Climatic factors, soil chemistry and geography are considered as major factors affecting lichen distribution and diversity. To determine how these factors limit or support the associations between the symbiotic partners, we revise the lichen symbiosis as a network of relationships here. More than one thousand thalli of terricolous Cladonia lichens were collected at sites with a wide range of soil chemical properties from seven biogeographical regions of Europe. A total of 18 OTUs of the algal genus Asterochloris and 181 OTUs of Cladonia mycobiont were identified. We displayed all realized pairwise mycobiont-photobiont relationships and performed modularity analysis. It revealed four virtually separated modules of cooperating OTUs. The modules differed in mean annual temperature, isothermality, precipitation, evapotranspiration, soil pH, nitrogen, and carbon contents. Photobiont switching was strictly limited to algae from one module, i.e., algae of similar ecological preferences, and only few mycobionts were able to cooperate with photobionts from different modules. Thus, Cladonia mycobionts generally cannot widen their ecological niches through photobiont switching. The modules also differed in the functional traits of the mycobionts, e.g., sexual reproduction rate, presence of soredia, and thallus type. These traits may represent adaptations to the environmental conditions that drive the differentiation of the modules. In conclusion, the promiscuity in Cladonia mycobionts is strictly limited by climatic factors and soil chemistry.

Botánica ICBIBE Fac CC Biológicas Universitat de València Valencia Spain

Department of Botany Faculty of Science Charles University Prague Czechia

Museum of West Bohemia in Pilsen Pilsen Czechia

Zobrazit více v PubMed

Ahti T. (2000). Cladoniaceae.

Ahti T., Stenroos S., Moberg R. (2013). DOI

Ammerman J. (2001).

Armstrong R. A. (1991). The influence of climate on the dispersal of lichen soredia. DOI

Arnold A. E., Miadlikowska J., Higgins K. L., Sarvate S. D., Gugger P., Way A., et al. (2009). A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? PubMed DOI

Bačkor M., Hudák J., Repčák M., Ziegler W., Bačkorová M. (1992). The influence of pH and lichen metabolites (vulpinic acid and (+) usnic acid) on the growth of the lichen photobiont DOI

Baker A. C. (2003). Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of DOI

Bastian M., Heymann S., Jacomy M. (2009). “Gephi: an open source software for exploring and manipulating networks,” in

Bates S. T., Cropsey G. W., Caporaso J. G., Knight R., Fierer N. (2011). Bacterial communities associated with the lichen symbiosis. PubMed DOI PMC

Beck A. (2002).

Blaha J., Baloch E., Grube M. (2006). High photobiont diversity associated with the euryoecious lichen-forming ascomycete DOI

Borcard D., Legendre P., Avois-Jacquet C., Tuomisto H. (2004). Dissecting the spatial structure of ecological data at multiple scales. DOI

Borcard D., Legendre P., Drapeau P. (1992). Partialling out the spatial component of ecological variation. DOI

Brodo I. M. (1973). “Substrate ecology,” in DOI

Chambers J. M. (2013). SoDA: Functions and Examples for “Software for Data Analysis”. R Package Version, 1-0. Available online at: https://CRAN.R-project.org/package=SoDA

Cocchietto M., Skert N., Nimis P., Sava G. (2002). A review on usnic acid, an interesting natural compound. PubMed DOI

Cubero O. F., Crespo A. N. A., Fatehi J., Bridge P. D. (1999). DNA extraction and PCR amplification method suitable for fresh, herbarium-stored, lichenized, and other fungi. DOI

Dal Grande F., Beck A., Cornejo C., Singh G., Cheenacharoen S., Nelsen M. P., et al. (2014). Molecular phylogeny and symbiotic selectivity of the green algal genus PubMed DOI

Dal Grande F., Widmer I., Wagner H. H., Scheidegger C. (2012). Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. PubMed DOI

Del M., Molina C., Bajon C., Sauvanet A., Robert D., Vicente C. (1998). Detection of polysaccharides and ultrastructural modification of the photobiont cell wall produced by two arginase isolectins from DOI

DePriest P. T. (2004). Early molecular investigations of lichen-forming symbionts: 1986–2001. PubMed DOI

Dixon P. (2003). VEGAN, a package of R functions for community ecology. DOI

Dray S., Dufour A. B. (2007). The ade4 package: implementing the duality diagram for ecologists.

