Abstract
The dual nature of fungal-algal lichen symbioses is extended by other microbial associations. Increasing evidence has confirmed that lichens are successful holobionts composed of complex and multiple species. Specific interactions between these microbes contributed to the lichens’ health, growth and fitness. Previous studies suggested that the composition of microorganisms in lichens was potentially influenced by the genetic background of the host-symbiont, large-scale geography or different photobiont-types (cyanobiont and chlorobiont). However, our knowledge of the interactions between the main symbiotic partners under a certain ecological condition and how horizontal acquisition of these microorganisms contributes to endolichenic microbiome diversity remains limited. In the present study, using amplicon sequencing, we investigated the complex diversity and community composition of fungi, bacteria, and microalgae within Heterodermia obscurata from a similar niche. We found that endophytic bacteria displayed greater diversity than fungi and microalgae. Although preferences for core taxa varied among the different definitions, all analyses support that lichen-forming genus Heterodermia and green alga Trebouxia sp. OTU A15 were the main symbionts, and the bacterium Beijerinckiaceae was the core microbiome in H. obscurata. Significantly, we found that different alga species (Trebouxia) from H. obscurata are accompanying with a shift in composition and function of endolichenic bacteria and fungi. This finding suggested that besides host- or habitat specificity as well as photobiont-types, the shifts of dominant alga may also contribute to the taxonomical and functional differences of microbiomes within lichens.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The raw data were deposited in the NCBI Sequence Read Archive (SRA) with the accession BioProject ID PRJNA672244 (https://dataview.ncbi.nlm.nih.gov/object/PRJNA672244). The voucher specimens of materials were saved in the Herbarium, Kunming Institute of Botany, CAS.
References
Ahmadjian V (1988) The lichen alga Trebouxia: does it occur free-living? Plant Syst Evol 158:243–247. https://doi.org/10.1007/BF00936348
Ahmadjian V (1993) The lichen symbiosis. Q Rev Biol 59:374–381. https://doi.org/10.2307/1294228
Ahmadjian V (2001) Trebouxia: Reflections on a perplexing and controversial lichen photobiont. Symbiosis 4:373–383
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–402. https://doi.org/10.1093/nar/25.17.3389
Archer SDJ, de los Ríos A, Lee KC, Niederberger TS, Cary SC, Coyne KJ, Douglas S, Lacap-Bugler DC, Pointing SB (2017) Endolithic microbial diversity in sandstone and granite from the McMurdo Dry Valleys, Antarctica. Polar Biol 40:997–1006. https://doi.org/10.1007/s00300-016-2024-9
Aschenbrenner IA, Cardinale M, Berg G, Grube M (2014) Microbial cargo: do bacteria on symbiotic propagules reinforce the microbiome of lichens? Environ Microbiol 16:3743–3752. https://doi.org/10.1111/1462-2920.12658
Aschenbrenner IA, Cernava T, Berg G, Grube M (2016) Understanding microbial multi-species symbioses. Front Microbiol 7:1–9. https://doi.org/10.3389/fmicb.2016.00180
Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. J Phycol. https://doi.org/10.13140/2.1.1341.1520
Bates ST, Berg-Lyons D, Lauber CL, Walters WA, Knight R, Fierer N (2012) A preliminary survey of lichen associated eukaryotes using pyrosequencing. Lichenologist 44:137–146. https://doi.org/10.1017/s0024282911000648
