Microgeographic distribution and mycobiont–photobiont associations in Arctic <em>Umbilicaria</em> lichens

Shunan  Cao; Chunyan Yang; Weiran  Liu; Jiewei  Sun; Chuanpeng  Liu; Qiming  Zhou

doi:10.33265/polar.v45.13990

Shunan Cao Key Laboratory for Polar Science, Polar Research Institute of China, Ministry of Natural Resources, Shanghai, China; and Key Laboratory of Polar Ecosystem and Climate Change, Shanghai Jiao Tong University, Ministry of Education, Shanghai, China
Chunyan Yang School of Life Science and Technology, Harbin Institute of Technology, Harbin, China
Weiran Liu School of Life Science and Technology, Harbin Institute of Technology, Harbin, China
Jiewei Sun Key Laboratory for Polar Science, Polar Research Institute of China, Ministry of Natural Resources, Shanghai, China
Chuanpeng Liu Key Laboratory of Polar Ecosystem and Climate Change, Shanghai Jiao Tong University, Ministry of Education, Shanghai, China; and School of Life Science and Technology, Harbin Institute of Technology, Harbin, China
Qiming Zhou School of Life Science and Technology, Harbin Institute of Technology, Harbin, China

DOI: https://doi.org/10.33265/polar.v45.13990

Keywords: Lichen symbiosis, Trebouxia jamesii, group I introns, rDNA sequencing, symbiotic flexibility, Svalbard

Abstract

Lichen symbioses are shaped by interactions between mycobionts and photobionts, yet how these relationships are structured at extremely small spatial scales in polar ecosystems remains poorly understood. Here, we investigated mycobiont–photobiont associations in Umbilicaria lichens collected from two isolated boulders in Ny-Ålesund, Svalbard, using ITS rDNA sequencing of both symbiotic partners and analyses of group I introns in mycobiont SSU rDNA. We identified five co-occurring Umbilicaria taxa across the two boulders, with four taxa occurring on each boulder. These taxa displayed pronounced horizontal and vertical segregation associated with rock orientation and surface position, revealing strong ecological structuring at the within-boulder scale. In contrast, all photobionts belonged to Trebouxia jamesii and showed low genetic differentiation, forming four weakly structured haplotype groups that were not correlated with host species or microhabitat. This pattern indicates weak sorting amongst local T. jamesii lineages and extensive photobiont sharing across mycobiont species and microhabitats. In addition, group I introns at the SSU rDNA 1769 insertion site were detected in two Umbilicaria lineages and occurred as short and long variants with highly conserved catalytic core structures. Their lineage-specific distribution and structural conservation provide additional information on mycobiont evolutionary history and may be relevant to stress responses, although their functional and adaptive significance remains to be experimentally evaluated. Together, our results demonstrate that Arctic Umbilicaria communities combine high fungal diversity and fine-scale spatial niche partitioning with broad photobiont sharing. This dual strategy of ecological differentiation and symbiotic flexibility may facilitate lichen persistence in extreme polar environments.

Downloads

Download data is not yet available.

References

Adams P.L., Stahley M.R., Gill M.L., Kosek A.B., Wang J. & Strobel S.A. 2004. Crystal structure of a group I intron splicing intermediate. RNA 10, 1867–1887, doi: 10.1261/rna.7140504.

Asplund J. & Wardle D.A. 2017. How lichens impact on terrestrial community and ecosystem properties. Biological Reviews of the Cambridge Philosophical Society 92, 1720–1738, doi: 10.1111/brv.12305.

Bhattacharya D., Friedl T. & Helms G. 2002. Vertical evolution and intragenic spread of lichen-fungal group I introns. Journal of Molecular Evolution 55, 74–84, doi: 10.1007/s00239-001-2305-x.

Burke J.M., Belfort M., Cech T.R., Davies R.W., Schweyen R.J., Shub D.A., Szostak J.W. & Tabak H.F. 1987. Structural conventions for group I introns. Nucleic Acids Research 15, 7217–7221, doi: 10.1093/nar/15.18.7217.

Cech T.R., Damberger S.H. & Gutell R.R. 1994. Representation of the secondary and tertiary structure of group I introns. Nature Structural Biology 1, 273–280, doi: 10.1038/nsb0594-273.

