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Exploring the natural microbiome of the model liverwort: fungal endophyte diversity in Marchantia polymorpha L

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Abstract

Within their tissues, plants host diverse communities of fungi, termed fungal endophytes. These fungi can affect plant growth, competitiveness, and resistance to stressors, thereby influencing plant community structure. Research characterizing fungal endophyte communities has so far mostly focused on seed plants, but information on the endophytes of other plant lineages is needed to understand how plant microbiomes impact whole ecosystems and how major changes through land plant evolution have affected plant-microbe relationships. In this study, we assess the fungal endophyte community of the model liverwort Marchantia polymorpha L. by both culturing and Illumina amplicon sequencing methods. We detect a very diverse fungal community that is distinct between M. polymorpha patches and only shares a few core fungi between populations across the United States. We also show low overlap in taxa detected by the different methods. This study helps build a foundation for using M. polymorpha and other Marchantia species as models for the ecology and dynamics of bryophyte microbiomes.

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References

  • Abarenkov K, Henrik Nilsson R, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungi–recent updates and future perspectives. New Phytol 186:281–285

    Article  PubMed  Google Scholar 

  • Afkhami ME, Strauss SY (2016) Native fungal endophytes suppress an exotic dominant and increase plant diversity over small and large spatial scales. Ecology 97:1159–1169

    Article  PubMed  Google Scholar 

  • Aguilar-Trigueros CA, Rillig MC (2016) Effect of different root endophytic fungi on plant community structure in experimental microcosms. Ecol Evol 6:8149–8158

    Article  PubMed  PubMed Central  Google Scholar 

  • Akita M, Lehtonen MT, Koponen H, Marttinen EM, Valkonen JPT (2011) Infection of the Sunagoke moss panels with fungal pathogens hampers sustainable greening in urban environments. Sci Total Environ 409(17):3166–3173

    Article  CAS  PubMed  Google Scholar 

  • Alcaraz LD, Peimbert M, Barajas HR, Dorantes-Acosta AE, Bowman JL, Arteaga-Vázquez MA (2018) Marchantia liverworts as a proxy to plants’ basal microbiomes. Sci Rep 8:12712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnold AE (2002) Neotropical fungal endophytes: diversity and ecology. Dissertation, The University of Arizona

  • Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66

    Article  Google Scholar 

  • Arnold AE, Maynard Z, Gilbert GS (2001) Fungal endophytes in dicotyledonous neotropical trees: patterns of abundance and diversity. Mycol Res 105:1502–1507

    Article  Google Scholar 

  • Berg G, Rybakova D, Grube M, Köberl M (2015) The plant microbiome explored: implications for experimental botany. J Exp Bot 67:995–1002

    Article  CAS  PubMed  Google Scholar 

  • Bischler-Causse H, Boisselier-Dubayle M (1991) Lectotypification of Marchantia polymorpha L. J Bryol 16:361–365

    Article  Google Scholar 

  • Boisselier-Dubayle MC, Jubier MF, Lejeune B, Bischler H (1995) Genetic variability in the three subspecies of Marchantia polymorpha (Hepaticae): isozymes, RFLP and RAPD markers. Taxon 44(3):363

    Article  Google Scholar 

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

  • Bowman JL, Araki T, Kohchi T (2016) Marchantia: past, present and future. Plant Cell Physiol 57:205–209

    Article  CAS  PubMed  Google Scholar 

  • Bowman JL et al (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:287–304

    Article  CAS  PubMed  Google Scholar 

  • Bradbury S (2006) Response of the post-fire bryophyte community to salvage logging in boreal mixedwood forests of northeastern Alberta, Canada. For Ecol Manag 234:313–322

    Article  Google Scholar 

  • Bresinsky A, Schotz A (2006) Behaviour in cultures and habitat requirements of species within the genera Loreleia and Rickenella (Agaricales). Acta Mycol 41:189–208