Bates ST, Cropsey GWG, Caporaso JG, Knight R, Fierer N (2011) Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 77:1309–1314. https://doi.org/10.1128/aem.02257-10
Bellemain E, Carlsen T, Brochmann C, Coissac E, Taberlet P, Kauserud H (2010) ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol 10:9. https://doi.org/10.1186/1471-2180-10-189
Berbee ML, Yoshimura A, Sugiyama J, Taylor JW (1995) Is Penicillium monophyletic? An evaluation of phylogeny in the family Trichocomaceae from 18S, 5.8S, and ITS ribosomal DNA sequence data. Mycologia 87:210–222. https://doi.org/10.2307/3760907
Berg G, Rybakova D, Fischer D, Cernava T, Vergès M-CC, Charles T, Chen X, Cocolin L, Eversole K, Corral GH, Kazou M, Kinkel L, Lange L, Lima N, Loy A, Macklin JA, Maguin E, Mauchline T, McClure R, Mitter B, Ryan M, Sarand I, Smidt H, Schelkle B, Roume H, Kiran GS, Selvin J, van Souza RSCd L, Singh BK, Wagner M, Walsh A, Sessitsch A, Schloter M (2020) Microbiome definition re-visited: old concepts and new challenges. Microbiome 8:103. https://doi.org/10.1186/s40168-020-00875-0
Bjelland T, Grube M, Hoem S, Jorgensen SL, Daae FL, Thorseth IH, Ovreas L (2011) Microbial metacommunities in the lichen-rock habitat. Environ Microbiol Rep 3:434–442. https://doi.org/10.1111/j.1758-2229.2010.00206.x
Blaha J, Baloch E, Grube M (2006) High photobiont diversity associated with the euryoecious lichen-forming ascomycete Lecanora rupicola (Lecanoraceae, Ascomycota). Biol J Linn Soc Lond 88:283–293. https://doi.org/10.1111/j.1095-8312.2006.00640.x
Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One 8:9. https://doi.org/10.1371/journal.pone.0056329
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu Y-X, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Cardinale M, de Castro JV, Muller H, Berg G, Grube M (2008) In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol Ecol 66:63–71. https://doi.org/10.1111/j.1574-6941.2008.00546.x
Cardinale M, Grube M, Castro JV Jr, Mueller H, Berg G (2012) Bacterial taxa associated with the lung lichen Lobaria pulmonaria are differentially shaped by geography and habitat. FEMS Microbiol Lett 329:111–115. https://doi.org/10.1111/j.1574-6968.2012.02508.x
Casano LM, del Campo EM, Garcia-Breijo FJ, Reig-Arminana J, Gasulla F, del Hoyo A, Guera A, Barreno E (2011) Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition? Environ Microbiol 13:806–818. https://doi.org/10.1111/j.1462-2920.2010.02386.x
Caspi R, Billington R, Keseler IM, Kothari A, Krummenacker M, Midford PE, Ong WK, Paley S, Subhraveti P, Karp PD (2019) The MetaCyc database of metabolic pathways and enzymes - a 2019 update. Nucleic Acids Res 48:D445–D453. https://doi.org/10.1093/nar/gkz862
Castillo RV, Beck A (2012) Photobiont selectivity and specificity in Caloplaca species in a fog-induced community in the Atacama Desert, northern Chile. Fungal Biol 116:665–676. https://doi.org/10.1016/j.funbio.2012.04.001
Cernava T, Aschenbrenner IA, Grube M, Liebminger S, Berg G (2015) A novel assay for the detection of bioactive volatiles evaluated by screening of lichen-associated bacteria. Front Microbiol 6:398. https://doi.org/10.3389/fmicb.2015.00398
Cernava T, Erlacher A, Aschenbrenner IA, Krug L, Lassek C, Riedel K, Grube M, Berg G (2017) Deciphering functional diversification within the lichen microbiota by meta-omics. Microbiome 5:13. https://doi.org/10.1186/s40168-017-0303-5