Cech T.R., Zaug A.J. & Grabowski P.J. 1981. In vitro splicing of the ribosomal RNA precursor of Tetrahymena: involvement of a guanosine nucleotide in the excision of the intervening sequence. Cell 27, 487–496, doi: 10.1016/0092-8674(81)90390-1.

Corsaro D. & Venditti D. 2020. Putative group I introns in the eukaryote nuclear internal transcribed spacers. Current Genetics 66, 373–384, doi: 10.1007/s00294-019-01027-0.

Dal Grande F., Rolshausen G., Divakar P.K., Crespo A., Otte J., Schleuning M. & Schmitt I. 2018. Environment and host identity structure communities of green algal symbionts in lichens. New Phytologist 217, 277–289, doi: 10.1111/nph.14770.

Damberger S.H. & Gutell R.R. 1994. A comparative database of group I intron structures. Nucleic Acids Research 22, 3508–3510, doi: 10.1093/nar/22.17.3508.

Davydov E.A., Himelbrant D.E., Kuznetsova E.S., Stepanchikova I.S. & Yakovchenko L.S. 2024. Multilocus molecular phylogeny of the Umbilicaria aprina group (Umbilicariaceae, lichenized Ascomycota) supports species level and neo-endemic status of Umbilicaria krascheninnikovii. Plants 13, article no. 729, doi: 10.3390/plants13050729.

Davydov E.A., Peršoh D. & Rambold G. 2017. Umbilicariaceae (lichenized Ascomycota)—trait evolution and a new generic concept. Taxon 66, 1282–1303, doi: 10.12705/666.2.

De Carolis R., Cometto A., Moya P., Barreno E., Grube M., Tretiach M., Leavitt S.D. & Muggia L. 2022. Photobiont diversity in lichen symbioses from extreme environments. Frontiers in Microbiology 13, article no. 809804, doi: 10.3389/fmicb.2022.809804.

del Campo E.M., Casano L.M., Gasulla F. & Barreno E. 2009. Presence of multiple group I introns closely related to bacteria and fungi in plastid 23S rRNAs of lichen-forming Trebouxia. International Microbiology 12, 59–67, doi: 10.2436/20.1501.01.82.

del Campo E.M., Catalá S., Gimeno J., del Hoyo A., Martínez-Alberola F., Casano L.M., Grube M. & Barreno E. 2013. The genetic structure of the cosmopolitan three-partner lichen Ramalina farinacea evidences the concerted diversification of symbionts. FEMS Microbiology Ecology 83, 310–323, doi: 10.1111/j.1574-6941.2012.01474.x.

Del Hoyo A., Álvarez R., Gasulla F., Casano L.M. & del Campo E.M. 2018. Origin and evolution of chloroplast group I introns in lichen algae. Journal of Phycology 54, 66–78, doi: 10.1111/jpy.12600.

DePriest P.T. & Been M.D. 1992. Numerous group I introns with variable distributions in the ribosomal DNA of a lichen fungus. Journal of Molecular Biology 228, 315–321, doi: 10.1016/0022-2836(92)90819-6.

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 Cetraria aculeata. Molecular Ecology 20, 1208–1232, doi: 10.1111/j.1365-294X.2010.04993.x.

Friedl T., Besendahl A., Pfeiffer P. & Bhattacharya D. 2000. The distribution of group I introns in lichen algae suggests that lichenization facilitates intron lateral transfer. Molecular Phylogenetics and Evolution 14, 342–352, doi: 10.1006/mpev.1999.0711.

Furulund B.M.N., Karlsen B.O., Babiak I., Haugen P. & Johansen S.D. 2022. Structural organization of S516 group I introns in myxomycetes. Genes 13, article no. 944, doi: 10.3390/genes13060944.

Gargas A., DePriest P.T. & Taylor J.W. 1995. Positions of multiple insertions in SSU rDNA of lichen-forming fungi. Molecular Biology and Evolution 12, 208–218, doi: 10.1093/oxfordjournals.molbev.a040199.

