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Polyol-assimilation capacities of lichen-inhabiting fungi

Published online by Cambridge University Press:  04 March 2020

Kanami Yoshino Open the ORCID record for Kanami Yoshino [Opens in a new window] ,
Kohei Yamamoto ,
Hiroshi Masumoto ,
Yousuke Degawa ,
Hiroko Yoshikawa ,
Hiroshi Harada  and
Kazunori Sakamoto
Kanami Yoshino*
Affiliation:
Graduate School of Horticulture, Chiba University, 648 Matsudo, Matsudo, Chiba271-8510, Japan
Kohei Yamamoto
Affiliation:
Tochigi Prefectural Museum, 2-2 Mutsumi-cho, Utsunomiya, Tochigi320-0865, Japan
Hiroshi Masumoto
Affiliation:
Mountain Science Center, Sugadaira Research Station, University of Tsukuba, 1278-294, Sugadaira, Nagano386-2204, Japan
Yousuke Degawa
Affiliation:
Mountain Science Center, Sugadaira Research Station, University of Tsukuba, 1278-294, Sugadaira, Nagano386-2204, Japan
Hiroko Yoshikawa
Affiliation:
Natural History Museum & Institute, Chiba, Aoba-cho 955-2, Chuo-ku, Chiba260-8682, Japan
Hiroshi Harada
Affiliation:
Natural History Museum & Institute, Chiba, Aoba-cho 955-2, Chuo-ku, Chiba260-8682, Japan
Kazunori Sakamoto
Affiliation:
Graduate School of Horticulture, Chiba University, 648 Matsudo, Matsudo, Chiba271-8510, Japan
*
Author for correspondence: Kanami Yoshino. E-mail: [email protected]
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Abstract

Fungi are one of the most diverse carbon source-assimilating organisms, living as saprobes, parasites and symbionts; they play an important role in carbon cycling in the ecosystem. A lichen thallus provides habitats for many non-lichenized fungi and usually contains large quantities of polyols. However, research has not been undertaken to identify carbon sources of lichen-inhabiting fungi. In this study, we isolated various lichen-inhabiting fungi from surface-sterilized Ramalina spp., Flavoparmelia caperata and Peltigera degenii, and demonstrated their ability to assimilate carbon sources, namely glucose, ribitol and mannitol. Several isolates efficiently assimilated mannitol and ribitol; however, most isolates could assimilate only mannitol or both ribitol and mannitol at low levels. It is suggested that there are different preferences and niche segregation of carbon sources among lichen-inhabiting fungi, and that this assemblage includes fungi with different lifestyles such as saprobes, endophytes and transient visitors.

Keywords

DothideomycetesLecanoromycetesmannitolPezizomycetesribitolSordariomycetes
Type
Standard Papers
Information
The Lichenologist , Volume 52 , Issue 1 , January 2020 , pp. 49 - 59
Copyright
Copyright © British Lichen Society 2020

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References

Arnold, AE, Miadlikowska, J, Higgins, KL, Sarvate, SD, Gugger, P, Way, A, Hofstetter, V, Kauff, F and Lutzoni, F (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Systematic Biology 58, 283–297. doi: 10.1093/sysbio/syp001CrossRefGoogle ScholarPubMed
Beck, A, Friedel, T and Rambold, G (1998) Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytologist 139, 709–720. doi: 10.1046/j.1469-8137.1998.00231.xCrossRefGoogle Scholar
Beckett, RP, Zavarzina, AG and Liers, C (2013) Oxidoreductases and cellulases in lichens: possible roles in lichen biology and soil organic matter turnover. Fungal Biology 117, 431–438. doi: 10.1016/j.funbio.2013.04.007CrossRefGoogle ScholarPubMed
Carbone, M, Loizides, M and Alvarado, P (2015) Preliminary phylogenetic and morphological studies in the Plectania melastoma lineage (Ascomycota, Pezizales). Ascomycete.org 7, 23–29.Google Scholar