Chelius MK, Triplett EW (2001) The diversity of archaea and bacteria in association with the roots of Zea mays L. Microb Ecol 41:252–263. https://doi.org/10.1007/s002480000087
Chen KH, Miadlikowska J, Molnar K, Arnold EA, Lutzoni F (2013) Phylogenetic relationships of endophytic and endolichenic fungi reveal a new order within the class Eurotiomycetes. APS-MSA Joint Meeting
Chen T, Zhang H, Liu Y, Liu YX, Huang L (2021) EVenn: Easy to create repeatable and editable Venn diagrams and Venn networks online. J Genet Genomics. Proc Natl Acad Sci U S A. https://doi.org/10.1016/j.jgg.2021.07.007
Cohen PA, Towers GHN (1995) The Anthraquinones of Heterodermia obscurata. Phytochemistry 40:911–915. https://doi.org/10.1016/0031-9422(95)00407-x
Cordova MM, Martins DF, Silva MD, Baggio CH, Carbonero ER, Ruthes AC, Iacomini M, Santos ARS (2013) Polysaccharide glucomannan isolated from Heterodermia obscurata attenuates acute and chronic pain in mice. Carbohydr Polym 92:2058–2064. https://doi.org/10.1016/j.carbpol.2012.11.041
Cornejo C, Scheidegger C (2013) New morphological aspects of cephalodium formation in the lichen Lobaria pulmonaria (Lecanorales, Ascomycota). Lichenologist 45:77–87. https://doi.org/10.1017/s0024282912000631
Dal Grande F, Rolshausen G, Divakar PK, Crespo A, Otte J, Schleuning M, Schmitt I (2018) Environment and host identity structure communities of green algal symbionts in lichens. New Phytol 217:277–289. https://doi.org/10.1111/nph.14770
Dal Grande F, Widmer I, Wagner HH, Scheidegger C (2012) Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. Mol Ecol 21:3159–3172. https://doi.org/10.1111/j.1365-294X.2012.05482.x
De Cáceres M, Legendre P, Moretti M (2010) Improving indicator species analysis by combining groups of sites. Oikos 119:1674–1684. https://doi.org/10.1111/j.1600-0706.2010.18334.x
Del Campo EM, Casano LM, Gasulla F, Barreno E (2010) Suitability of chloroplast LSU rDNA and its diverse group I introns for species recognition and phylogenetic analyses of lichen-forming Trebouxia algae. Mol Phylogenet Evol 54:437–444. https://doi.org/10.1016/j.ympev.2009.10.024
Del Campo EM, Catala S, Gimeno J, del Hoyo A, Martinez-Alberola F, Casano LM, Grube M, Barreno E (2013) The genetic structure of the cosmopolitan three-partner lichen Ramalina farinacea evidences the concerted diversification of symbionts. FEMS Microbiol Ecol 83:310–323. https://doi.org/10.1111/j.1574-6941.2012.01474.x
Douglas GM, Maffei VJ, Zaneveld J, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI (2019) PICRUSt2: An improved and extensible approach for metagenome inference. bioRxiv. 672295. https://doi.org/10.1101/672295
Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38:685–688. https://doi.org/10.1038/s41587-020-0548-6
Doyle J (1991) DNA protocols for plants CTAB Total DNA Isolation. In: Hewitt GM, Johnston AWB, Young JPW (eds) Molecular techniques in taxonomy. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 283–293
Egidi E, de Hoog GS, Isola D, Onofri S, Quaedvlieg W, de Vries M, Verkley GJM, Stielow JB, Zucconi L, Selbmann L (2014) Phylogeny and taxonomy of meristematic rock-inhabiting black fungi in the Dothideomycetes based on multi-locus phylogenies. Fungal Divers 65:127–165. https://doi.org/10.1007/s13225-013-0277-y
Engelen A, Convey P, Popa O, Ott S (2016) Lichen photobiont diversity and selectivity at the southern limit of the maritime Antarctic region (Coal Nunatak, Alexander Island). Polar Biol 39:2403–2410. https://doi.org/10.1007/s00300-016-1915-0
