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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.

SUBMITTER: Vancurova L

PROVIDER: S-EPMC8712729 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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 ? 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.

Project description:Thin, hair-like lichens (Alectoria, Bryoria, Usnea) form conspicuous epiphyte communities across the boreal biome. These poikilohydric organisms provide important ecosystem functions and are useful indicators of global change. We analyse how environmental drivers influence changes in occurrence and length of these lichens on Norway spruce (Picea abies) over 10 years in managed forests in Sweden using data from >6000 trees. Alectoria and Usnea showed strong declines in southern-central regions, whereas Bryoria declined in northern regions. Overall, relative loss rates across the country ranged from 1.7% per year in Alectoria to 0.5% in Bryoria. These losses contrasted with increased length of Bryoria and Usnea in some regions. Occurrence trajectories (extinction, colonization, presence, absence) on remeasured trees correlated best with temperature, rain, nitrogen deposition, and stand age in multinomial logistic regression models. Our analysis strongly suggests that industrial forestry, in combination with nitrogen, is the main driver of lichen declines. Logging of forests with long continuity of tree cover, short rotation cycles, substrate limitation and low light in dense forests are harmful for lichens. Nitrogen deposition has decreased but is apparently still sufficiently high to prevent recovery. Warming correlated with occurrence trajectories of Alectoria and Bryoria, likely by altering hydration regimes and increasing respiration during autumn/winter. The large-scale lichen decline on an important host has cascading effects on biodiversity and function of boreal forest canopies. Forest management must apply a broad spectrum of methods, including uneven-aged continuous cover forestry and retention of large patches, to secure the ecosystem functions of these important canopy components under future climates. Our findings highlight interactions among drivers of lichen decline (forestry, nitrogen, climate), functional traits (dispersal, lichen colour, sensitivity to nitrogen, water storage), and population processes (extinction/colonization).

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Choosing the Right Life Partner: Ecological Drivers of Lichen Symbiosis.

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