Chapman, BE, Roser, DJ and Seppelt, RD (1994) 13C NMR analysis of Antarctic cryptogam extracts. Antarctic Science 6, 295–305. doi: 10.1017/S0954102094000465CrossRefGoogle Scholar
Coronado-Ruiz, C, Avendaño, R, Escudero-Leyva, E, Conejo-Barboza, G, Chaverri, P and Chavarría, M (2018) Two new cellulolytic fungal species isolated from a 19th-century art collection. Scientific Reports 8, 7492. doi: 10.1038/s41598-018-24934-7CrossRefGoogle ScholarPubMed
Culberson, CF (1972) Improved conditions and new data for the identification of lichen products by a standardized thin-layer chromatographic method. Journal of Chromatography A 72, 113–125. doi: 10.1016/0021-9673(72)80013-XCrossRefGoogle ScholarPubMed
Culberson, CF and Johnson, A (1976) A standardized two dimensional thin-layer chromatographic method for lichen products. Journal of Chromatography A 128, 253–259. doi: 10.1016/S0021-9673(00)99256-2CrossRefGoogle Scholar
Culberson, CF and Johnson, A (1982) Substitution of methyl tert.-butyl ether for diethyl ether in the standardized thin-layer chromatographic method for lichen products. Journal of Chromatography A 238, 483–487. doi: 10.1016/S0021-9673(00)81336-9CrossRefGoogle Scholar
Culberson, CF and Kristinsson, HD (1970) A standardized method for the identification of lichen products. Journal of Chromatography A 46, 85–93. doi: 10.1016/S0021-9673(00)83967-9CrossRefGoogle Scholar
da Silva, MDLC, Iacomini, M, Jablonski, E and Gorin, PA (1993) Carbohydrate, glycopeptide and protein components of the lichen Sticta sp. and effect of storage. Phytochemistry 33, 547–552.CrossRefGoogle Scholar
Davis, EC, Franklin, JB, Shaw, AJ and Vilgalys, R (2003) Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: phylogenetics, distribution, and symbiosis. American Journal of Botany 90, 1661–1667. doi: 10.3732/ajb.90.11.1661CrossRefGoogle ScholarPubMed
Diederich, P and Puntillo, D (1995) New or interesting lichenicolous fungi. 7. Nectria brutia sp. nov. (Ascomycotina, Hypocreales). Bulletin de la Société des Naturalistes Luxembourgeois 96, 95–98.Google Scholar
Doveri, F (2011) Addition to “Fungi Fimicoli Italici”: an update on the occurrence of coprophilous Basidiomycetes and Ascomycetes in Italy with new records and descriptions. Mycosphere 2, 331–427.Google Scholar
Drew, EA and Smith, DC (1967) Studies in the physiology of lichens. VIII. Movement of glucose from alga to fungus during photosynthesis in the thallus of Peltigera polydactyla. New Phytologist 66, 389–400.CrossRefGoogle Scholar
Eisenreich, W, Knispel, N and Beck, A (2011) Advanced methods for the study of the chemistry and the metabolism of lichens. Phytochemistry Reviews 10, 445–456. doi: 10.1007/s11101-011-9215-3CrossRefGoogle Scholar
Fernández-Mendoza, F, Fleischhacker, A, Kopun, T, Grube, M and Muggia, L (2017) ITS1 metabarcoding highlights low specificity of lichen mycobiomes at a local scale. Molecular Ecology 26, 4811–4830. doi: 10.1111/mec.14244CrossRefGoogle Scholar
Gaio-Oliveira, G, Dahlman, L, Palmqvist, K, Martins-Loução, MA and Máguas, C (2005) Nitrogen uptake in relation to excess supply and its effects on the lichens Evernia prunastri (L.) Ach and Xanthoria parietina (L.) Th. Fr. Planta 220, 794–803. doi: 10.1007/s00425-004-1396-1CrossRefGoogle Scholar
Geydan, TD, Debets, AJ, Verkley, GJ and Van Diepeningen, AD (2012) Correlated evolution of senescence and ephemeral substrate use in the Sordariomycetes. Molecular Ecology 21, 2816–2828. doi: 10.1111/j.1365-294X.2012.05569.xCrossRefGoogle ScholarPubMed
Gonzalez-Menendez, V, Martin, J, Siles, JA, Gonzalez-Tejero, MR, Reyes, F, Platas, G, Tormo, JR and Genilloud, O (2017) Biodiversity and chemotaxonomy of Preussia isolates from the Iberian Peninsula. Mycological Progress 16, 713–728. doi: 10.1007/s11557-017-1305-1CrossRefGoogle Scholar
Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hansen, K, Laessoe, T and Pfister, DH (2002) Phylogenetic diversity in the core group of Peziza inferred from ITS sequences and morphology. Mycological Research 106, 879–902. doi: 10.1017/S0953756202006287CrossRefGoogle Scholar
Hawksworth, DL and Sherwood, MA (1981) A reassessment of three widespread resinicolous discomycetes. Canadian Journal of Botany 59, 357–372.CrossRefGoogle Scholar
Henskens, FL, Green, TGA and Wilkins, A (2012) Cyanolichens can have both cyanobacteria and green algae in a common layer as major contributors to photosynthesis. Annals of Botany 110, 555–563. doi: 10.1093/aob/mcs108CrossRefGoogle Scholar
Honegger, R (2012) The symbiotic phenotype of lichen-forming ascomycetes and their endo- and epibionts. In Hock, B (ed.) The Mycota IX, Fungal Associations, 2nd Edition. Berlin, Heidelberg: Springer-Verlag, pp. 305–315.Google Scholar
Honegger, R, Axe, L and Edwards, D (2013) Bacterial epibionts and endolichenic actinobacteria and fungi in the Lower Devonian lichen Chlorolichenomycites salopensis. Fungal Biology 117, 512–518. doi: 10.1016/j.funbio.2013.05.003CrossRefGoogle ScholarPubMed
Iwamoto, K and Shiraiwa, Y (2005) Salt-regulated mannitol metabolism in algae. Marine Biotechnology 7, 407–415. doi: 10.1007/s10126-005-0029-4CrossRefGoogle Scholar
Izumitsu, K, Hatoh, K, Sumita, T, Kitade, Y, Morita, A, Gafur, A, Ohta, A, Kawai, M, Yamanaka, T, Neda, H, et al. (2012) Rapid and simple preparation of mushroom DNA directly from colonies and fruiting bodies for PCR. Mycoscience 53, 396–401. doi: 10.1007/s10267-012-0182-3CrossRefGoogle Scholar
Knapp, DG, Kovács, GM, Zajta, E, Groenewald, JZ and Crous, PW (2015) Dark septate endophytic pleosporalean genera from semiarid areas. Persoonia 35, 87–100. doi: 10.3767/003158515X687669CrossRefGoogle ScholarPubMed
Komiya, T and Shibata, S (1971) Polyols produced by the cultured phyco- and mycobionts of some Ramalina species. Phytochemistry 10, 695–699.CrossRefGoogle Scholar
Koukol, O and Baldrian, P (2012) Intergeneric variability in enzyme production of microfungi from pine litter. Soil Biology and Biochemistry 49, 1–3.CrossRefGoogle Scholar
Kroken, S and Taylor, JW (2000) Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist 103, 645–660. doi: 10.1639/0007-2745(2000)103[0645:PSRMAS]2.0.CO;2CrossRefGoogle Scholar
Lagarde, A, Jargeat, P, Roy, M, Girardot, M, Imbert, C, Millot, M and Mambu, L (2018) Fungal communities associated with Evernia prunastri, Ramalina fastigiata and Pleurosticta acetabulum: three epiphytic lichens potentially active against Candida biofilms. Microbiological Research 211, 1–12. doi: 10.1016/j.micres.2018.03.006CrossRefGoogle ScholarPubMed
Lewis, DH and Smith, DC (1967) Sugar alcohols (polyols) in fungi and green plants. I. Distribution, physiology and metabolism. New Phytologist 66, 143–184.CrossRefGoogle Scholar
Li, WC, Zhou, J, Guo, SY and Guo, LD (2007) Endophytic fungi associated with lichens in Baihua mountain of Beijing, China. Fungal Diversity 25, 69–80.Google Scholar
Liers, C, Ullrich, R, Steffen, KT, Hatakka, A and Hofrichter, M (2006) Mineralization of 14C-labelled synthetic lignin and extracellular enzyme activities of the wood-colonizing ascomycetes Xylaria hypoxylon and Xylaria polymorpha. Applied Microbiology and Biotechnology 69, 573–579.CrossRefGoogle ScholarPubMed
Liers, C, Ullrich, R, Pecyna, M, Schlosser, D and Hofrichter, M (2007) Production, purification and partial enzymatic and molecular characterization of a laccase from the wood-rotting ascomycete Xylaria polymorpha. Enzyme and Microbial Technology 41, 785–793.CrossRefGoogle Scholar
