The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata

Abstract

Background Lichens, encompassing 20,000 known species, are symbioses between specialized fungi (mycobionts), mostly ascomycetes, and unicellular green algae or cyanobacteria (photobionts). Here we describe the first parallel genomic analysis of the mycobiont Cladonia grayi and of its green algal photobiont Asterochloris glomerata . We focus on genes/predicted proteins of potential symbiotic significance, sought by surveying proteins differentially activated during early stages of mycobiont and photobiont interaction in coculture, expanded or contracted protein families, and proteins with differential rates of evolution. Results A) In coculture, the fungus upregulated small secreted proteins, membrane transport proteins, signal transduction components, extracellular hydrolases and, notably, a ribitol transporter and an ammonium transporter, and the alga activated DNA metabolism, signal transduction, and expression of flagellar components. B) Expanded fungal protein families include heterokaryon incompatibility proteins, polyketide synthases, and a unique set of G-protein α subunit paralogs. Expanded algal protein families include carbohydrate active enzymes and a specific subclass of cytoplasmic carbonic anhydrases. The alga also appears to have acquired by horizontal gene transfer from prokaryotes novel archaeal ATPases and Desiccation-Related Proteins. Expanded in both symbionts are signal transduction components, ankyrin domain proteins and transcription factors involved in chromatin remodeling and stress responses. The fungal transportome is contracted, as are algal nitrate assimilation genes. C) In the mycobiont, slow-evolving proteins were enriched for components involved in protein translation, translocation and sorting. Conclusions The surveyed genes affect stress resistance, signaling, genome reprogramming, nutritional and structural interactions. The alga carries many genes likely transferred horizontally through viruses, yet we found no evidence of inter-symbiont gene transfer. The presence in the photobiont of meiosis-specific genes supports the notion that sexual reproduction occurs in Asterochloris while they are free-living, a phenomenon with implications for the adaptability of lichens and the persistent autonomy of the symbionts. The diversity of the genes affecting the symbiosis suggests that lichens evolved by accretion of many scattered regulatory and structural changes rather than through introduction of a few key innovations. This predicts that paths to lichenization were variable in different phyla, which is consistent with the emerging consensus that ascolichens could have had a few independent origins. Electronic supplementary material The online version of this article (10.1186/s12864-019-5629-x) contains supplementary material, which is available to authorized users.

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

“…(Figure 3e and Table 7). Previous genetic studies on early stages of lichenization reported increased expression of fungal ammonium transporter genes (11,13). However in the present study fungal ammonium transporter genes showed no up-regulated expression in neither resynthesized nor natural symbiotic state relative to the non-symbiotic state.…”

“…In line with their nding we identi ed three AmLAT2-like genes in the fungal transcriptome, two of which (Uhk_000003 and Uhk_000004) were up-regulated in the symbiotic states. Armaleo et al (13) reported that one of the ve putative ribitol transporters found in the C. grayi genome was induced in the early stage of lichenization. The up-regulated gene expression of the ribitol transporters in the early and late stages of lichenization may indicate their fundamental roles in lichenization (Figure 3c).…”

“…The comparative transcriptomic analysis between the non-symbiotic state and the two symbiotic states can identify sets of fungal and algal genes that show up-or down-regulation in the symbiotic states. Predicted functions of the genes can indicate their relevance to symbiosis-speci c features of lichens as presented in previous studies on early stages of lichenization (12,13).…”

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

“…(Figure 3e and Table 7). Previous genetic studies on early stages of lichenization reported increased expression of fungal ammonium transporter genes (11,13). However in the present study fungal ammonium transporter genes showed no up-regulated expression in either the resynthesized or the natural symbiotic state relative to the non-symbiotic state.…”

“…mycobionts and photobionts have been reported as those likely to function in lichen symbioses (11)(12)(13).…”