Garrido-Benavent I., Pérez-Ortega S., de los Ríos A. & Fernández-Mendoza F. 2020. Amphitropical variation of the algal partners of Pseudephebe (Parmeliaceae, lichenized fungi). Symbiosis 82, 35–48, doi: 10.1007/s13199-020-00709-5.

Gomes R.M.O.D.S., Silva K.J.G.D. & Theodoro R.C. 2024. Group I introns: structure, splicing and their applications in medical mycology. Genetics and Molecular Biology 47(Suppl. 1), e20230228, doi: 10.1590/1678-4685-GMB-2023-0228.

Gutiérrez G., Blanco O., Divakar P.K., Lumbsch H.T. & Crespo A. 2007. Patterns of group I intron presence in nuclear SSU rDNA of the lichen family Parmeliaceae. Journal of Molecular Evolution 64, 181–195, doi: 10.1007/s00239-005-0313-y.

Jüriado I., Kaasalainen U., Jylhä M. & Rikkinen J. 2019. Relationships between mycobiont identity, photobiont specificity and ecological preferences in the lichen genus Peltigera (Ascomycota) in Estonia (northeastern Europe). Fungal Ecology 39, 45–54, doi: 10.1016/j.funeco.2018.11.005.

Krzewicka B. 2004. The lichen genera Lasallia and Umbilicaria in the Polish Tatra Mts. Polish Botanical Studies 17, 1–88.

Krzewicka B., García M.A., Johansen S.D., Sancho L.G. & Martín M.P. 2009. Morphological and nuclear ribosomal DNA data support distinguishing two new species of Umbilicaria (Umbilicariaceae, Ascomycota) from Europe. The Lichenologist 41, 631–648, doi: 10.1017/S0024282909990120.

Krzewicka B. & Maciejowski W. 2008. Lichen species from the northeastern shore of Sørkapp Land (Svalbard). Polar Biology 31, 1319–1324, doi: 10.1007/s00300-008-0469-1.

Krzewicka B., Parnikoza I., Ivanets V., Yevchun H. & Smykla J. 2024. Diversity and distribution of the lichen genus Umbilicaria in the Argentine Islands–Kyiv Peninsula region, the maritime Antarctic. Scientific Reports 14, article no. 17310, doi: 10.1038/s41598-024-65806-7.

Krzewicka B. & Smykla J. 2004. The lichen genus Umbilicaria from the neighbourhood of Admiralty Bay (King George Island, maritime Antarctic), with a proposed new key to all Antarctic taxa. Polar Biology 28, 15–25, doi: 10.1007/s00300-004-0638-9.

Leavitt S.D., Kraichak E., Nelsen M.P., Altermann S., Divakar P.K., Alors D., Esslinger T.L., Crespo A. & Lumbsch H.T. 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). Molecular Ecology 24, 3779–3797, doi: 10.1111/mec.13271.

Lian K., Furulund B.M.N., Tveita A.A., Haugen P. & Johansen S.D. 2022. Mobile group I introns at nuclear rDNA position L2066 harbor sense and antisense homing endonuclease genes intervened by spliceosomal introns. Mobile DNA 13, article no. 23, doi: 10.1186/s13100-022-00280-4.

Liu T. & Pyle A.M. 2024. Highly reactive group I introns ubiquitous in pathogenic fungi. Journal of Molecular Biology 436, article no. 168513, doi: 10.1016/j.jmb.2024.168513.

Lücking R., Moncada B. & Smith C.W. 2017. The genus Lobariella (Ascomycota: Lobariaceae) in Hawaii: late colonization, high inferred endemism and three new species resulting from “micro-radiation.” The Lichenologist 49, 673–691, doi: 10.1017/S0024282917000470.

Muggia L., Leavitt S. & Barreno E. 2018. The hidden diversity of lichenised Trebouxiophyceae (Chlorophyta). Phycologia 57, 503–524, doi: 10.2216/17-134.1.

Müller U.F. 2017. Design and experimental evolution of trans-splicing group I intron ribozymes. Molecules 22, article no. 75, doi: 10.3390/molecules22010075.

Nawrocki E.P., Jones T.A. & Eddy S.R. 2018. Group I introns are widespread in archaea. Nucleic Acids Research 46, 7970–7976, doi: 10.1093/nar/gky414.