Lilly, VG and Barnett, HL (1951) Physiology of the Fungi. New York: McGraw-Hill.Google Scholar
Mandyam, K, Loughin, T and Jumpponen, A (2010) Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie. Mycologia 102, 813–821.CrossRefGoogle ScholarPubMed
Masumoto, H and Degawa, Y (2019) The effect of surface sterilization and the type of sterilizer on the genus composition of lichen-inhabiting fungi with notes on some frequently isolated genera. Mycoscience 60, 331–342. doi: 10.1016/j.myc.2019.07.004CrossRefGoogle Scholar
Muggia, L and Grube, M (2018) Fungal diversity in lichens: from extremotolerance to interactions with algae. Life 8, 15. doi: 10.3390/life8020015CrossRefGoogle ScholarPubMed
Olafsdottir, ES and Ingólfsdottir, K (2001) Polysaccharides from lichens: structural characteristics and biological activity. Planta Medica 67, 199–208.CrossRefGoogle ScholarPubMed
Osono, T (2007) Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecological Research 22, 955–974. doi: 10.1007/s11284-007-0390-zCrossRefGoogle Scholar
Osono, T, Tateno, O and Masuya, H (2013) Diversity and ubiquity of xylariaceous endophytes in live and dead leaves of temperate forest trees. Mycoscience 54, 54–61. doi: 10.1016/j.myc.2012.08.003CrossRefGoogle Scholar
Richardson, DHS and Smith, DC (1968) Lichen physiology IX. Carbohydrate movement from the Trebouxia symbiont of Xanthoria aureola to the fungus. New Phytologist 67, 61–68.CrossRefGoogle Scholar
Richardson, DHS, Hill, DJ and Smith, DC (1968) Lichen physiology XI. The role of the alga in determining the pattern of carbohydrate movement between lichen symbionts. New Phytologist 67, 469–486.CrossRefGoogle Scholar
Rogers, JD, Miller, AN and Vasilyeva, LN (2008) Pyrenomycetes of the Great Smoky Mountains National Park. VI. Kretzschmaria, Nemania, Rosellinia and Xylaria (Xylariaceae). Fungal Diversity 29, 109–118.Google Scholar
Roser, DJ, Melick, DR, Ling, HU and Seppelt, RD (1992) Polyol and sugar content of terrestrial plants from continental Antarctica. Antarctic Science 4, 413–420. doi: 10.1017/S0954102092000610CrossRefGoogle Scholar
Sakata, A, Matsuzaki, T, Yoshikawa, H and Harada, H (2019) Lichens of Sugadaira Montane Research Center, University of Tsukuba, Ueda-shi, Nagano-ken, central Japan, as a record of collection during the 12th Field Meetings of the Japanese Society for Lichenology (Nov. 2013). Lichenology 18, 23–28.Google Scholar
Smith, DC (1961) The physiology of Peltigera polydactyla (Neck.) Hoffm. Lichenologist 1, 209–226.CrossRefGoogle Scholar
Smith, DC (1963) Studies in the physiology of lichens IV. Carbohydrates in Peltigera polydactyla and the utilization of absorbed glucose. New Phytologist 62, 205–216. doi: 10.1111/j.1469-8137.1963.tb06327.xCrossRefGoogle Scholar
Smith, DC (1968) The movement of carbohydrate from alga to fungus in lichens. Bulletin de la Société Botanique de France 115, 129–133. doi: 10.1080/00378941.1968.10838622CrossRefGoogle Scholar
Spribille, T, Tuovinen, V, Resl, P, Vanderpool, D, Wolinski, H, Aime, MC, Schneider, K, Stabentheiner, E, Toome-Heller, M, Thor, G, et al. (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353, 488–492. doi: 10.1126/science.aaf8287CrossRefGoogle ScholarPubMed
Stoop, JMH, Williamson, JD and Pharr, DM (1996) Mannitol metabolism in plants: a method for coping with stress. Trends in Plant Science 1, 139–144. doi: 10.1016/S1360-1385(96)80048-3CrossRefGoogle Scholar
Suryanarayanan, TS, Govindarajulu, MB, Rajamani, T, Tripathi, M and Joshi, Y (2017) Endolichenic fungi in lichens of Champawat district, Uttarakhand, northern India. Mycological Progress 16, 205–211. doi: 10.1007/s11557-016-1268-7CrossRefGoogle Scholar