Drummond A. J., Suchard M. A., Xie D., Rambaut A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. PubMed DOI PMC

Easton R. (1994). Lichens and rocks: a review.

Egan L. (2001).

Egerton-Warburton L., Allen M. F. (2001). Endo-and ectomycorrhizas in PubMed DOI

Etges S., Ott S. (2001). Lichen mycobionts transplanted into the natural habitat.

Ezard T., Fujisawa T., Barraclough T. G. (2009). Splits: species’ limits by threshold statistics.

Fernández-Mendoza F., Domaschke S., García M. A., Jordan P., Martín M. P., Printzen C. (2011). Population structure of mycobionts and photobionts of the widespread lichen PubMed DOI

Fontaine K. M., Teuvo A. H. T. I., Piercey-Normore M. D. (2010). Convergent evolution in DOI

Friedl T. (1987). Thallus development and phycobionts of the parasitic lichen DOI

Gardes M., Bruns T. D. (1993). ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. PubMed DOI

Gardner C. R., Mueller D. M. (1981). Factors affecting the toxicity of several lichen acids: effect of pH and lichen acid concentration. DOI

Gasulla F., de Nova P. G., Esteban-Carrasco A., Zapata J. M., Barreno E., Guéra A. (2009). Dehydration rate and time of desiccation affect recovery of the lichenic algae PubMed DOI

Gilbert O. L. (1986). Field evidence for an acid rain effect on lichens. DOI

Goyal R., Seaward M. R. D. (1981). Metal uptake in terricolous lichens: I. Metal localization within the thallus. DOI

Grube M., Cardinale M., de Castro J. V., Müller H., Berg G. (2009). Species-specific structural and functional diversity of bacterial communities in lichen symbioses. PubMed DOI

Hamlett C. A., Shirtcliffe N. J., Pyatt F. B., Newton M. I., McHale G., Koch K. (2011). Passive water control at the surface of a superhydrophobic lichen. PubMed DOI

Hauck M., Jürgens S. R. (2008). Usnic acid controls the acidity tolerance of lichens. PubMed DOI

Hawksworth D. L., Grube M. (2020). Lichens redefined as complex ecosystems. PubMed DOI PMC

Hepperle D. (2004).

Higgins N. F., Connan S., Stengel D. B. (2015). Factors influencing the distribution of coastal lichens DOI

Hijmans R. J. (2019).

Hill D. J. (1994). The nature of the symbiotic relationship in lichens. DOI

Honegger R. (1991). Functional aspects of the lichen symbiosis. DOI

Honegger R. (1996). Experimental studies of growth and regenerative capacity in the foliose lichen DOI

Honegger R. (2006).

Hume B. C., D’Angelo C., Smith E. G., Stevens J. R., Burt J., Wiedenmann J. (2015). PubMed DOI PMC

Jackson D. A. (1993). Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. DOI

James P. W. (2009). “

Jukes T. H., Cantor C. R. (1969). Evolution of protein molecules.

Kaplan J. (2020).

Karger D. N., Conrad O., Böhner J., Kawohl T., Kreft H., Soria-Auza R. W., et al. (2017). Climatologies at high resolution for the earth’s land surface areas. PubMed DOI PMC

Katoh K., Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. PubMed DOI PMC

Kawaida H., Ohba K., Koutake Y., Shimizu H., Tachida H., Kobayakawa Y. (2013). Symbiosis between hydra and chlorella: molecular phylogenetic analysis and experimental study provide insight into its origin and evolution. PubMed DOI

Kemp D. W., Hernandez-Pech X., Iglesias-Prieto R., Fitt W. K., Schmidt G. W. (2014). Community dynamics and physiology of DOI

Kosecka M., Guzow-Krzemińska B., Černajová I., Škaloud P., Jabłońska A., Kukwa M. (2021). New lineages of photobionts in Bolivian lichens expand our knowledge on habitat preferences and distribution of PubMed DOI PMC

Kotelko R., Piercey-Normore M. D. (2010). PubMed DOI

Lapeyrie F. F., Chilvers G. A. (1985). An endomycorrhiza-ectomycorrhiza succession associated with enhanced growth of DOI

Leavitt S. D., Kraichak E., Nelsen M. P., Altermann S., Divakar P. K., Alors D., et al. (2015). Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen-forming family Parmeliaceae (Ascomycota). PubMed DOI

Lechowicz M. J. (1982). The effects of simulated acid precipitation on photosynthesis in the caribou lichen DOI

Lücking R., Lawrey J. D., Sikaroodi M., Gillevet P. M., Chaves J. L., Sipman H. J., et al. (2009). Do lichens domesticate photobionts like farmers domesticate crops? Evidence from a previously unrecognized lineage of filamentous cyanobacteria. PubMed DOI

Moya P., Škaloud P., Chiva S., García-Breijo F. J., Reig-Arminana J., Vančurová L., et al. (2015). Molecular phylogeny and ultrastructure of the lichen microalga PubMed DOI

Nakazawa M. (2012).

