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Metagenomic data reveal diverse fungal and algal communities associated with the lichen symbiosis

Abstract

Lichens have traditionally been considered the symbiotic phenotype from the interactions of a single fungal partner and one or few photosynthetic partners. However, lichen symbioses have been shown to be far more complex and may include a wider range of other interacting organisms, including non-photosynthetic bacteria, accessory fungi, and algae. In this study, we analyzed metagenomic shotgun sequences in an attempt to characterize lichen mycobiomes. Specifically, we inferred the range of fungi associated within lichen thalli from five groups of lichens – horsehair lichens (mycobiont = Bryoria spp.), shadow lichens (taxa in Physciaceae), rock posies (Rhizoplaca spp.), rock tripes (Umbilicaria spp.), and green rock shields (Xanthoparmelia spp.). Metagenomic reads from the multi-copy nuclear ribosomal internal transcribed spacer region, the standard DNA barcode region for fungi, were extracted, clustered, and used to infer taxonomic assignments. Our data revealed diverse lichen-associated mycobiomes. Many of the members of the lichen-associated mycobiomes that were identified here have not previously been found in association with lichens. Furthermore, closely related mycobionts tended to have more similar mycobiomes. We found little evidence supporting the ubiquitous presence of Cystobasidiales yeasts in macrolichens, although reads representing this putative symbiotic partner were found in samples of Bryoria lichens, albeit in low abundance. Our study further highlights the ecosystem-like features of lichens, with partners and interactions far from being completely understood. Future research is needed to more fully and accurately characterize lichen mycobiomes and how these fungi interact with the major lichen components, the photo- and mycobionts.

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References

  • Anslan S, Nilsson RH, Wurzbacher C, Baldrian P, Leho T, Bahram M (2018) Great differences in performance and outcome of high-throughput sequencing data analysis platforms for fungal metabarcoding. MycoKeys 39:29–40

    Google Scholar 

  • Arnold AE, Miadlikowska J, Higgins KL, Sarvate SD, Gugger P, Way A, Hofstetter V, Kauff F, Lutzoni F (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58:283–297

    PubMed  Google Scholar 

  • Bačkor M, Peksa O, Škaloud P, Bačkorová M (2010) Photobiont diversity in lichens from metal-rich substrata based on ITS rDNA sequences. Ecotoxicol Environ Saf 73:603–612

    PubMed  Google Scholar 

  • Bates ST, Cropsey GW, Caporaso JG, Knight R, Fierer N (2011) Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 77:1309–1314

    CAS  PubMed  Google Scholar 

  • Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Gregory Caporaso J (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2's q2-feature-classifier plugin. Microbiome 6:90

    PubMed  PubMed Central  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 YX, 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 II, 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boustie J, Grube M (2005) Lichens - a promising sources of bioactive secondary metabolites. Plant Gen Res 3:273–287

    CAS  Google Scholar 

  • Bradshaw M, Grewe F, Thomas A, Harrison CH, Lindgren H, Muggia L, St Clair LL, Lumbsch HT, Leavitt SD (2020) Characterizing the ribosomal tandem repeat and its utility as a DNA barcode in lichen-forming fungi. BMC Evol Biol 20:2

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cao S, Zhang F, Liu C, Hao Z, Tian Y, Zhu L, Zhou Q (2015) Distribution patterns of haplotypes for symbionts from Umbilicaria esculenta and U muehlenbergii reflect the importance of reproductive strategy in shaping population genetic structure. BMC Microbiol 15:212

    PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cardinale M, Puglia AM, Grube M (2006) Molecular analysis of lichen-associated bacterial communities. FEMS Microbiol Ecol 57:484–495

    CAS  PubMed  Google Scholar 

  • Cardinale M, Grube M, Castro JV Jr, Muller 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

    CAS  PubMed  Google Scholar 

  • Černajová I, Škaloud P (2019) The first survey of Cystobasidiomycete yeasts in the lichen genus Cladonia; with the description of Lichenozyma pisutiana gen nov, sp nov. Fungal Biol 123:625–637

    PubMed  Google Scholar 

  • 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 5:82

    PubMed  PubMed Central  Google Scholar 

  • Crittenden PD, David JC, Hawksworth DL, Campbell FS (1995) Attempted isolation and success in the culturing of a broad spectrum of lichen-forming and lichenicolous fungi. New Phytol 130:267–297

    Google Scholar 

  • Dal Grande F, Alors D, Divakar PK, Bálint M, Crespo A, Schmitt I (2014) Insights into intrathalline genetic diversity of the cosmopolitan lichen symbiotic green alga Trebouxia decolorans Ahmadjian using microsatellite markers. Mol Phylogenet Evol 72:54–60

