Evolutionary biology of lichen symbioses

Abstract

Lichens are the symbiotic outcomes of open, interspecies relationships, central to which are a fungus and a phototroph, typically an alga and/or cyanobacterium. The evolutionary processes that led to the global success of lichens are poorly understood. In this review, we explore the goods and services exchange between fungus and phototroph and how this propelled the success of both symbiont and symbiosis. Lichen fungal symbionts count among the only filamentous fungi that expose most of their mycelium to an aerial environment. Phototrophs export carbohydrates to the fungus, which converts them to specific polyols. Experimental evidence suggests that polyols are not only growth and respiratory substrates but also play a role in anhydrobiosis, the capacity to survive desiccation. We propose that this dual functionality is pivotal to the evolution of fungal symbionts, enabling persistence in environments otherwise hostile to fungi while simultaneously imposing costs on growth. Phototrophs, in turn, benefit from fungal protection from herbivory and light stress, while appearing to exert leverage over fungal sex and morphogenesis. Combined with the recently recognized habit of symbionts to occur in multiple symbioses, this creates the conditions for a multiplayer marketplace of rewards and penalties that could drive symbiont selection and lichen diversification.

The lichen market place

“…1 in Spribille et al . (2022)). Fungi convert glucose and ribitol into another pentitol, arabitol, and the hexitol mannitol, whereas erythritol appears to remain unchanged after import by the fungus.…”

“…By summarizing the current knowledge of lichens, Spribille et al . (2022; pp. 1566–1582) in their Tansley review in this issue of New Phytologist , outline how lichens could fit the theory of biological markets, where sugar alcohols containing multiple hydroxyl groups, referred to as ‘polyols’ play prominent roles, also contemplating the relationship between genotype and phenotype, and calling for a paradigm change regarding the rewards of the symbiotic state for the photosynthetic symbionts – certainly an enjoyable read!

‘The “dual functionality” of polyols as carbon sources and compatible solutes … combined with the recently recognized habit of symbionts to occur in multiple symbioses, creates the conditions for a multiplayer market place of rewards and penalties that could drive symbiont selection and lichen diversification.’

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“…A key part of the Spribille et al . (2022) Tansley review is dedicated to previous work demonstrating that carbohydrates, including polyols, produced by the photobiont are exported to the fungal partner, which can convert them into other polyols. The authors highlight a ‘dual role’ of polyols, as substrates for growth and respiration, but also as important players in a lichens’ capability to survive desiccation.…”

“…The authors highlight a ‘dual role’ of polyols, as substrates for growth and respiration, but also as important players in a lichens’ capability to survive desiccation. In turn, the photosynthetic symbiont would benefit from protection from herbivory and excess light provided by the fungus, while exerting leverage over fungal sex and morphogenesis (Spribille et al ., 2022). In many lichens, shielding against strong light is mediated by crystallized fungal metabolites that accumulate in the intercellular spaces (sometimes termed ‘extrolites’) and may act as ‘smart switches’ letting more light pass to the photosynthetic powerhouse when crystals are more spaced in the hydrated state.…”

“…This approach is particularly useful for the interpretation of mutualistic associations of different species, where partners achieve a self-sustaining agreement by giving away goods they easily produce in exchange for other goods provided by their partners. By summarizing the current knowledge of lichens, Spribille et al (2022;pp. 1566-1582 in their Tansley review in this issue of New Phytologist, outline how lichens could fit the theory of biological markets, where sugar alcohols containing multiple hydroxyl groups, referred to as 'polyols' play prominent roles, also contemplating the relationship between genotype and phenotype, and calling for a paradigm change regarding the rewards of the symbiotic state for the photosynthetic symbiontscertainly an enjoyable read!…”