Nelsen M. P., Gargas A. (2008). Dissociation and horizontal transmission of codispersing lichen symbionts in the genus PubMed DOI

Nelson D. W., Sommers L. E. (1996). Total carbon, organic carbon, and organic matter. DOI

Nowack E. C., Price D. C., Bhattacharya D., Singer A., Melkonian M., Grossman A. R. (2016). Gene transfers from diverse bacteria compensate for reductive genome evolution in the chromatophore of PubMed DOI PMC

Orange A., James P. W., White F. J. (2001).

Osyczka P., Lenart-Boroń A., Boroń P., Rola K. (2021). Lichen-forming fungi in postindustrial habitats involve alternative photobionts. PubMed DOI

Paradis E., Schliep K. (2019). ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. PubMed DOI

Peksa O., Škaloud P. (2011). Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga PubMed DOI

Pennell M. W., Eastman J. M., Slater G. J., Brown J. W., Uyeda J. C., FitzJohn R. G., et al. (2014). geiger v2. 0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. PubMed DOI

Perret X., Staehelin C., Broughton W. J. (2000). Molecular basis of symbiotic promiscuity. PubMed DOI PMC

Piercey-Normore M. D., DePriest P. T. (2001). Algal switching among lichen symbioses. PubMed DOI

Pino-Bodas R., Stenroos S. (2020). Global biodiversity patterns of the photobionts associated with the genus PubMed DOI PMC

Pino-Bodas R., Martin M. P., Burgaz A. R., Lumbsch H. T. (2013). Species delimitation in PubMed DOI

Puillandre N., Lambert A., Brouillet S., Achaz G. (2012). ABGD, Automatic barcode gap discovery for primary species delimitation. PubMed DOI

Purvis O. W., Halls C. (1996). A review of lichens in metal-enriched environments. DOI

Pyatt F. B. (1973). “Lichen propagules,” in DOI

R Core Team (2020).

Rambaut A., Drummond A. J., Xie D., Baele G., Suchard M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. PubMed DOI PMC

Resl P., Fernández-Mendoza F., Mayrhofer H., Spribille T. (2018). The evolution of fungal substrate specificity in a widespread group of crustose lichens. PubMed DOI PMC

Revell L. J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). DOI

Rikkinen J. (2003). Ecological and evolutionary role of photobiont-mediated guilds in lichens.

Rola K., Lenart-Boroń A., Boroń P., Osyczka P. (2021). Heavy-metal pollution induces changes in the genetic composition and anatomical properties of photobionts in pioneer lichens colonizing post-industrial habitats. PubMed DOI

Rolshausen G., Hallman U., Grande F. D., Otte J., Knudsen K., Schmitt I. (2020). Expanding the mutualistic niche: parallel symbiont turnover along climatic gradients. PubMed DOI PMC

Rosabal D., Burgaz A. R., Reyes O. J. (2013). Substrate preferences and phorophyte specificity of corticolous lichens on five tree species of the montane rainforest of Gran Piedra, Santiago de Cuba. DOI

Scott M. G., Hutchinson T. C. (1987). Effects of a simulated acid rain episode on photosynthesis and recovery in the caribou-forage lichens DOI

Singh G., Dal Grande F., Divakar P. K., Otte J., Crespo A., Schmitt I. (2017). Fungal–algal association patterns in lichen symbiosis linked to macroclimate. PubMed DOI

Škaloud P., Peksa O. (2010). Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga PubMed DOI

Škaloud P., Steinová J., Řídká T., Vančurová L., Peksa O. (2015). Assembling the challenging puzzle of algal biodiversity: species delimitation within the genus PubMed DOI