    PubMed  Google Scholar 

  • Dal Grande F, Sharma R, Meiser A, Rolshausen G, Büdel B, Mishra B, Thines M, Otte J, Pfenninger M, Schmitt I (2017) Adaptive differentiation coincides with local bioclimatic conditions along an elevational cline in populations of a lichen-forming fungus. BMC Evol Biol 17:93

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Diederich P (1996) The lichenicolous heterobasidiomycetes. Bibliotheca Lichenologica 61:1–198

    Google Scholar 

  • Fernández-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(3):fiz012. 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

    CAS  PubMed  Google Scholar 

  • Fleischhacker A, Grube M, Kopun T, Hafellner J, Muggia L (2015) Community analyses uncover high diversity of lichenicolous fungi in alpine habitats. Microb Ecol 70:348–360

    PubMed  Google Scholar 

  • Girlanda M, Isocrono D, Bianco C, Luppi-Mosca A (1997) Two foliose lichens as microfungal ecological niches. Mycologia 89:531–536

    Google Scholar 

  • Gostinčar C, Grube M, De Hoog S, Zalar P, Gunde-Cimerman N (2009) Extremotolerance in fungi: evolution on the edge. FEMS Microbiol Ecol 71:2–11

    Google Scholar 

  • Goward T (2008) Nameless little things. Evansia 25:54–56

    Google Scholar 

  • Grube M, Cardinale M, de Castro Jr JV, Muller H, Berg G (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J 3:1105–1115

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Hawksworth DL, Lücking R (2017) Fungal diversity revisited: 22 to 38 million species. Microbiol Spectr 5

  • Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson O, Huhndorf S, James T, Kirk PM, Lücking R, Lumbsch T, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai Y-C, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde K, Koljalg U, Kurtzman CP, Larsson KH, Lichtward R, Longcore J, Miadlikowska J, Miller A, Monclavo J-M, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schuessler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White M, Winka K, Yao Y-J, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547

    PubMed  Google Scholar 

  • Hodkinson B, Lutzoni F (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49:163–180

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Honegger R (2000) Simon Schwendener (1829-1919) and the dual hypothesis of lichens. Bryologist 103:307–313

    Google Scholar 

  • Honegger R (2001) The symbiotic phenotype of lichen-forming ascomycetes. In: Fungal Associations. Springer, Berlin, Heidelberg, pp 165–188

    Google Scholar 

  • Honegger R (1993) Developmental biology of lichens. New Phytol 125:659–677

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    PubMed  PubMed Central  Google Scholar 

  • Keepers KG, Pogoda CS, White KH, Anderson Stewart CR, Hoffman JR, Ruiz AM, Mccain CM, Lendemer JC, Kane NC, Tripp EA (2019) Whole genome shotgun sequencing detects greater lichen fungal diversity than amplicon-based methods in environmental samples. Front Ecol Evol:7

  • Kono M, Tanabe H, Ohmura Y, Satta Y, Terai Y (2017) Physical contact and carbon transfer between a lichen-forming Trebouxia alga and a novel Alphaproteobacterium. Microbiology 163:678–691

    CAS  PubMed  Google Scholar 

  • LaBonte NR, Jacobs J, Ebrahimi A, Lawson S, Woeste K (2018) Data mining for discovery of endophytic and epiphytic fungal diversity in short-read genomic data from deciduous trees. Fungal Ecol 35:1–9

    Google Scholar 

  • Lawrey JD, Diederich P (2003) Lichenicolous fungi: interactions, evolution, and biodiversity. Bryologist 106:80–120

    Google Scholar 

  • Leavitt SD, Johnson LA, Goward T, St Clair LL (2011) Species delimitation in taxonomically difficult lichen-forming fungi: an example from morphologically and chemically diverse Xanthoparmelia (Parmeliaceae) in North America. Mol Phylogenet Evol 60:317–332

    PubMed  Google Scholar 

  • Leavitt SD, Fernández-Mendoza F, Pérez-Ortega S, Sohrabi M, Divakar PK, Vondrák J, Lumbsch HT, St. Clair LL (2013a) Local representation of global diversity in a cosmopolitan lichen-forming fungal species complex (Rhizoplaca, Ascomycota). J Biogeogr 40:1792–1806

    Google Scholar 

  • Leavitt SD, Nelsen MP, Lumbsch HT, Johnson LA, St Clair LL (2013b) Symbiont flexibility in subalpine rock shield lichen communities in the southwestern USA. Bryologist 116:149–161

    Google Scholar 

  • Leavitt SD, Kraichak E, Nelsen MP, Altermann S, Divakar PK, Alors D, Esslinger TL, Crespo A, Lumbsch HT (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). Mol Ecol 24:3779–3797

