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This article is a Commentary on Mark et al. (2020), 227: 1362–1375.

A review of algal (including cyanobacterial) symbionts associated with lichen-forming fungi is presented. General aspects of their biology relevant to lichen symbioses are summarized. The genera of algae currently believed to include lichen symbionts are outlined; approximately 50 can be recognized at present. References reporting algal taxa in lichen symbiosis are tabulated, with emphasis on those published since the 1988 review by Tschermak-Woess, and particularly those providing molecular evidence for their identifications. This review is dedicated in honour of Austrian phycologist Elisabeth Tschermak-Woess (1917–2001), for her numerous and significant contributions to our knowledge of lichen algae (some published under the names Elisabeth Tschermak and Liesl Tschermak).

In order to re-establish lichen symbiosis, fungal spores must first germinate and then associate with a compatible photobiont. To detect possible establishment limitations in a sexually reproducing cyanolichen species, we studied ascospore germination, photobiont growth and photobiont association patterns in Pectenia plumbea. Germination tests were made with ascospores from 500 apothecia under different treatments, and photobiont growth was analysed in 192 isolates obtained from 24 thalli. We determined the genotype identity [tRNALeu (UAA) intron] of the Nostoc cyanobionts from 30 P. plumbea thalli from one population. We also sequenced cyanobionts of 41 specimens of other cyanolichen species and 58 Nostoc free-living colonies cultured from the bark substrate. Not a single fungal ascospore germinated and none of the photobiont isolates produced motile hormogonia. Genetic analyses revealed that P. plumbea shares Nostoc genotypes with two other cyanolichen species of the same habitat, but these photobionts were hardly present in the bark substrate. Due to the inability of both symbionts to thrive independently, the establishment of P. plumbea seems to depend on Dendriscocaulon umhausense, the only cyanolichen species in the same habitat that reproduces asexually and acts as a source of appropriate cyanobionts. This provides support to the hypothesis about facilitation among lichens.

ABSTRACT Lichens are classic models of symbiosis, and one of the most frequent nutritional modes among fungi. The ecologically and geographically widespread lichen-forming algal (LFA) genus Trebouxia is one of the best-studied groups of LFA and associates with over 7000 fungal species. Despite its importance, little is known about its diversification. We synthesized twenty years of publicly available data by characterizing the ecological preferences of this group and testing for time-variant shifts in climatic regimes over a distribution of trees. We found evidence for limited shifts among regimes, but that disparate lineages convergently evolved similar ecological tolerances. Early Trebouxia lineages were largely forest specialists or habitat generalists that occupied a regime whose extant members occur in moderate climates. Trebouxia then convergently diversified in non-forested habitats and expanded into regimes whose modern representatives occupy wet-warm and cool-dry climates. We rejected models in which climatic diversification slowed through time, suggesting climatic diversification is inconsistent with that expected under an adaptive radiation. In addition, we found that climatic and vegetative regime shifts broadly coincided with the evolution of biomes and associated or similar taxa. Together, our work illustrates how this keystone symbiont from an iconic symbiosis evolved to occupy diverse habitats across the globe. Lichen algae convergently evolved to occupy shared climates and habitats at a gradual rate, and broadly coincident with the evolution of these biomes and associated taxa.

This article is a Commentary on Spribille et al. (2022), 234: 1566–1582.

Patterns of specificity among symbiotic partners are key to a comprehensive understanding of the evolution of symbiotic systems. Specificity of mutualistic partners, within a widespread monophyletic group for which all species are sampled has rarely been explored. Here, we assess the level of specificity between the cosmopolitan lichen-forming fungus (mycobiont) from the genus Peltigera, section Polydactylon, and its cyanobacterial partner Nostoc (cyanobiont). The mycobiont and cyanobiont phylogenies are inferred from five nuclear loci and the rbcLX region, respectively. These sequences were obtained from 206 lichen thalli, representing ca. 40 closely related Peltigera species sampled worldwide, doubling the number of known species in this group. We found a broad spectrum of specificity for both partners ranging from strict specialists to generalists. Overall, mycobionts are more specialized than cyanobionts by associating mostly with one or a few Nostoc phylogroups, whereas most cyanobionts associate frequently with several Peltigera species. Specialist mycobionts are older than generalists, supporting the hypothesis that specialization of mycobionts to one or few cyanobionts, is favored through time in geographic areas where species have been established for long periods of time. The relatively recent colonization of a new geographic area (Central and South America) by members of section Polydactylon is associated with a switch to a generalist pattern of association and an increased diversification rate by the fungal partner, suggesting that switches to generalism are rare events that are advantageous in new environments. We detected higher genetic diversity in generalist mycobionts. We also found that Peltigera species specialized on a single Nostoc phylogroup have narrower geographical distributions compared with generalist species.