  • Bunyard BA, Nicholson MS, Royse DJ (1994) A systematic assessment of Morchella using RFLP analysis of the 28S ribosomal RNA gene. Mycologia 86:762–772

    Article  CAS  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carbone I et al (2016) T-BAS: tree-based alignment selector toolkit for phylogenetic-based placement, alignment downloads and metadata visualization: an example with the Pezizomycotina tree of life. Bioinformatics 33:1160–1168

    Google Scholar 

  • Chen KH, Liao HL, Arnold AE, Bonito G, Lutzoni F (2018) RNA-based analyses reveal fungal communities structured by a senescence gradient in the moss Dicranum scoparium and the presence of putative multi-trophic fungi. New Phytol 218:1597–1611

    Article  CAS  PubMed  Google Scholar 

  • Cordier T, Robin C, Capdevielle X, Fabreguettes O, Desprez-Loustau ML, Vacher C (2012) The composition of phyllosphere fungal assemblages of European beech (Fagus sylvatica) varies significantly along an elevation gradient. New Phytol 196:510–519

    Article  PubMed  Google Scholar 

  • Davey ML, Currah RS (2006) Interactions between mosses (Bryophyta) and fungi. Can J Bot 84(10):1509–1519

    Article  Google Scholar 

  • Davey ML, Currah RS (2009) Atradidymella muscivora gen. Et sp. nov.(Pleosporales) and its anamorph Phoma muscivora sp. nov.: a new pleomorphic pathogen of boreal bryophytes. Am J Bot 96:1281–1288

    Article  PubMed  Google Scholar 

  • Davey ML, Tsuneda A, Currah RS (2009) Pathogenesis of bryophyte hosts by the ascomycete. Atradidymella muscivora. Am J Bot 96:1274–1280

    Article  PubMed  Google Scholar 

  • Davey ML, Heegaard E, Halvorsen R, Ohlson M, Kauserud H (2012) Seasonal trends in the biomass and structure of bryophyte-associated fungal communities explored by 454 pyrosequencing. New Phytol 195:844–856

    Article  CAS  PubMed  Google Scholar 

  • Davey ML, Heegaard E, Halvorsen R, Kauserud H, Ohlson M (2013) Amplicon-pyrosequencing-based detection of compositional shifts in bryophyte-associated fungal communities along an elevation gradient. Mol Ecol 22:368–383

    Article  CAS  PubMed  Google Scholar 

  • Davey ML, Kauserud H, Ohlson M (2014) Forestry impacts on the hidden fungal biodiversity associated with bryophytes. FEMS Microbiol Ecol 90:313–325

    Article  CAS  PubMed  Google Scholar 

  • Davey ML, Skogen MJ, Heegaard E, Halvorsen R, Kauserud H, Ohlson M (2017) Host and tissue variations overshadow the response of boreal moss-associated fungal communities to increased nitrogen load. Mol Ecol 26:571–588

    Article  CAS  PubMed  Google Scholar 

  • Davis EC, Shaw AJ (2008) Biogeographic and phylogenetic patterns in diversity of liverwort-associated endophytes. Am J Bot 95:914–924

    Article  PubMed  Google Scholar 

  • Davis EC, Franklin JB, Shaw AJ, Vilgalys R (2003) Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: phylogenetics, distribution, and symbiosis. Am J Bot 90:1661–1667

    Article  PubMed  Google Scholar 

  • Delaux P-M, Nanda AK, Mathé C, Sejalon-Delmas N, Dunand C (2012) Molecular and biochemical aspects of plant terrestrialization. Perspect Plant Ecol Evol Syst 14:49–59

    Article  Google Scholar 

  • Desirò A, Duckett JG, Pressel S, Villarreal JC, Bidartondo MI (2013) Fungal symbioses in hornworts: a chequered history. Proc R Soc Lond B Biol Sci 280:20130207

    Article  CAS  Google Scholar 

  • Döbbeler P (1997) Biodiversity of bryophilous ascomycetes. Biodivers Conserv 6:721–738

