A tale of two lineages: how the strains of the earliest divergent symbiotic Frankia clade spread over the world

Abstract

AbstractIt is currently assumed that around 100 million years ago, the common ancestor to the Fabales, Fagales, Rosales and Cucurbitales in Gondwana, developed a root nodule symbiosis with a nitrogen-fixing bacterium. The symbiotic trait evolved first inFrankiacluster-2; thus, strains belonging to this cluster are the best extant representatives of this original symbiont. Most cluster-2 strains could not be cultured to date, except forFrankia coriariae,and therefore many aspects of the symbiosis are still elusive. Based on phylogenetics of cluster-2 metagenome-assembled genomes (MAGs), it has been shown that the genomes of strains originating in Eurasia are highly conserved. These MAGs are more closely related toFrankiacluster-2 in North America than to the single genome available thus far from the southern hemisphere, i.e., from Papua New Guinea.To unravel more biodiversity withinFrankiacluster-2 and predict routes of dispersal from Gondwana, we sequenced and analysed the MAGs ofFrankiacluster-2 fromCoriaria japonicaandCoriaria intermediagrowing in Japan, Taiwan and the Philippines. Phylogenetic analyses indicate there is a clear split withinFrankiacluster-2, separating a continental from an island lineage. Presumably, these lineages already diverged in Gondwana.Based on fossil data on the host plants, we propose that these two lineages dispersed via at least two routes. While the continental lineage reached Eurasia together with their host plants via the Indian subcontinent, the island lineage spread towards Japan with an unknown host plant.