Nelsen M.P., Leavitt S.D., Heller K., Muggia L. & Lumbsch H.T. 2021. Macroecological diversification and convergence in a clade of keystone symbionts. FEMS Microbiology Ecology 97, fiab072, doi: 10.1093/femsec/fiab072.

Nelsen M.P., Lücking R., Boyce C.K., Lumbsch H.T. & Ree R.H. 2020. No support for the emergence of lichens prior to the evolution of vascular plants. Geobiology 18, 3–13, doi: 10.1111/gbi.12369.

Nyati S., Bhattacharya D., Werth S. & Honegger R. 2013. Phylogenetic analysis of LSU and SSU rDNA group I introns of lichen photobionts associated with the genera Xanthoria and Xanthomendoza (Teloschistaceae, lichenized Ascomycetes). Journal of Phycology 49, 1154–1166, doi: 10.1111/jpy.12126.

Ohmura Y., Takeshita S. & Kawachi M. 2019. Photobiont diversity within populations of a vegetatively reproducing lichen, Parmotrema tinctorum, can be generated by photobiont switching. Symbiosis 77, 59–72, doi: 10.1007/s13199-018-0572-1.

Peksa O. & Škaloud P. 2011. Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Molecular Ecology 20, 3936–3948, doi: 10.1111/j.1365-294X.2011.05168.x.

Pichler G., Muggia L., Carniel F.C., Grube M. & Kranner I. 2023. How to build a lichen: from metabolite release to symbiotic interplay. New Phytologist 238, 1362–1378, doi: 10.1111/nph.18780.

Piercey-Normore M.D. 2006. The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii. New Phytologist 169, 331–344, doi: 10.1111/j.1469-8137.2005.01576.x.

Piercey-Normore M.D. & DePriest P.T. 2001. Algal switching among lichen symbioses. American Journal of Botany 88, 1490–1498.

Rolshausen G., Hallman U., Grande F.D., Otte J., Knudsen K. & Schmitt I. 2020. Expanding the mutualistic niche: parallel symbiont turnover along climatic gradients. Proceedings of the Royal Society of London B 287, article no. 20192311, doi: 10.1098/rspb.2019.2311.

Sancho L.G., Schroeter B. & Valladares F. 1998. Umbilicaria kappeni (Umbilicariaceae) a new lichen species from Antarctica with multiple mechanisms for the simultaneous dispersal of both symbionts. Nova Hedwigia 67, 279–288, doi: 10.1127/nova.hedwigia/67/1998/279.

Tamura K., Stecher G. & Kumar S. 2021. MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38, 3022–3027, doi: 10.1093/molbev/msab120.

Thompson J.D., Higgins D.G. & Gibson T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680, doi: 10.1093/nar/22.22.4673.

White T.J., Bruns T., Lee S. & Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M.A. Innis et al. (eds.): PCR protocols: a guide to methods and applications. Pp. 315–322. San Diego: Academic Press.

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 Psora decipiens. Ecology and Evolution 7, 2560–2574, doi: 10.1002/ece3.2809.

Woodson S.A. 2005. Structure and assembly of group I introns. Current Opinion in Structural Biology 15, 324–330, doi: 10.1016/j.sbi.2005.05.007.

Yahr R., Vilgalys R. & DePriest P.T. 2004. Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Molecular Ecology 13, 3367–3378, doi: 10.1111/j.1365-294X.2004.02350.x.

Yahr R., Vilgalys R. & DePriest P.T. 2006. Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytologist 171, 847–860, doi: 10.1111/j.1469-8137.2006.01792.x.

Zhang X., Guo C., Zhang W., Cao H., Xie H., Wang K. & Liu C. 2010. A folding “framework structure” of Tetrahymena group I intron. Journal of Theoretical Biology 267, 495–501, doi: 10.1016/j.jtbi.2010.09.001.

Zhou Q.M., Guo S.Y., Huang M.R. & Wei J.C. 2006. A study of the genetic variability of Rhizoplaca chrysoleuca using DNA sequences and secondary metabolic substances. Mycologia 98, 57–67, doi: 10.3852/mycologia.98.1.57.

Microgeographic distribution and mycobiont–photobiont associations in Arctic Umbilicaria lichens

Abstract

Downloads

References