Slocum R. D., Ahmadjian V., Hildreth K. C. (1980). Zoosporogenesis in DOI

Spribille T., Tuovinen V., Resl P., Vanderpool D., Wolinski H., Aime M. C., et al. (2016). Basidiomycete yeasts in the cortex of ascomycete macrolichens. PubMed DOI PMC

Steinová J., Škaloud P., Yahr R., Bestová H., Muggia L. (2019). Reproductive and dispersal strategies shape the diversity of mycobiont-photobiont association in PubMed DOI

Stenroos S., Hyvönen J., Myllys L., Thell A., Ahti T. (2002). Phylogeny of the genus PubMed DOI

Stenroos S., Pino-Bodas R., Hyvönen J., Lumbsch H. T., Ahti T. (2019). Phylogeny of the family Cladoniaceae (Lecanoromycetes, Ascomycota) based on sequences of multiple loci. PubMed DOI

Suchard M. A., Lemey P., Baele G., Ayres D. L., Drummond A. J., Rambaut A. (2018). Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. PubMed DOI PMC

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. PubMed DOI PMC

Ten Veldhuis M. C., Ananyev G., Dismukes G. C. (2020). Symbiosis extended: exchange of photosynthetic O PubMed DOI PMC

Thüs H., Muggia L., Pérez-Ortega S., Favero-Longo S. E., Joneson S., O’Brien H., et al. (2011). Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota). DOI

Thüs H., Schultz M. (2008).

Tormo R., Recio D., Silva I., Muñoz A. F. (2001). A quantitative investigation of airborne algae and lichen soredia obtained from pollen traps in south-west Spain. DOI

Trabucco A., Zomer R. J. (2019). PubMed PMC

Uphof J. T. (1925). The occurrence of purple bacteria as symbionts of a lichen. PubMed DOI

Vančurová L., Muggia L., Peksa O., Řídká T., Škaloud P. (2018). The complexity of symbiotic interactions influences the ecological amplitude of the host: a case study in PubMed DOI

Vandenkoornhuyse P., Husband R., Daniell T. J., Watson I. J., Duck J. M., Fitter A. H., et al. (2002). Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. PubMed DOI

Vargas A. A., Graham P. H. (1989). Cultivar and pH effects on competition for nodule sites between isolates of DOI

Vondrák J., Liška J. (2010). Changes in distribution and substrate preferences of selected threatened lichens in the Czech Republic. DOI

Weber K., Kabsch W. (1994). Intron positions in actin genes seem unrelated to the secondary structure of the protein. PubMed DOI PMC

Wedin M., Maier S., Fernandez-Brime S., Cronholm B., Westberg M., Grube M. (2016). Microbiome change by symbiotic invasion in lichens. PubMed DOI

Wei T., Simko V., Levy M., Xie Y., Jin Y., Zemla J. (2017). Package ‘corrplot’.

White T. J., Bruns T., Lee S. J. W. T., Taylor J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics.

Wilcoxon F. (1992). “Individual comparisons by ranking methods,” in DOI

Williams L., Colesie C., Ullmann A., Westberg M., Wedin M., Büdel B. (2017). Lichen acclimation to changing environments: photobiont switching vs. climate-specific uniqueness in PubMed DOI PMC

Wirtz N., Lumbsch H. T., Green T. A., Türk R., Pintado A., Sancho L., et al. (2003). Lichen fungi have low cyanobiont selectivity in maritime Antarctica. PubMed DOI

Wornik S., Grube M. (2010). Joint dispersal does not imply maintenance of partnerships in lichen symbioses. PubMed DOI

Yahr R., Vilgalys R., DePriest P. T. (2006). Geographic variation in algal partners of PubMed DOI

Zedler J. B. (2000). Progress in wetland restoration ecology. PubMed DOI

Zhang J., Kapli P., Pavlidis P., Stamatakis A. (2013). A general species delimitation method with applications to phylogenetic placements. PubMed DOI PMC

Zhang Z. S., Song X. L., Lu X. G., Xue Z. S. (2013). Ecological stoichiometry of carbon, nitrogen, and phosphorus in estuarine wetland soils: influences of vegetation coverage, plant communities, geomorphology, and seawalls. DOI

Zraik M., Booth T., Piercey-Normore M. D. (2018). Relationship between lichen species composition, secondary metabolites and soil pH, organic matter, and grain characteristics in Manitoba. DOI

Broad Ecological Niche in Seashore Lichens Emerges From a Stable, Selective Association With Generalist Algal Symbionts

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