Lichen algae: the photosynthetic partners in lichen symbioses

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).

Large differences in carbohydrate degradation and transport potential in the genomes of lichen fungal symbionts

Lichen symbioses are generally thought to be stabilized by the transfer of fixed carbon compounds from a photosynthesizing unicellular symbiont to a fungus. In other fungal symbioses, carbohydrate subsidies correlate with genomic reductions in the number of genes for plant cell wall-degrading enzymes (PCWDEs), but whether this is the case with lichen fungal symbionts (LFSs) is unknown. We predicted genes encoding carbohydrate-active enzymes (CAZymes) and sugar transporters in 17 existing and 29 newly sequenced genomes from across the class Lecanoromycetes, the largest extant clade of LFSs. Despite possessing lower mean numbers of PCWDE genes compared to non-symbiont Ascomycota, all LFS genomes possessed a robust suite of predicted PCWDEs. The largest CAZyme gene numbers, on par with model species such as Penicillium, were retained in genomes from the subclass Ostropomycetidae, which are found in crust lichens with highly specific ecologies. The lowest numbers were in the subclass Lecanoromycetidae, which are symbionts of many generalist macrolichens. Our results suggest that association with phototroph symbionts does not in itself result in functional loss of PCWDEs and that PCWDE losses may have been driven by adaptive processes within the evolution of specific LFS lineages. The inferred capability of some LFSs to access a wide range of carbohydrates suggests that some lichen symbioses may augment fixed CO2 with carbon from external sources.

Complex Interaction Networks Among Cyanolichens of a Tropical Biodiversity Hotspot

Interactions within lichen communities include, in addition to close mutualistic associations between the main partners of specific lichen symbioses, also more elusive relationships between members of a wider symbiotic community. Here, we analyze association patterns of cyanolichen symbionts in the tropical montane forests of Taita Hills, southern Kenya, which is part of the Eastern Afromontane biodiversity hotspot. The cyanolichen specimens analyzed represent 74 mycobiont taxa within the order Peltigerales (Ascomycota), associating with 115 different variants of the photobionts genus Nostoc (Cyanobacteria). Our analysis demonstrates wide sharing of photobionts and reveals the presence of several photobiont-mediated lichen guilds. Over half of all mycobionts share photobionts with other fungal species, often from different genera or even families, while some others are strict specialists and exclusively associate with a single photobiont variant. The most extensive symbiont network involves 24 different fungal species from five genera associating with 38 Nostoc photobionts. The Nostoc photobionts belong to two main groups, the Nephroma-type Nostoc and the Collema/Peltigera-type Nostoc, and nearly all mycobionts associate only with variants of one group. Among the mycobionts, species that produce cephalodia and those without symbiotic propagules tend to be most promiscuous in photobiont choice. The extent of photobiont sharing and the structure of interaction networks differ dramatically between the two major photobiont-mediated guilds, being both more prevalent and nested among Nephroma guild fungi and more compartmentalized among Peltigera guild fungi. This presumably reflects differences in the ecological characteristics and/or requirements of the two main groups of photobionts. The same two groups of Nostoc have previously been identified from many lichens in various lichen-rich ecosystems in different parts of the world, indicating that photobiont sharing between fungal species is an integral part of lichen ecology globally. In many cases, symbiotically dispersing lichens can facilitate the dispersal of sexually reproducing species, promoting establishment and adaptation into new and marginal habitats and thus driving evolutionary diversification.

Towards a Systems Biology Approach to Understanding the Lichen Symbiosis: Opportunities and Challenges of Implementing Network Modelling

Lichen associations, a classic model for successful and sustainable interactions between micro-organisms, have been studied for many years. However, there are significant gaps in our understanding about how the lichen symbiosis operates at the molecular level. This review addresses opportunities for expanding current knowledge on signalling and metabolic interplays in the lichen symbiosis using the tools and approaches of systems biology, particularly network modelling. The largely unexplored nature of symbiont recognition and metabolic interdependency in lichens could benefit from applying a holistic approach to understand underlying molecular mechanisms and processes. Together with ‘omics’ approaches, the application of signalling and metabolic network modelling could provide predictive means to gain insights into lichen signalling and metabolic pathways. First, we review the major signalling and recognition modalities in the lichen symbioses studied to date, and then describe how modelling signalling networks could enhance our understanding of symbiont recognition, particularly leveraging omics techniques. Next, we highlight the current state of knowledge on lichen metabolism. We also discuss metabolic network modelling as a tool to simulate flux distribution in lichen metabolic pathways and to analyse the co-dependence between symbionts. This is especially important given the growing number of lichen genomes now available and improved computational tools for reconstructing such models. We highlight the benefits and possible bottlenecks for implementing different types of network models as applied to the study of lichens.