Erlacher A, Cernava T, Cardinale M, Soh J, Sensen CW, Grube M, Berg G (2015) Rhizobiales as functional and endosymbiontic members in the lichen symbiosis of Lobaria pulmonaria L. Front Microbiol 6:9. https://doi.org/10.3389/fmicb.2015.00053
Eymann C, Lassek C, Wegner U, Bernhardt J, Fritsch OA, Fuchs S, Otto A, Albrecht D, Schiefelbein U, Cernava T, Aschenbrenner I, Berg G, Grube M, Riedel K (2017) Symbiotic interplay of fungi, algae, and bacteria within the lung lichen Lobaria pulmonaria L. Hoffm. as assessed by state-of-the-art metaproteomics. J Proteome Res 16:2160–2173. https://doi.org/10.1021/acs.jproteome.6b00974
Fernandez-Brime S, Muggia L, Maier S, Grube M, Wedin M (2019) Bacterial communities in an optional lichen symbiosis are determined by substrate, not algal photobionts. FEMS Microbiol Ecol 95:11. https://doi.org/10.1093/femsec/fiz012
Fernandez-Mendoza F, Fleischhacker A, Kopun T, Grube M, Muggia L (2017) ITS1 metabarcoding highlights low specificity of lichen mycobiomes at a local scale. Mol Ecol 26:4811–4830. https://doi.org/10.1111/mec.14244
Garg N, Zeng Y, Edlund A, Melnik AV, Sanchez LM, Mohimani H, Gurevich A, Miao V, Schiffler S, Lim YW, Luzzatto-Knaan T, Cai S, Rohwer F, Pevzner PA, Cichewicz RH, Alexandrov T, Dorrestein PC (2016) Spatial molecular architecture of themicrobial community of a Peltigera lichen. Msystems 1. https://doi.org/10.1128/mSystems.00139-16
Grube M, Berg G (2009) Microbial consortia of bacteria and fungi with focus on the lichen symbiosis. Fungal Biol Rev 23:72–85. https://doi.org/10.1016/j.fbr.2009.10.001
Grube M, Cardinale M, de Castro JV, Muller H, Berg G (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J 3:1105–1115. https://doi.org/10.1038/ismej.2009.63
Grube M, Cernava T, Soh J, Fuchs S, Aschenbrenner I, Lassek C, Wegner U, Becher D, Riedel K, Sensen CW, Berg G (2015) Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics. ISME J 9:412–424. https://doi.org/10.1038/ismej.2014.138
Harrell FE Jr, with contributions from Charles Dupont and many others (2021) Hmisc: Harrell Miscellaneous. R package version 4.5-0. https://CRAN.R-project.org/package=Hmisc
Harutyunyan S, Muggia L, Grube M (2008) Black fungi in lichens from seasonally arid habitats. Stud Mycol 61:83–90. https://doi.org/10.3114/sim.2008.61.08
Hassa J, Maus I, Off S, Pühler A, Scherer P, Klocke M, Schlüter A (2018) Metagenome, metatranscriptome, and metaproteome approaches unraveled compositions and functional relationships of microbial communities residing in biogas plants. Appl Microbiol Biotechnol 102:5045–5063. https://doi.org/10.1007/s00253-018-8976-7
Hawksworth DL, Grube M (2020) Lichens redefined as complex ecosystems. New Phytol 227:1281–1283. https://doi.org/10.1111/nph.16630
Hodkinson BP, Gottel NR, Schadt CW, Lutzoni F (2012) Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ Microbiol 14:147–161. https://doi.org/10.1111/j.1462-2920.2011.02560.x
Hodkinson BP, Lutzoni F (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49:163–180. https://doi.org/10.1007/s13199-009-0049-3
Honegger R (2000) Great discoveries in bryology and lichenology - Simon Schwendener (1829–1919) and the dual hypothesis of lichens. Bryologist 103:307–313. https://doi.org/10.1639/0007-2745(2000)103[0307:Ssatdh]2.0.co;2
Honegger R, Axe L, Edwards D (2013) Bacterial epibionts and endolichenic actinobacteria and fungi in the Lower Devonian lichen Chlorolichenomycites salopensis. Fungal Biol 117:512–518. https://doi.org/10.1016/j.funbio.2013.05.003