    Article  Google Scholar 

  • Egertová Z, Eckstein J, Vega M (2015) Lamprospora tuberculata, Octospora ithacaensis, O. orthotrichi and O. affinis–four bryoparasitic ascomycetes new to the Czech Republic. Czech Mycol 67

  • Field KJ, Cameron DD, Leake JR, Tille S, Bidartondo MI, Beerling DJ (2012) Contrasting arbuscular mycorrhizal responses of vascular and non-vascular plants to a simulated. Palaeozoic CO2 decline. Nat Commun 3:835

    Article  CAS  PubMed  Google Scholar 

  • Field KJ, Rimington WR, Bidartondo MI, Allinson KE, Beerling DJ, Cameron DD, Duckett JG, Leake JR, Pressel S (2016) Functional analysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline. ISME J 10:1514–1526

    Article  CAS  PubMed  Google Scholar 

  • Garcia G, Van Vooren N (2005) Un discomycète inoperculé plutôt discret, Pezoloma ciliifera, et remarques sur le genre Pezoloma. Publications de la Société Linnéenne de Lyon 74:115–130

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Glime JM (2013a) Protozoa diversity. In: Bryophyte ecology volume 2: byological interaction

  • Glime JM (2013b) Invertebrates: nematodes. In: Bryophyte ecology volume 2: bryological interaction

  • Glime JM (2017) The fauna: a place to call home. In: Bryophyte ecology volume 2: bryological interaction

  • Glynou K, Ali T, Buch AK, Haghi Kia S, Ploch S, Xia X, Çelik A, Thines M, Maciá-Vicente JG (2016) The local environment determines the assembly of root endophytic fungi at a continental scale. Environ Microbiol 18:2418–2434

    Article  CAS  PubMed  Google Scholar 

  • Graff PW (1936) Invasion by Marchantia polymorpha following forest fires. Bull Torrey Bot Club 63:67–74

    Article  Google Scholar 

  • Guminska B, Mierzenska M (1992) Gerronema marchantiae Sing et Clem-a fungus associating with Marchantia polymorpha L and Nostoc sp Zeszyty Naukowe Uniwersytetu Jagiellońskiego Prace Botaniczne 24:171–177

  • Hamayun M, Khan SA, Khan AL, Rehman G, Sohn EY, Shah AA, Kim SK, Joo GJ, Lee IJ (2009) Phoma herbarum as a new gibberellin-producing and plant growth-promoting fungus. J Microbiol Biotechnol 19:1244–1249

    CAS  PubMed  Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    Article  CAS  PubMed  Google Scholar 

  • Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133

    Article  CAS  PubMed  Google Scholar 

  • Hipol R, Tamang SMA, Gargabite BF, Broñola Hipol R (2015) Diversity of fungal endophytes isolated from Marchantia polymorpha populations from Baguio City, Philippines bulletin of environment, Pharmacology and Life Sciences 4:87–91

  • Hoshina R, Kusuoka Y (2016) DNA analysis of algal endosymbionts of ciliates reveals the state of algal integration and the surprising specificity of the symbiosis. Protist 167:174–184

    Article  CAS  PubMed  Google Scholar 

  • Humphreys CP, Franks PJ, Rees M, Bidartondo MI, Leake JR, Beerling DJ (2010) Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nat Commun 1:103

    Article  CAS  PubMed  Google Scholar 

  • Innis MA, Gelfand DH, Sninsky JJ, White TJ (2012) PCR protocols: a guide to methods and applications. Academic Press, London

    Google Scholar 

  • Junker C, Draeger S, Schulz B (2012) A fine line–endophytes or pathogens in Arabidopsis thaliana. Fungal Ecol 5:657–662

    Article  Google Scholar 

  • Kivlin SN, Lynn JS, Kazenel MR, Beals KK, Rudgers JA (2017) Biogeography of plant-associated fungal symbionts in mountain ecosystems: a meta-analysis. Divers Distrib 23:1067–1077

