Origin of earliest land plants from ancestral algae dramatically accelerated the evolution of Earth's terrestrial ecosystems, in which microbial symbioses have played key roles. Recent molecular diversification analyses identify the rare, geographically-limited moss Takakia as Earth's most archaic modern land plant. Despite occupying a phylogenetic position pivotal for understanding earliest plants, Takakia microbial associations are poorly known. Here, we describe symbiosis-related structural features and contig-based metagenomic data that illuminate the evolutionary transition from streptophyte algae to early embryophytes. We observed that T. lepidozioides shares with streptophyte algae secretion of microbe-harboring mucilage and bacterial taxa such as Rhizobium and genes indicating nitrogen fixation. We find that Takakia root-analogs produce lateral mucilage organs that are more complex than generally understood, having structural analogies to angiosperm lateral roots adapted for N-fixation symbioses, including presence of intracellular microbes. We also find structural and metagenomic evidence for mycorrhiza-like species of glomalean fungi (including Rhizophagus irregularis) not previously known for mosses, as well as ascomycete fungi (e.g. Rhizoscyphus ericae) that associate with other early-diverging plants. Because Takakia is the oldest known modern plant genus, this study of plants of a remote locale not strongly influenced by human activities may indicate microbiome features of early land plants.
© 2022. The Author(s).