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Kosecka M, Jablonska A, Flakus A, Rodriguez-Flakus P, Kukwa M, Guzow-Krzeminska B (2020) Trentepohlialean algae (Trentepohliales, Ulvophyceae) show preference to selected mycobiont lineages in lichensymbioses. J Phycol 56:979–993. https://doi.org/10.1111/jpy.12994
Leiva D, Fernández-Mendoza F, Acevedo J, Carú M, Grube M, Orlando J (2021) The bacterial community of the foliose macro-lichen Peltigera frigida is more than a mere extension of the microbiota of the subjacent substrate. Microb Ecol 81:965–976. https://doi.org/10.1007/s00248-020-01662-y
Lohtander K, Oksanen I, Rikkinen J (2003) Genetic diversity of green algal and cyanobacterial photobionts in Nephroma (Peltigerales). Lichenologist 35:325–339. https://doi.org/10.1016/s0024-2829(03)00051-3
Lucking R, Dal-Forno M, Sikaroodi M, Gillevet PM, Bungartz F, Moncada B, Yynez-Ayabaca A, Chaves JL, Coca LF, Lawrey JD (2014) A single macrolichen constitutes hundreds of unrecognized species. Proc Natl Acad Sci U S A 111:11091–11096. https://doi.org/10.1073/pnas.1403517111
Mark K, Laanisto L, Bueno CG, Niinemets, Keller C, Scheidegger C (2020) Contrasting co-occurrence patterns of photobiont and cystobasidiomycete yeast associated with common epiphytic lichen species. New Phytol 227:1362–1375. https://doi.org/10.1111/nph.16475
Ming LI, Wang HY, Zhao ZT (2011) A molecular phylogenetic analysis of the endolichenic fungi of Umbilicariales. Shandong ence 24:14–20
Molins A, Chiva S, Calatayud Á, Marco F, García-Breijo F, Reig-Armiñana J, Carrasco P, Moya P (2020) Multidisciplinary approach to describe Trebouxia diversity within lichenized fungi Buellia zoharyi from the Canary Islands. Symbiosis 82:19–34. https://doi.org/10.1007/s13199-020-00722-8
Molins A, Moya P, García-Breijo FJ, Reig-Armiñana J, Barreno E (2018) Molecular and morphological diversity of Trebouxia microalgae in sphaerothallioid Circinaria spp. lichens1. J Phycol 54:494–504. https://doi.org/10.1111/jpy.12751
Moya P, Molins A, Martinez-Alberola F, Muggia L, Barreno E (2017) Unexpected associated microalgal diversity in the lichen Ramalina farinacea is uncovered by pyrosequencing analyses. PLoS One 12. https://doi.org/10.1371/journal.pone.0175091
Muggia L, Grube M (2010) Fungal composition of lichen thalli assessed by single strand conformation polymorphism. Lichenologist 42:461–473. https://doi.org/10.1017/s0024282909990752
Muggia L, Grube M (2018) Fungal diversity in lichens: from extremotolerance to interactions with algae. Life-Basel 8:1–14. https://doi.org/10.3390/life8020015
Muggia L, Kocourková J, Knudsen K (2015) Disentangling the complex of Lichenothelia species from rock communities in the desert. Mycologia 107:1223–1253. https://doi.org/10.3852/15-021
Muggia L, Perez-Ortega S, Kopun T, Zellnig G, Grube M (2014) Photobiont selectivity leads to ecological tolerance and evolutionary divergence in a polymorphic complex of lichenized fungi. Ann Bot 114:463–475. https://doi.org/10.1093/aob/mcu146
Mushegian AA, Peterson CN, Baker CCM, Pringle A (2011) Bacterial diversity across individual lichens. Appl Environ Microbiol 77:4249–4252. https://doi.org/10.1128/aem.02850-10
Nelsen MP, Gargas A (2009) Symbiont flexibility in Thamnolia vermicularis (Pertusariales: Icmadophilaceae). Bryologist 112:404–417. https://doi.org/10.1639/0007-2745-112.2.404
