A Glimpse into Genetic Diversity and Symbiont Interaction Patterns in Lichen Communities from Areas with Different Disturbance Histories in Białowieża Forest, Poland
Tóm tắt
Anthropogenic disturbances can have strong impacts on lichen communities, as well as on individual species of lichenized fungi. Traditionally, lichen monitoring studies are based on the presence and abundance of fungal morphospecies. However, the photobionts, as well photobiont mycobiont interactions also contribute to the structure, composition, and resilience of lichen communities. Here we assess the genetic diversity and interaction patterns of algal and fungal partners in lichen communities along an anthropogenic disturbance gradient in Białowieża Forest (Poland). We sampled a total of 224 lichen thalli in a protected, a managed, and a disturbed area of the forest, and sequenced internal transcribed spacer (ITS) ribosomal DNA (rDNA) of both, fungal and algal partners. Sequence clustering using a 97% similarity threshold resulted in 46 fungal and 23 green algal operational taxonomic units (OTUs). Most of the recovered photobiont OTUs (14 out of 23) had no similar hit in the NCBI-BLAST search, suggesting that even in well studied regions, such as central Europe, a lot of photobiont diversity is yet undiscovered. If a mycobiont was present at more than one site, it was typically associated with the same photobiont OTU(s). Generalist species, i.e., taxa that associate with multiple symbiont partners, occurred in all three disturbance regimes, suggesting that such taxa have few limitations in colonizing or persisting in disturbed areas. Trebouxia jamesii associated with 53% of the fungal OTUs, and was generally the most common photobiont OTU in all areas, implying that lichens that associate with this symbiont are not limited by the availability of compatible photobionts in Central European forests, regardless of land use intensity.
Từ khóa
Tài liệu tham khảo
Izquierdo, 2010, Effects of forest management on epiphytic lichen diversity in Mediterranean forests, Appl. Veg. Sci., 13, 183, 10.1111/j.1654-109X.2009.01060.x
Ardelean, I.V., Keller, C., and Scheidegger, C. (2015). Effects of management on lichen species richness, ecological traits and community structure in the Rodnei mountains national park (Romania). PLoS ONE, 10.
Ellis, 2006, Contrasting functional traits maintain lichen epiphyte diversity in response to climate and autogenic succession, J. Biogeogr., 33, 1643, 10.1111/j.1365-2699.2006.01522.x
Boch, S., Prati, D., Hessenmöller, D., Schulze, E.-D., and Fischer, M. (2013). Richness of lichen species, especially of threatened ones, is promoted by management methods furthering stand continuity. PLoS ONE, 8.
Giordani, 2012, Functional traits of epiphytic lichens as potential indicators of environmental conditions in forest ecosystems, Ecol. Indic., 18, 413, 10.1016/j.ecolind.2011.12.006
Zedda, 2002, The epiphytic lichens on Quercus in Sardinia (Italy) and their value as ecological indicators, Englera, 24, 5
Jovan, 2008, Lichen Bioindication of Biodiversity, Air Quality, and Climate: Baseline Results From Monitoring in Washington, Oregon, and California, For. Sci., 115, 737
Rico, 2006, Lichen diversity from Cazorla, Segura and Las Villas Biosphere Reserve (SE Spain), Nov. Hedwigia, 82, 31, 10.1127/0029-5035/2006/0082-0031
Nascimbene, 2007, Influence of forest management on epiphytic lichens in a temperate beech forest of northern Italy, For. Ecol. Manage., 247, 43, 10.1016/j.foreco.2007.04.011
Kukwa, 2018, Changes in the epiphytic lichen biota of Białowieża Primeval Forest are not explained by climate warming, Sci. Total Environ., 643, 468, 10.1016/j.scitotenv.2018.06.222
Peksa, 2011, Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae), Mol. Ecol., 20, 3936, 10.1111/j.1365-294X.2011.05168.x
Yahr, 2006, Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis, New Phytol., 171, 847, 10.1111/j.1469-8137.2006.01792.x
Beck, 2012, Photobiont selectivity and specificity in Caloplaca species in a fog-induced community in the Atacama Desert, northern Chile, Fungal Biol., 116, 665, 10.1016/j.funbio.2012.04.001
Rolshausen, 2018, Environment and host identity structure communities of green algal symbionts in lichens, New Phytol., 217, 277, 10.1111/nph.14770
Rolshausen, 2018, Quantifying the climatic niche of symbiont partners in a lichen symbiosis indicates mutualist-mediated niche expansions, Ecography (Cop.)., 41, 1380, 10.1111/ecog.03457