New lineages of Asterochloris photobionts in Bolivian lichens, and expand our knowledge on habitat preferences and distribution of Asterochloris algae

We studied biodiversity of Asterochloris photobionts found in lichen symbioses in Bolivian Andean vegetation and, to better understand global spatial distribution and adaptation strategies of this algae, in relation to worldwide phylogeny of the genus. Based on nuclear ITS rDNA, chloroplast rbcL gene and actin type I gene we constructed a phylogenetic tree that recovered 12 new Asterochloris lineages; and 29 Bolivian photobiont samples were assigned to 11 previously recognized Asterochloris lineages. We showed that some Asterochloris photobiont species and lineages known to date may occur in a broader spectrum of climatic conditions and mycobiont species and photobionts may show different preferences in the altitude gradient. To reveal general patterns of specificity of the mycobionts towards the photobiont in Asterochloris dependent symbiosis on global range, we tested the influence of climate, altitude, geographical distance and effects of symbiotic partner (mycobiont) at the species level of three genera of lichen forming fungi, i.e. Stereocaulon, Cladonia and Lepraria. Also, we compared specificity of mycobionts towards Asterochloris photobionts in cosmopolitan, Neotropical, and Pantropical lichen forming fungi. Interestingly, cosmopolitan species showed the lowest specificity to their photobionts’, but also the lowest haplotype diversity. While, Neotropical and Paleotropical mycobionts were more specific.

The beauty and the yeast: can the microalgae Dunaliella form a borderline lichen with Hortaea werneckii?

Lichenized fungi usually develop complex, stratified morphologies through an intricately balanced living together with their algal partners, but several species are known to form only more or less loose associations with algae. These borderline lichens are still little explored although they could inform us about early stages of lichen evolution. We studied the association of the extremely halotolerant fungus Hortaea werneckii with the alga Dunaliella atacamensis, discovered in a cave in the Atacama Desert (Chile), and with D. salina, common inhabitant of saltern brines. D. atacamensis forms small colonies, in which cells of H. werneckii can be frequently observed, while such interaction has not been observed with D. salina. As symbiotic interactions between Dunaliella and Hortaea have not been reported, we performed a series of co-cultivation experiments to inspect whether these species could interact and develop more distinct lichen-like symbiotic structures. We set up co-cultures between axenic strains of Hortaea werneckii (isolated both from Mediterranean salterns and from the Atacama cave) and isolates of D. atacamensis (from the Atacama cave) and D. salina (isolated from Mediterranean salterns). Although we used different growth media and cultivation approaches, bright field and SEM microscopy analyses did not indicate any mutual effects in these experiments. We discuss the implications for fungal algal interactions along the transition from algal exploiters to lichen symbioses.

3D biofilms: in search of the polysaccharides holding together lichen symbioses

ABSTRACT Stable, long-term interactions between fungi and algae or cyanobacteria, collectively known as lichens, have repeatedly evolved complex architectures with little resemblance to their component parts. Lacking any central scaffold, the shapes they assume are casts of secreted polymers that cement cells into place, determine the angle of phototropic exposure and regulate water relations. A growing body of evidence suggests that many lichen extracellular polymer matrices harbor unicellular, non-photosynthesizing organisms (UNPOs) not traditionally recognized as lichen symbionts. Understanding organismal input and uptake in this layer is key to interpreting the role UNPOs play in lichen biology. Here, we review both polysaccharide composition determined from whole, pulverized lichens and UNPOs reported from lichens to date. Most reported polysaccharides are thought to be structural cell wall components. The composition of the extracellular matrix is not definitively known. Several lines of evidence suggest some acidic polysaccharides have evaded detection in routine analysis of neutral sugars and may be involved in the extracellular matrix. UNPOs reported from lichens include diverse bacteria and yeasts for which secreted polysaccharides play important biological roles. We conclude by proposing testable hypotheses on the role that symbiont give-and-take in this layer could play in determining or modifying lichen symbiotic outcomes.