Nguyen NH, Song ZW, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006
Nilsson RH, Larsson KH, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L, Saar I, Kõljalg U, Abarenkov K (2019) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47:D259–d264. https://doi.org/10.1093/nar/gky1022
Niu B, Paulson JN, Zheng X, Kolter R (2017) Simplified and representative bacterial community of maize roots. Proc Natl Acad Sci India A 114:E2450–E2459. https://doi.org/10.1073/pnas.1616148114
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. https://doi.org/10.1007/s13199-018-0572-1
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2020) Vegan: community ecology package. R package version 2.5-7. https://CRAN.R-project.org/package=vegan
Onofri S, Zucconi L, Selbmann L, Hoog Sd R, DAdl RS, Grube M (2007) Fungal associations at the cold edge of life. In: Algae and Cyanobacteria in extreme environments, edited by Seckbach, Joseph. Springer Netherlands, Dordrecht, 735–757
Onut-Brannstrom I, Benjamin M, Scofield DG, Heidmarsson S, Andersson MGI, Lindstrom ES, Johannesson H (2018) Sharing of photobionts in sympatric populations of Thamnolia and Cetraria lichens: evidence from high-throughput sequencing. Sci Rep 8:14. https://doi.org/10.1038/s41598-018-22470-y
Pankratov TA, Kachalkin AV, Korchikov ES, Dobrovol’skaya TG (2017) Microbial communities of lichens. Microbiology 86:293–309. https://doi.org/10.1134/s0026261717030134
Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124. https://doi.org/10.1093/bioinformatics/btu494
Parrot D, Antony-Babu S, Intertaglia L, Grube M, Tomasi S, Suzuki MT (2015) Littoral lichens as a novel source of potentially bioactive Actinobacteria. Sci Rep 5:14. https://doi.org/10.1038/srep15839
Paul F, Otte J, Schmitt I, Dal Grande F (2018) Comparing Sanger sequencing and high-throughput metabarcoding for inferring photobiont diversity in lichens. Sci Rep 8. https://doi.org/10.1038/s41598-018-26947-8
Pereira MI, Ruthes AC, Carbonero ER, Marcon R, Baggio CH, Freitas CS, Santos ARS, Eliasaro S, Sassaki GL, Gorin PAJ, Iacomini M (2010) Chemical structure and selected biological properties of a glucomannan from the lichenized fungus Heterodermia obscurata. Phytochemistry 71:2132–2139. https://doi.org/10.1016/j.phytochem.2010.09.007
Platzer A, Polzin J, Rembart K, Han PP, Rauer D, Nussbaumer T (2018) BioSankey: visualization of microbial communities over time. J Integr Bioinform 15. https://doi.org/10.1515/jib-2017-0063
Prillinger H, Kraepelin G, Lopandic K, Schweigkofler W, Molnar O, Weigang F, Dreyfuss MM (1997) New species of Fellomyces isolated from epiphytic lichen species. Syst Appl Microbiol 20:572–584. https://doi.org/10.1016/s0723-2020(97)80029-x
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
Rangseekaew P, Pathom-Aree W (2019) Cave Actinobacteria as producers of bioactive metabolites. Front Microbiol 10:387. https://doi.org/10.3389/fmicb.2019.00387
Revelle W (2013) Psych: Procedures for psychological, psychometric, and personality pesearch. R package version 1.0–95. Evanston, Illinois
Rikkinen J, Oksanen I, Lohtander K (2002) Lichen guilds share related cyanobacterial symbionts. Science 297:357–357. https://doi.org/10.1126/science.1072961
Schneider T, Schmid E, de Castro JV, Cardinale M, Eberl L, Grube M, Berg G, Riedel K (2011) Structure and function of the symbiosis partners of the lung lichen (Lobaria pulmonaria L. Hoffm.) analyzed by metaproteomics. Proteomics 11:2752–2756. https://doi.org/10.1002/pmic.201000679