Tanaka, K, Hirayama, K, Yonezawa, H, Sato, G, Toriyabe, A, Kudo, H, Hashimoto, A, Matsumura, M, Harada, Y, Kurihara, Y, et al. (2015) Revision of the Massarineae (Pleosporales, Dothideomycetes). Studies in Mycology 82, 75–136. doi: 10.1016/j.simyco.2015.10.002CrossRefGoogle Scholar
Tedersoo, L and Smith, ME (2013) Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biology Reviews 27, 83–99.CrossRefGoogle Scholar
Tuovinen, V, Ekman, S, Thor, G, Vanderpool, D, Spribille, T and Johannesson, H (2019) Two basidiomycete fungi in the cortex of wolf lichens. Current Biology 29, 1–8. doi: 10.1016/j.cub.2018.12.022CrossRefGoogle ScholarPubMed
Tysiaczny, MJ and Kershaw, KA (1979) Physiological-environmental interactions in lichens. VII. The environmental control of glucose movement from alga to fungus in Peltigera canina v. praetextata Hue. New Phytologist 83, 137–146. doi: 10.1111/j.1469-8137.1979.tb00735.xCrossRefGoogle Scholar
U'Ren, JM, Lutzoni, F, Miadlikowska, J and Arnold, AE (2010) Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microbial Ecology 60, 340–353. doi: 10.1007/s00248-010-9698-2CrossRefGoogle ScholarPubMed
U'Ren, JM, Lutzoni, F, Miadlikowska, J, Laetsch, AD and Arnold, AE (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. American Journal of Botany 99, 898–914. doi: 10.3732/ajb.1100459CrossRefGoogle Scholar
U'Ren, JM, Riddle, JM, Monacell, JT, Carbone, I, Miadlikowska, J and Arnold, AE (2014) Tissue storage and primer selection influence pyrosequencing-based inferences of diversity and community composition of endolichenic and endophytic fungi. Molecular Ecology Resources 14, 1032–1048. doi: 10.1111/1755-0998.12252Google ScholarPubMed
U'Ren, JM, Miadlikowska, J, Zimmerman, NB, Lutzoni, F, Stajich, JE and Arnold, AE (2016) Contributions of North American endophytes to the phylogeny, ecology, and taxonomy of Xylariaceae (Sordariomycetes, Ascomycota). Molecular Phylogenetics and Evolution 98, 210–232. doi: 10.1016/j.ympev.2016.02.010CrossRefGoogle Scholar
Wang, Y, Zheng, Y, Wang, X, Wei, X and Wei, J (2016) Lichen-associated fungal community in Hypogymnia hypotrypa (Parmeliaceae, Ascomycota) affected by geographic distribution and altitude. Frontiers in Microbiology 5, 1231. doi: 10.3389/fmicb.2016.01231Google Scholar
Wendt, L, Sir, EB, Kuhnert, E, Heitkämper, S, Lambert, C, Hladki, AI, Romero, AI, Luangsa-ard, JJ, Srikitikulchai, P, Peršoh, D, et al. (2018) Resurrection and emendation of the Hypoxylaceae, recognized from a multigene phylogeny of the Xylariales. Mycological Progress 17, 115–154. doi: 10.1007/s11557-017-1311-3CrossRefGoogle Scholar
White, TJ, Bruns, T, Lee, S and Taylor, JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, MA, Gelfand, DH, Sninsky, JJ and White, TJ (eds), PCR Protocols: a Guide to Methods and Applications. New York: Academic Press, pp. 315–322. doi: 10.1016/b978-0-12-372180-8.50042-1Google Scholar
Yoshino, K, Yamamoto, K, Hara, K, Sonoda, M, Yamamoto, Y and Sakamoto, K (2019 a) The conservation of polyol transporter proteins and their involvement in lichenized Ascomycota. Fungal Biology 123, 318–329. doi: 10.1016/j.funbio.2019.01.006CrossRefGoogle ScholarPubMed
Yoshino, K, Kawakami, H and Sakamoto, K (2019 b) Optimizing synthetic culture medium for growth of Ramalina conduplicans mycobiont. Lichenology 18, 1–7.Google Scholar
Zhang, T, Wei, XL, Zhang, YQ, Liu, HY and Yu, LY (2015) Diversity and distribution of lichen-associated fungi in the Ny-Ålesund Region (Svalbard, High Arctic) as revealed by 454 pyrosequencing. Scientific Reports 14, 14850. doi: 10.1038/srep14850CrossRefGoogle Scholar
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