Inter‐ and intraspecific phytochemical variation correlate with epiphytic flower and leaf bacterial communities

Abstract

Microbes associated with flowers and leaves affect plant health and fitness and modify the chemical phenotypes of plants with consequences for interactions of plants with their environment. However, the drivers of bacterial communities colonizing above‐ground parts of grassland plants in the field remain largely unknown. We therefore examined the relationships between phytochemistry and the epiphytic bacterial community composition of flowers and leaves of Ranunculus acris and Trifolium pratense. On 252 plant individuals, we characterized primary and specialized metabolites, that is, surface sugars, volatile organic compounds (VOCs), and metabolic fingerprints, as well as epiphytic flower and leaf bacterial communities. The genomic potential of bacterial colonizers concerning metabolic capacities was assessed using bacterial reference genomes. Phytochemical composition displayed pronounced variation within and between plant species and organs, which explained part of the variation in bacterial community composition. Correlation network analysis suggests strain‐specific correlations with metabolites. Analysis of bacterial reference genomes revealed taxon‐specific metabolic capabilities that corresponded with genes involved in glycolysis and adaptation to osmotic stress. Our results show relationships between phytochemistry and the flower and leaf bacterial microbiomes suggesting that plants provide chemical niches for distinct bacterial communities. In turn, bacteria may induce alterations in the plants' chemical phenotype. Thus, our study may stimulate further research on the mechanisms of trait‐based community assembly in epiphytic bacteria.

Adding experimental precision to the realism of field observations: Plant communities structure bacterial communities in a glacier forefield

“…By experimentally controlling plant species composition and richness, we can—to a large extent—exclude other factors apart from plant communities as causes for differences in bacterial communities at the end of the experiment. Plant species evolved multiple strategies to shape the microbes colonizing the soil that involve the plant immune system, phytohormone signalling and metabolites facilitating or preventing microbial growth indicating the plants' necessity to modulate the bacteria they interact with (Bulgarelli et al, 2013; Gaube et al, 2023; Junker & Tholl, 2013; Mesny et al, 2023). Bacteria often determine the fate of plants in ecosystems either by pathogenic functions reducing the plants' chance to establish or by growth‐promoting functions that provide higher competitive abilities (Berendsen et al, 2012; Delaux & Schornack, 2021).…”

“…Plant adaptations that facilitate the establishment of beneficial microbiota and those that restrict the growth of pathogens shape the microbial communities associated with plants and the surrounding substrate (Mesny et al, 2023). These adaptations involve the plant immune system, phytohormone signalling and metabolite‐mediated structuring mechanisms such as root exudates that shape plant species‐specific soil microbiomes (Bulgarelli et al, 2013; Gaube et al, 2023; Junker & Tholl, 2013; Mesny et al, 2023). Consequently, plant species composition has often been reported to explain variation in the composition of microbial communities (e.g.…”