    Article  Google Scholar 

  • Knack J et al (2015) Microbiomes of streptophyte algae and bryophytes suggest that a functional suite of microbiota fostered plant colonization of land. Int J Plant Sci 176:405–420

    Article  Google Scholar 

  • Kowal J, Pressel S, Duckett JG, Bidartondo MI (2016) Liverworts to the rescue: an investigation of their efficacy as mycorrhizal inoculum for vascular plants. Funct Ecol 30:1014–1023

    Article  Google Scholar 

  • Kowal J, Pressel S, Duckett JG, Bidartondo MI, Field KJ (2018) From rhizoids to roots? Experimental evidence of mutualism between liverworts and ascomycete fungi. Ann Bot 121:221–227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ligrone R, Carafa A, Lumini E, Bianciotto V, Bonfante P, Duckett JG (2007) Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis. Am J Bot 94:1756–1777

    Article  CAS  PubMed  Google Scholar 

  • Lundberg DS, Yourstone S, Mieczkowski P, Jones CD, Dangl JL (2013) Practical innovations for high-throughput amplicon sequencing. Nat Methods 10:999–1002

    Article  CAS  PubMed  Google Scholar 

  • Marks RA, Smith JJ, Cronk Q, McLetchie DN (2018) Variation in the bacteriome of the tropical liverwort, Marchantia inflexa, between the sexes and across habitats. Symbiosis 75:93–101

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12

    Article  Google Scholar 

  • Nelson JM (2017) Diversity and effects of the fungal endophytes of the liverwort Marchantia polymorpha. Dissertation. Duke University

  • Nelson JM, Hauser DA, Hinson R, Shaw AJ (2018) A novel experimental system using the liverwort Marchantia polymorpha and its fungal endophytes reveals diverse and context-dependent effects. New Phytol 218:1217–1232

    Article  CAS  PubMed  Google Scholar 

  • Nguyen NH, Smith D, Peay K, Kennedy P (2015) Parsing ecological signal from noise in next generation amplicon sequencing. New Phytol 205:1389–1393

    Article  CAS  PubMed  Google Scholar 

  • Oksanen, J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MH (2017) vegan: Community Ecology Package. R package version 2.4–3

  • Peay KG, Kennedy PG, Talbot JM (2016) Dimensions of biodiversity in the earth mycobiome. Nat Rev Microbiol 14:434–447

    Article  CAS  PubMed  Google Scholar 

  • Peršoh D (2015) Plant-associated fungal communities in the light of meta’omics. Fungal Divers 75:1–25

    Article  Google Scholar 

  • Ploch S, Rose LE, Bass D, Bonkowski M (2016) High diversity revealed in leaf-associated protists (Rhizaria: Cercozoa) of Brassicaceae. J Eukaryot Microbiol 63:635–641

    Article  PubMed  PubMed Central  Google Scholar 

  • Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315

    Article  CAS  PubMed  Google Scholar 

  • Pressel S, Bidartondo MI, Ligrone R, Duckett JG (2010) Fungal symbioses in bryophytes: new insights in the twenty first century. Phytotaxa 9:238–253

    Article  Google Scholar 

  • Radhakrishnan G (2017) Tracing the evolution of the arbuscular mycorrhizal symbiosis in the plant lineage. Doctoral dissertation, University of East Anglia

  • Reese WD (1981) " Chlorochytrium," a green alga endophytic in Musci. Bryologist 84:75–78

    Article  Google Scholar 

  • Reese WD (1992) More mosses with Chlorochytrium1. J Phycol 28:707–707

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Ross A, Yasutake W, Leek S (1975) Phoma herbarum, a fungal plant saprophyte, as a fish pathogen. J Fish Res Board Can 32:1648–1652

