Choosing the Right Life Partner: Ecological Drivers of Lichen Symbiosis

Abstract

Lichens are an iconic example of symbiotic systems whose ecology is shaped by the requirements of the symbionts. Previous studies suggest that fungal (mycobionts) as well as photosynthesizing (phycobionts or cyanobionts) partners have a specific range of acceptable symbionts that can be chosen according to specific environmental conditions. This study aimed to investigate the effects of climatic conditions and mycobiont identity on phycobiont distribution within the lichen genera Stereocaulon, Cladonia, and Lepraria. The study area comprised the Canary Islands, Madeira, Sicily, and the Aeolian Islands, spanning a wide range of climatic conditions. These islands are known for their unique and diverse fauna and flora; however, lichen phycobionts have remained unstudied in most of these areas. In total, we genetically analyzed 339 lichen samples. The phycobiont pool differed significantly from that outside the studied area. Asterochloris mediterranea was identified as the most abundant phycobiont. However, its distribution was limited by climatic constraints. Other species of Asterochloris and representatives of the genera Chloroidium, Vulcanochloris, and Myrmecia were also recovered as phycobionts. The selection of symbiotic partners from the local phycobiont pool was driven by mycobiont specificity (i.e., the taxonomic range of acceptable partners) and the environmental conditions, mainly temperature. Interestingly, the dominant fungal species responded differently in their selection of algal symbionts along the environmental gradients. Cladonia rangiformis associated with its phycobiont A. mediterranea in a broader range of temperatures than Stereocaulon azoreum, which favors other Asterochloris species along most of the temperature gradient. Stereocaulon vesuvianum associated with Chloroidium spp., which also differed in their temperature optima. Finally, we described Stereocaulon canariense as a new endemic species ecologically distinct from the other Stereocaulon species on the Canary Islands.

An Exception to the Rule? Could Photobiont Identity Be a Better Predictor of Lichen Phenotype than Mycobiont Identity?

“…The final dataset included 241 sequences, of which 205 were newly produced (51 sequences of mycobiont ITS rDNA, 30 of cox1, 29 of EF-1α, 27 of mtSSU, 32 of RPB2, 33 sequences of photobiont ITS rDNA and three of photobiont actin type I gene), 15 were retrieved from our previous datasets [55,56] and 21 downloaded from GenBank (https: //www.ncbi.nlm.nih.gov/ (accessed on 25 November 2021)). The newly obtained sequences have been deposited in GenBank (see Supplementary Table S1 for accession numbers).…”

“…For example, C. polydactyla/umbricola, which commonly grow on dead wood among bryophytes in humid forests, is associated with A. italiana , which has previously been reported from Stereocaulon and Cladonia spp. in relatively humid and stable climates [ 55 , 58 ]. Similarly, A. irregularis , which is restricted to cold areas of the northern hemisphere [ 26 ], was one of the associated photobionts of C. bellidiflora , which usually occurs on mineral soils or boulders in tundra, mountain heaths or on higher hilltops.…”

Regionally Varying Habitat Relationships in Lichens: The Concept and Evidence with an Emphasis on North-Temperate Ecosystems

“…First, many lichen-forming species reveal large and unexplained distribution patterns, such as various disjunct ranges [ 17 ]. One could thus expect significant geographic variation in lichen environments, favoring a diversity of responses through plasticity and acclimation [ 18 ], switching to alternative algal (phototroph) partners [ 19 , 20 ] or adaptive divergence [ 21 , 22 ]. At the same time, a scarcity of taxonomically useful morphological or chemical characters implies that many historically described lichen-forming species involve multiple evolutionary lineages that may be habitat specific and merit recognition as full species (e.g., [ 23 ]).…”

Composition, structure and robustness of Lichen guilds

“…However, it is widely acknowledged that specificity of the mycobiont-photobiont association as well as the spatial distribution of their component species largely drives the formation of new lichen organisms 6,[14][15][16] . Indeed, many symbionts are quite stringent in the partnerships they form, which are often determined by biophysical gradients [17][18][19][20][21][22] . It has also been suggested that highly specific mycobionts are typically restricted to few environments and display limited ecological range 23,24 .…”