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60
Selbmann L, Hoog S, Mazzaglia A, Friedmann EI, Onofri S (2005) Fungi at the edge of life: Cryptoendolithic black fungi from Antarctic desert. Stud Mycol 51:1–32
Selbmann L, Isola D, Egidi E, Zucconi L, Gueidan C, de Hoog GS, Onofri S (2014) Mountain tips as reservoirs for new rock-fungal entities: Saxomyces gen. nov. and four new species from the Alps. Fungal Divers 65:167–182. https://doi.org/10.1007/s13225-013-0234-9
Simon JC, Marchesi JR, Mougel C, Selosse MA (2019) Host-microbiota interactions: from holobiont theory to analysis. Microbiome 7:5. https://doi.org/10.1186/s40168-019-0619-4
Singh G, Kukwa M, Dal Grande F, Łubek A, Otte J, Schmitt I (2019) A glimpse into genetic diversity and symbiont interaction patterns in lichen communities from areas with different disturbance histories in Białowieża Forest, Poland. Microorganisms 7:335. https://doi.org/10.3390/microorganisms7090335
Suryanarayanan TS, Thirunavukkarasu N (2017) Endolichenic fungi: the lesser known fungal associates of lichens. Mycology 8:189–196. https://doi.org/10.1080/21501203.2017.1352048
Tehler A (1996) Systematics, phylogeny and classification. In: Lichen Biology, edited by Nash, T.H., III. Cambridge University Press, Cambridge, 217–239
U’Ren JM, Lutzoni F, Miadlikowska J, Arnold AE (2010) Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microb Ecol 60:340–353. https://doi.org/10.1007/s00248-010-9698-2
U’Ren JM, Riddle JM, Monacell JT, Carbone I, Miadlikowska J, Arnold AE (2014) Tissue storage and primer selection influence pyrosequencing-based inferences of diversity and community composition of endolichenic and endophytic fungi. Mol Ecol Resour 14:1032–1048. https://doi.org/10.1111/1755-0998.12252
Wei J (2018) A review on the present situation of lichenology in China. Mygosystema 37:812–818
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA Genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols, a guide to methods and applications. Academic Press, San Diego, pp 315–322
Zhang T, Wei XL, Zhang YQ, Liu HY, Yu LY (2015) Diversity and distribution of lichen-associated fungi in the Ny-Alesund Region (Svalbard, High Arctic) as revealed by 454 pyrosequencing. Sci Rep 5:10. https://doi.org/10.1038/srep14850
Acknowledgements
The authors thank Dr. Jian Liu, Ying Zheng, Yujuan Zhao and Li Hu for manuscript revision. We would like to thank the anonymous reviewers for the thoughtful comments and constructive suggestions toward improving our manuscript.
Funding
This work was supported by the National Key R&D Program of China [2017YF0505200 to H.S.] and the Strategic Biological Resources Service Network Programme of Chinese Academy of Sciences [ZSSD-006 to X.G. ].
Author information
Authors and Affiliations
Contributions
Xun Gong contributed to the study conception. Lisong Wang identified the material. Haiyan Xu and Xiuyan Feng performed data collection and analyses. Haiyan Xu wrote the first draft, and all authors commented, revised and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 462 KB)
Rights and permissions
About this article
Cite this article
Xu, H., Wang, L., Feng, X. et al. Core taxa and photobiont-microbial interaction within the lichen Heterodermia obscurata (Physcsiaceae, Heterodermia). Symbiosis 86, 187–204 (2022). https://doi.org/10.1007/s13199-022-00832-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-022-00832-5