    PubMed  Google Scholar 

  • Leavitt SD, Grewe F, Widhelm T, Muggia L, Wray B, Lumbsch HT (2016) Resolving evolutionary relationships in lichen-forming fungi using diverse phylogenomic datasets and analytical approaches. Sci Rep 6:22262

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leavitt SD, Keuler R, Newberry CC, Rosentreter R, St Clair LL (2019) Shotgun sequencing decades-old lichen specimens to resolve phylogenomic placement of type material. Plant Fungal Syst 64:237–247

    Google Scholar 

  • Lendemer JC, Keepers KG, Tripp EA, Pogoda CS, McCain CM, Kane NC (2019) A taxonomically broad metagenomic survey of 339 species spanning 57 families suggests cystobasidiomycete yeasts are not ubiquitous across all lichens. Am J Bot 106:1090–1095

    CAS  PubMed  Google Scholar 

  • Lofgren LA, Uehling JK, Branco S, Bruns TD, Martin F, Kennedy PG (2019) Genome-based estimates of fungal rDNA copy number variation across phylogenetic scales and ecological lifestyles. Mol Ecol 28:721–730

    PubMed  Google Scholar 

  • Lu J, Magain N, Miadlikowska J, Coyle JR, Truong C, Lutzoni F (2018) Bioclimatic factors at an intrabiome scale are more limiting than cyanobiont availability for the lichen-forming genus Peltigera. Am J Bot 105:1198–1211

    PubMed  Google Scholar 

  • McDonald D, Clemente JC, Kuczynski J, Rideout JR, Stombaugh J, Wendel D, Wilke A, Huse S, Hufnagle J, Meyer F, Knight R, Caporaso JG (2012) The biological observation matrix (BIOM) format or: how I learned to stop worrying and love the ome-ome. Gigascience 1:7

    PubMed  PubMed Central  Google Scholar 

  • McKinney W (2010) Data structures for statistical computing in Python

  • Millanes AM, Diederich P, Wedin M (2016) Cyphobasidium gen nov, a new lichen-inhabiting lineage in the Cystobasidiomycetes (Pucciniomycotina, Basidiomycota, Fungi). Fungal Biol 120:1468–1477

    PubMed  Google Scholar 

  • Moya P, Molins A, Martínez-Alberola F, Muggia L, Barreno E (2017) Unexpected associated microalgal diversity in the lichen Ramalina farinacea is uncovered by pyrosequencing analyses. PLoS One 12:e0175091

    PubMed  PubMed Central  Google Scholar 

  • Muggia L, Grube M (2018) Fungal diversity in lichens: from extremotolerance to interactions with algae. Life 8:15

    PubMed Central  Google Scholar 

  • Muggia L, Vancurova L, Škaloud P, Peksa O, Wedin M, Grube M (2013) The symbiotic playground of lichen thalli – a highly flexible photobiont association in rock-inhabiting lichens. FEMS Microbiol Ecol 85:313–323

    CAS  PubMed  Google Scholar 

  • Muggia L, Pérez-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

    PubMed  PubMed Central  Google Scholar 

  • Muggia L, Nelsen MP, Kirika PM, Barreno E, Beck A, Lindgren H, Lumbsch HT, Leavitt SD, Trebouxia working group (2020) Formally described species woefully underrepresent phylogenetic diversity in the common lichen photobiont genus Trebouxia (Trebouxiophyceae, Chlorophyta): An impetus for developing an integrated taxonomy. Mol Phylogenet Evol 106821. https://doi.org/10.1016/j.ympev.2020.106821

  • Muggia L, Fleischhacker A, Kopun T, Grube M (2016) Extremotolerant fungi from alpine rock lichens and their phylogenetic relationships. Fungal Divers 76:119–142

    PubMed  Google Scholar 

  • Nilsson RH, Larsson K-H, 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

    CAS  PubMed  Google Scholar 

  • 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 8:8624

    PubMed  PubMed Central  Google Scholar 

  • Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B, Grisel O, Blondel M, Prettenhofer P, Weiss R, Dubourg V, Vanderplas J, Passos A, Cournapeau D, Brucher M, Perrot M, Duchesnay É (2011) Scikit-learn: machine learning in Python. J Mach Learn Res 12:2825–2830

    Google Scholar 

  • Petrini O, Hake U, Dreyfuss MM (1990) An analysis of fungal communities isolated from fruticose lichens. Mycologia 82:444–451

    Google Scholar 

  • Pizarro D (2019) Metagenomic sequencing with new bioinformatics approaches to understand the evolution of lichen forming fungi (dissertation). Complutense University of Madrid Complutense University of Madrid, Madrid

