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

Abstract

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.

Molecular phylogeny, morphology, pigment chemistry and ecology in Hygrophoraceae (Agaricales)

“…Lichenomphalia forms omphalinoid fruiting bodies associated with green, eukaryotic photobionts, whereas the Dictyonema s.l. clade (including Cyphellostereum, Acantholichen, Corella and Cora) features cyphelloid or corticioid basidiocarps and invariably associates with a novel cyanobacterial lineage, Rhizonema Lücking et al 2009). Both lineages are primarily tropical montane to temperate and often co-occur over soil and between bryophytes on the ground.…”

Population decline of endangered lichen Erioderma pedicellatum in Nova Scotia, Canada

“…Recent molecular study suggests that all lichenized Sctonema sp. studied so far are actually a new genetically distinct lichenized genus, Rhizonema (Lücking et al 2009). The thallus of E. pedicellatum is foliose with a diameter of 2-5 cm, occasionally reaching 12 cm.…”

New morphological aspects of cephalodium formation in the lichenLobaria pulmonaria(Lecanorales, Ascomycota)

“…Lichen-forming fungi seem to be highly selective in choosing their cyanobacterial partner because only a few closely related Nostoc strains typically serve as the appropriate symbiotic partner for each fungal species (Paulsrud et al 1998(Paulsrud et al , 2000Lohtander et al 2003;Stenroos et al 2006;Myllys et al 2007;Lü cking et al 2009;Rikkinen 2009). However, Lobaria pulmonaria and Peltigera venosa are exceptions to this rule.…”