRACT 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.