Carbon-concentrating mechanisms (CCMs) are a widespread phenomenon in photosynthetic organisms. In vascular plants, the evolution of CCMs ([C44-carbon compound] and crassulacean acid metabolism [CAM]) is associated with significant shifts, most often to hot, dry and bright, or aquatic environments. If and how CCMs drive distributions of other terrestrial photosynthetic organisms, remains little studied. Lichens are ecologically important obligate symbioses between fungi and photosynthetic organisms. The primary photosynthetic partner in these symbioses can include CCM-presenting cyanobacteria (as carboxysomes), CCM-presenting green algae (as pyrenoids) or green algae lacking any CCM. We use an extensive dataset of lichen communities from eastern North America, spanning a wide climatic range, to test the importance of CCMs as predictors of lichen ecology and distribution. We show that the presence or absence of CCMs leads to opposite responses to temperature and precipitation in green algal lichens, and different responses in cyanobacterial lichens. These responses contrast with our understanding of lichen physiology, whereby CCMs mitigate carbon limitation by water saturation at the cost of efficient use of vapor hydration. This study demonstrates that CCM status is a key functional trait in obligate lichen symbioses, equivalent in importance to its role in vascular plants, and central for studying present and future climate responses.

1. Climate change is expected to cause several impacts at the global scale, and drylands will be amongst the most affected areas. Thus, investigating how these changes will affect the composition, structure and functioning of dryland ecosystems has become a priority. From an ecological indicator point of view, several works have shown that functional diversity is better than species richness to understand ecosystem functioning or response to environmental factors. However, most of these works focus on plants, while those of other organisms remain largely unknown. Lichens are amongst the ecosystem components more sensitive to climatic changes due to several physiological and ecological characteristics. Their poikilohydric nature (therefore highly dependent on the atmosphere for water supply) and their ubiquity on terrestrial ecosystems underlie their potential as indicators of climate. Nonetheless, works specifically aiming to identify lichen functional traits that respond to aridity remain poorly explored, particularly in drylands. 2. We proposed to identify lichen functional traits and respective functional groups responding to aridity in a Mediterranean drylands ecosystem. 3. Lichen diversity was sampled in open holm oak woodlands along an aridity gradient in SW Europe (Iberian Peninsula). Lichen functional traits that could be easily identified and related to water uptake were selected to be tested: type of photobiont, growth form and reproduction strategy. 4. Lichen species composition was related to the aridity gradient. The three traits chosen were related with the community’s response to aridity, but with contrasting responses in different functional groups. More specifically crustose and fruticose lichens, isidiate species and the ones with Trentepohlia as photobiont were related to the less arid part of the gradient. Foliose species and cyanolichens, on the contrary, were associated with the most arid areas. 5. Synthesis. We were able to identify lichen traits responding to aridity. Type of photobiont was particularly responsive, with Trentepohlia and cyanobacteria functional groups, responding clearly in contrasting ways to aridity in this drylands ecosystem. This work emphasizes functional diversity role on understanding and assessing the response to environmental factors, namely to climate. It also highlights the potential use of lichen functional groups as ecological indicators of climate change.

Lichens have long been considered as composite organisms composed of algae and/or cyanobacteria hosted by a fungus in a mutualistic relationship. Other organisms have been gradually discovered within the lichen thalli, such as multiple algal species, yeasts, or even viruses. Of pivotal relevance is the existence of the lichen microbiome, which is a community of microorganisms that can be found living together on the lichen surface. This community performs a growing number of functions. In this entry, we explore the journey of lichens being considered from a dual partnership to a multi-species symbiotic relationship.

Abstract Lichenized algae and cyanobacteria are known to be shared and selected by unrelated lichen-forming fungi coexisting in so-called photobiont-mediated guilds. Life in such a guild could be crucial for the survival of a large group of lichen fungi dependent on horizontal transmission of photobionts. Here, we investigate frequent lichen phycobionts of the genus Trebouxia in rock-dwelling lichen communities. We found intensive and repeated sharing of specific Trebouxia assemblages by co-occurring lichens across distant localities. Rock chemistry, expressed as pH, determined the composition of photobiont pools and separated three saxicolous lichen guilds, sharing environmentally specific photobiont groups. Moreover, unlike the majority of lichen fungi, many Trebouxia photobionts represented opportunists in the choice of general substrate form (soil-rock-tree bark/wood), maintaining their pH preferences. Thus, saxicolous communities form just a part of a complex guild system that is in principle mediated by environmentally conditioned groups of naturally co-occurring photobionts. The complexity of the system is influenced by diverse photobiont life strategies, including also dispersal style. The findings of photobionts strictly or predominantly associated with sexually reproducing fungi stimulated us to emphasize the role of free-dispersing photobionts in the establishment and maintenance of lichen guilds. Lichen fungi form highly complex and extensive photobiont-mediated system composed of various and differently overlapping guilds that are established across the basic ecological groups of saxi-, terricolous and epiphytic lichens.