Domaschke, 2011, Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata, Mol. Ecol., 20, 1208, 10.1111/j.1365-294X.2010.04993.x
Kalwij, 2005, Effects of stand-level disturbances on the spatial distribution of a lichen indicator, Ecol. Appl., 15, 2015, 10.1890/04-1912
Singh, 2015, Long-term consequences of disturbances on reproductive strategies of the rare epiphytic lichen Lobaria pulmonaria: Clonality a gift and a curse, FEMS Microbiol. Ecol., 91, 1, 10.1093/femsec/fiu009
Leavitt, 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, 10.1111/mec.13271
Lumbsch, 2011, Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi, Fungal Divers., 50, 59, 10.1007/s13225-011-0123-z
Taylor, 2000, Phylogenetic species recognition and species concepts in fungi, Fungal Genet. Biol., 31, 21, 10.1006/fgbi.2000.1228
Grube, 2000, Molecular approaches and the concept of species and species complexes in lichenized fungi, Mycol. Res., 104, 1284, 10.1017/S0953756200003476
Friedl, 2016, Taxonomic revision and species delimitation of coccoid green algae currently assigned to the genus Dictyochloropsis (Trebouxiophyceae, Chlorophyta), J. Phycol., 52, 599, 10.1111/jpy.12422
Lumbsch, 2014, Integrating coalescent and phylogenetic approaches to delimit species in the lichen photobiont Trebouxia, Mol. Phylogenet. Evol., 76, 202, 10.1016/j.ympev.2014.03.020
Kelly, 2011, DNA barcoding of lichenized fungi demonstrates high identification success in a floristic context, New Phytol., 191, 288, 10.1111/j.1469-8137.2011.03677.x
Schoch, 2012, Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi, Proc. Natl. Acad. Sci. USA, 109, 6241, 10.1073/pnas.1117018109
Gardes, 1993, ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts, Mol. Ecol., 2, 113, 10.1111/j.1365-294X.1993.tb00005.x
Leliaert, 2014, DNA-based species delimitation in algae, Eur. J. Phycol., 49, 179, 10.1080/09670262.2014.904524
2006, The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii, New Phytol., 169, 331, 10.1111/j.1469-8137.2005.01576.x
Kroken, 2000, Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia, Bryologist, 103, 645, 10.1639/0007-2745(2000)103[0645:PSRMAS]2.0.CO;2
Romeike, 2002, Genetic diversity of algal and fungal partners in four species of Umbilicaria (Lichenized Ascomycetes) along a transect of the Antarctic peninsula, Mol. Biol. Evol., 19, 1209, 10.1093/oxfordjournals.molbev.a004181
Skaloud, 2010, Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta), Mol. Phylogenet. Evol., 54, 36, 10.1016/j.ympev.2009.09.035
Muggia, 2011, Photobiont association and genetic diversity of the optionally lichenized fungus Schizoxylon albescens, FEMS Microbiol. Ecol., 75, 255, 10.1111/j.1574-6941.2010.01002.x
Rikkinen, 2013, Molecular studies on cyanobacterial diversity in lichen symbioses, MycoKeys, 6, 3, 10.3897/mycokeys.6.3869
Leavitt, 2013, Multilocus phylogeny of the lichen-forming fungal genus Melanohalea (Parmeliaceae, Ascomycota): Insights on diversity, distributions, and a comparison of species tree and concatenated topologies, Mol. Phylogenet. Evol., 66, 138, 10.1016/j.ympev.2012.09.013
Linskens, H.F., and Heslop-Harrison, J. (1984). Physiological interactions between the partners of the lichen symbiosis. Cellular Interactions, Springer.
Beck, 1998, Selectivity of photobiont choice in a defined lichen community: Inferences from cultural and molecular studies, New Phytol., 139, 709, 10.1046/j.1469-8137.1998.00231.x
Yahr, 2004, Strong fungal specifity and selectivity for algal symbionts in Florida scrub Cladonia lichens, Mol. Ecol., 13, 3367, 10.1111/j.1365-294X.2004.02350.x
Beck, 2014, Molecular phylogeny and symbiotic selectivity of the green algal genus Dictyochloropsis s.l. (Trebouxiophyceae): A polyphyletic and widespread group forming photobiont-mediated guilds in the lichen family Lobariaceae, New Phytol., 202, 455, 10.1111/nph.12678
Singh, 2017, Fungal–algal association patterns in lichen symbiosis linked to macroclimate, New Phytol., 214, 317, 10.1111/nph.14366
Kaasalainen, 2019, Relationships between mycobiont identity, photobiont specificity and ecological preferences in the lichen genus Peltigera (Ascomycota) in Estonia (northeastern Europe), Fungal Ecol., 39, 45, 10.1016/j.funeco.2018.11.005
Sabatini, 2018, Where are Europe’s last primary forests?, Divers. Distrib., 24, 1426, 10.1111/ddi.12778
Kranner, I., Beckett, R., and Varma, A. (2002). Isolation of nucleic acids from lichens. Protocols in Lichenology, Springer.