    Google Scholar 

  • R Core Team (2019) The R project for statistical computing. http://www.r-project.org/

  • Rognes T, Flouri T, Nichols B, Quince C, Mahe F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584

    PubMed  PubMed Central  Google Scholar 

  • Schoch CL, Seifert KA, Huhndorf S et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci 109:6241–6246. https://doi.org/10.1073/pnas1117018109

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Singh G, Dal Grande F, Schnitzler J, Pfenninger M, Schmitt I (2018) Different diversification histories in tropical and temperate lineages in the ascomycete subfamily Protoparmelioideae (Parmeliaceae). Mycokeys 36:1–19

    Google Scholar 

  • Škaloud P, Moya P, Molins A, Peksa O, Santos-Guerra A, Barreno E (2018) Untangling the hidden intrathalline microalgal diversity in Parmotrema pseudotinctorum: Trebouxia crespoana sp nov. Lichenologist 50:357–369

    Google Scholar 

  • Spribille T, Tuovinen V, Resl P, Vanderpool D, Wolinski H, Aime MC, Schneider K, Stabentheiner E, Toome-Heller M, Thor G, Mayrhofer H, Johannesson H, McCutcheon JP (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353:488–492

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spribille T, Tagirdzhanova G, Goyette S, Tuovinen V, Case R, Zandberg WF (2020) 3D biofilms: in search of the polysaccharides holding together lichen symbioses. FEMS Microbiol Lett 367:fnaa023.a

    Google Scholar 

  • Steinova J, Skaloud P, Yahr R, Bestova H, Muggi L (2019) Reproductive and dispersal strategies shape the diversity of mycobiont-photobiont association in Cladonia lichens. Mol Phylogenet Evol 134:226–237

    PubMed  Google Scholar 

  • Tuovinen V, Ekman S, Thor G, Vanderpool D, Spribille T, Johannesson H (2019) Two basidiomycete fungi in the cortex of wolf lichens. Curr Biol 29:476–483e475

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Velmala S, Myllys L, Halonen P, Goward T, Ahti T (2009) Molecular data show that Bryoria fremontii and B tortuosa ( Parmeliaceae) are conspecific. Lichenologist 41:231–242

    Google Scholar 

  • Wang Y, Zheng Y, Wang X, Wei X, Wei J (2016) Lichen-associated fungal community in Hypogymnia hypotrypa (Parmeliaceae, Ascomycota) affected by geographic distribution and altitude. Front Microbiol 7:1231

    PubMed  PubMed Central  Google Scholar 

  • Werth S, Sork VL (2014) Ecological specialization in Trebouxia (Trebouxiophyceae) photobionts of Ramalina menziesii (Ramalinaceae) across six range-covering ecoregions of western North America. Am J Bot 101:1127–1140

    PubMed  Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Google Scholar 

  • Wickham H, Averick M, Bryan J, Chang W, McGowan L, François R, Grolemund G, Hayes A, Henry L, Hester J (2019) Welcome to the Tidyverse. J Open Source Software 4:1686

    Google Scholar 

  • Yu NH, Park SY, Kim JA, Park CH, Jeong MH, Oh SO, Hong SG, Talavera M, Divakar PK, Hur JS (2018) Endophytic and endolichenic fungal diversity in maritime Antarctica based on cultured material and their evolutionary position among Dikarya. Fungal Syst Evol 2:263–272

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 5:14850

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We dedicate this publication to our friend and colleague, Dr. Eva Barreno. We gratefully acknowledge the fruitful discussions with Toby Spribille, Diane Haughland, Curtis Björk, and Trevor Goward. We gratefully acknowledge valuable feedback from anonymous reviewers and the editor that greatly improved this study. This research was supported by College of Life Sciences at Brigham Young University, Provo, Utah, USA. We thank Ed Wilcox, DNA Sequencing Center, Brigham Young University, Provo, Utah, USA, for help with sequencing. We also express appreciation to Gretchen Baker for organizing a lichen BioBlitz in Great Basin National Park, Nevada, USA that resulted in a number of collections used in this study (NPS Scientific Collecting and Research Permit number GRBA-2017-SCI-0012).

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Correspondence to Steven D. Leavitt.

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Smith, H.B., Dal Grande, F., Muggia, L. et al. Metagenomic data reveal diverse fungal and algal communities associated with the lichen symbiosis. Symbiosis 82, 133–147 (2020). https://doi.org/10.1007/s13199-020-00699-4

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Keywords

  • Cystobasidiomycetes
  • Endolichenic fungi
  • Genomics
  • Holobiont
  • ITS
  • Symbiosis