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Do lichens domesticate photobionts like farmers domesticate crops? Evidence from a previously unrecognized lineage of filamentous cyanobacteria.

Phylogenetic diversity of lichen photobionts is low compared to that of fungal counterparts. Most lichen fungi are thought to be associated with just four photobiont genera, among them the cyanobacteria Nostoc and Scytonema, two of the most important nitrogen fixers in humid ecosystems. Although many Nostoc photobionts have been identified using isolated cultures and sequences, the identity of Scytonema photobionts has never been confirmed by culturing or sequencing. We investigated the phylogenetic placement of presumed Scytonema photobionts and unicellular morphotypes previously assigned to Chroococcus, from tropical Dictyonema, Acantholichen, Coccocarpia, and Stereocaulon lichens. While we confirm that filamentous and unicellular photobiont morphotypes belong to a single clade, this clade does not cluster with Scytonema but represents a novel, previously unrecognized, highly diverse, exclusively lichenized lineage, for which the name Rhizonema is available. The phylogenetic structure observed in this novel lineage suggests absence of coevolution with associated mycobionts at the species or clade level. Instead, highly efficient photobiont strains appear to have evolved through photobiont sharing between unrelated, but ecologically similar, coexisting lineages of lichenized fungi ("lichen guilds"), via the selection of particular photobiont strains through and subsequent horizontal transfer among unrelated mycobionts, a phenomenon not unlike crop domestication.