Bog ecosystems as a playground for plant-microbe coevolution: bryophytes and vascular plants harbour functionally adapted bacteria.

ABSTRACT

BACKGROUND: Bogs are unique ecosystems inhabited by distinctive, coevolved assemblages of organisms, which play a global role for carbon storage, climate stability, water quality and biodiversity. To understand ecology and plant-microbe co-occurrence in bogs, we selected 12 representative species of bryophytes and vascular plants and subjected them to a shotgun metagenomic sequencing approach. We explored specific plant-microbe associations as well as functional implications of the respective communities on their host plants and the bog ecosystem. RESULTS: Microbial communities were shown to be functionally adapted to their plant hosts; a higher colonization specificity was found for vascular plants. Bryophytes that commonly constitute the predominant Sphagnum layer in bogs were characterized by a higher bacterial richness and diversity. Each plant group showed an enrichment of distinct phylogenetic and functional bacterial lineages. Detailed analyses of the metabolic potential of 28 metagenome-assembled genomes (MAGs) supported the observed functional specification of prevalent bacteria. We found that novel lineages of Betaproteobacteria and Actinobacteria in the bog environment harboured genes required for carbon fixation via RuBisCo. Interestingly, several of the highly abundant bacteria in both plant types harboured pathogenicity potential and carried similar virulence factors as found with corresponding human pathogens. CONCLUSIONS: The unexpectedly high specificity of the plant microbiota reflects intimate plant-microbe interactions and coevolution in bog environments. We assume that the detected pathogenicity factors might be involved in coevolution processes, but the finding also reinforces the role of the natural plant microbiota as a potential reservoir for human pathogens. Overall, the study demonstrates how plant-microbe assemblages can ensure stability, functioning and ecosystem health in bogs. It also highlights the role of bog ecosystems as a playground for plant-microbe coevolution. Video abstract.