In vitro resynthesis of lichenization reveals the genetic background of symbiosis-specific fungal-algal interaction in Usnea hakonensis.

Abstract

Background Symbiosis is central to ecosystems and has been an important driving force of the diversity of life. Close and long-term interactions are known to develop cooperative molecular mechanisms between the symbiotic partners and have often given them new functions as symbiotic entities. In lichen symbiosis, mutualistic relationships between lichen-forming fungi and algae and/or cyanobacteria produce unique features that make lichens adaptive to wide range of environments. Although morphological, physiological, and ecological uniqueness of lichens have been described for more than a century, the genetic mechanisms underlying this symbiosis remain elusive. Results This study investigated the fungal-algal interaction specific to the symbiosis in lichen using Usnea hakonensis as a model system. The whole genome of U. hakonensis , the fungal partner, was sequenced by using the culture isolated from a natural lichen thallus. Isolated cultures of the fungal and the algal partners were co-cultured in vitro for three months, and the thalli were successfully resynthesized into visible protrusions. Transcriptomes of resynthesized and natural thalli (symbiotic states) were compared to that of isolated cultures (non-symbiotic state). Sets of fungal and algal genes up-regulated in both symbiotic states were identified as symbiosis-related genes. Conclusion From the predicted functions of these genes, we identified the genetic background of two key features fundamental to the symbiotic lifestyle in lichen. First is an establishment of fungal symbiotic interface: (a) modification of cell walls at fungal-algal contact sites; and (b) production of a hydrophobic layer that ensheaths fungal and algal cells;. Second is a symbiosis-specific nutrient flow: (a) the algal supply of photosynthetic product to the fungus; and (b) the fungal supply of phosphorous and nitrogen compounds to the alga. Since both features are widespread among lichens, our result may indicate important facets of the genetic basis of lichen symbiosis.