    Article  Google Scholar 

  • Rudgers JA, Koslow JM, Clay K (2004) Endophytic fungi alter relationships between diversity and ecosystem properties. Ecol Lett 7:42–51

    Article  Google Scholar 

  • Sapp M, Ploch S, Fiore-Donno AM, Bonkowski M, Rose LE (2018) Protists are an integral part of the Arabidopsis thaliana microbiome. Environ Microbiol 20:30–43

    Article  CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  • Shaw J, Renzaglia K (2004) Phylogeny and diversification of bryophytes. Am J Bot 91:1557–1581

    Article  PubMed  Google Scholar 

  • Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O’Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stenroos S, Laukka T, Huhtinen S, Döbbeler P, Myllys L, Syrjänen K, Hyvönen J (2010) Multiple origins of symbioses between ascomycetes and bryophytes suggested by a five-gene phylogeny. Cladistics 26:281–300

    Article  PubMed  Google Scholar 

  • Stone JK, Bacon CW, White J (2000) An overview of endophytic microbes: endophytism defined. Microbial Endophytes 3:29–33

    Google Scholar 

  • Taylor TN, Krings M (2005) Fossil microorganisms and land plants: associations and interactions. Symbiosis 40:119–135

    CAS  Google Scholar 

  • Team RC (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Trémouillaux-Guiller J, Huss VA (2007) A cryptic intracellular green alga in Ginkgo biloba: ribosomal DNA markers reveal worldwide distribution. Planta 226:553–557

    Article  CAS  PubMed  Google Scholar 

  • U’Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot 99:898–914

    Article  PubMed  Google Scholar 

  • Venables WN, Ripley BD (2002) Random and mixed effects. In: Modern applied statistics with S Springer, pp 271–300

  • Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

  • Wickham H (2011) The split-apply-combine strategy for data analysis. J Stat Softw 40:1–29

    Google Scholar 

  • Wu L, Han T, Li W, Jia M, Xue L, Rahman K, Qin L (2013) Geographic and tissue influences on endophytic fungal communities of Taxus chinensis var. mairei in China. Curr Microbiol 66:40–48

    Article  CAS  PubMed  Google Scholar 

  • Yuan Z-L, Chen Y-C, Yang Y (2009) Diverse non-mycorrhizal fungal endophytes inhabiting an epiphytic, medicinal orchid (Dendrobium nobile): estimation and characterization. World J Microbiol Biotechnol 25:295

    Article  Google Scholar 

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Acknowledgements

The authors thank the following for assistance with field work logistics and facilities: G. Hermann and M. Metz (Lewis & Clark College); S. LaGreca and K. Hodge (Cornell University); K. McFarland (University of Tennessee); D. Allard and M. Tierney (University of Vermont); P. Ball (Oregon State University, Cascades); D. Taylor (Daniel Boone National Forest); B. Overton (Lock Haven University); A. DeMarais, M. Morrison, and B. Kirkpatrick (University of Puget Sound); C. Crisafulli (Pacific Northwest Research Station); K. Golinski (Smithsonian Institution); S. Heiney (North Carolina Botanical Garden). We thank R. Vilgalys, F. Lutzoni, F. Dietrich, and P. Manos for their advice on manuscript development. We also thank our undergraduate assistants: K. Atherton, C. Chen, R. Hinson, and S. Ou. Funding for this work was provided by grant no. DEB-1501826, U.S. National Science Foundation, an Anderson & Crum grant from the American Bryological and Lichenological Society, and a Grant in Aid of Research from the Duke University Biology Department.

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  1. Department of Biology, Duke University, Durham, NC, USA

    Jessica Nelson & A. Jonathan Shaw

  2. Boyce Thompson Institute, Ithaca, NY, USA

    Jessica Nelson

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Nelson, J., Shaw, A.J. Exploring the natural microbiome of the model liverwort: fungal endophyte diversity in Marchantia polymorpha L. Symbiosis 78, 45–59 (2019). https://doi.org/10.1007/s13199-019-00597-4

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