Innis, M., Gelfand, H., Sninsky, J., and White, T. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications, Academic Press.
Hametner, 2014, New insights into diversity and selectivity of trentepohlialean lichen photobionts from the extratropics, Symbiosis, 63, 31, 10.1007/s13199-014-0285-z
Drummond, A.J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., and Markowitz, S. (2019, April 11). Geneious. Available online: https://www.geneious.com/.
Rognes, 2016, VSEARCH: A versatile open source tool for metagenomics, PeerJ, 4, e2584, 10.7717/peerj.2584
MOYA, 2018, Untangling the hidden intrathalline microalgal diversity in Parmotrema pseudotinctorum: Trebouxia crespoana sp. nov, Lichenologist, 50, 357, 10.1017/S0024282918000208
Paradis, 2004, APE: Analyses of Phylogenetics and Evolution in R language, Bioinformatics, 20, 289, 10.1093/bioinformatics/btg412
R Core Team (2017). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing.
Giraud, 2007, When can host shifts produce congruent host and parasite phylogenies? A simulation approach, J. Evol. Biol., 20, 1428, 10.1111/j.1420-9101.2007.01340.x
Rambold, 1992, The Inter-lecanoralean Associations, Bibl. Lichenol., 48, 58027
Nyati, 2014, Green-algal photobiont diversity (Trebouxia spp.) in representatives of Teloschistaceae (Lecanoromycetes, lichen-forming ascomycetes), Lichenol., 46, 189, 10.1017/S0024282913000819
Ericson, 2000, Epiphytic macrolichens as conservation indicators: Successional sequence in Populus tremula stands, Biol. Conserv., 93, 43, 10.1016/S0006-3207(99)00113-5
Ranius, 2008, The influence of tree age and microhabitat quality on the occurrence of crustose lichens associated with old oaks, J. Veg. Sci., 19, 653, 10.3170/2008-8-18433
Fritz, 2009, Tree age is a key factor for the conservation of epiphytic lichens and bryophytes in beech forests, Appl. Veg. Sci., 12, 93, 10.1111/j.1654-109X.2009.01007.x
McCune, 1993, Gradients in epiphyte biomass in three Pseudotsuga-Tsuga forests of different ages in Western Oregon and Washington, Bryologist, 96, 405, 10.2307/3243870
Rambo, T.B., Harris, R.H., Larson, B.W., Majors, S., Peterson, E.T., Widmer, M., Shaw, D.C., Rosso, A., Proctor, J., and Camacho, F.J. (2019, June 24). Vertical Profile of Epiphytes in a Pacific Northwest Old-growth Forest. Available online: https://www.semanticscholar.org/paper/Vertical-Profile-of-Epiphytes-in-a-Pacific-Forest-Rambo-Harris/a29a6936685890d2fdb33ad87f92ad63a8598120.
Felton, 2017, Varying rotation lengths in northern production forests: Implications for habitats provided by retention and production trees, Ambio, 46, 324, 10.1007/s13280-017-0909-7
Fedrowitz, 2014, REVIEW: Can retention forestry help conserve biodiversity? A meta-analysis, J. Appl. Ecol., 51, 1669, 10.1111/1365-2664.12289
Gustafsson, 2012, Retention Forestry to Maintain Multifunctional Forests: A World Perspective, Bioscience, 62, 633, 10.1525/bio.2012.62.7.6
Gustafsson, 2010, Tree retention as a conservation measure in clear-cut forests of northern Europe: A review of ecological consequences, Scand. J. For. Res., 25, 295, 10.1080/02827581.2010.497495
2010, Epiphyte communities on the trunks of retention trees stabilise in 5 years after timber harvesting, but remain threatened due to tree loss, Biol. Conserv., 143, 891, 10.1016/j.biocon.2009.12.036
Jonsson, 2013, Lichen species richness on retained aspens increases with time since clear-cutting, For. Ecol. Manage., 293, 49, 10.1016/j.foreco.2012.12.027
2007, Conservation of epiphytic lichens: Significance of remnant aspen (Populus tremula) trees in clear-cuts, Biol. Conserv., 135, 388, 10.1016/j.biocon.2006.10.011
Rikkinen, 2002, Lichen guilds share related cyanobacterial symbionts, Science, 297, 357, 10.1126/science.1072961
Gjerde, 2012, Community assembly in epiphytic lichens in early stages of colonization, Ecology, 93, 749, 10.1890/11-1018.1
Sanders, 2002, Reproductive strategies, relichenization and thallus development observed in situ in leaf-dwelling lichen communities, New Phytol., 155, 425, 10.1046/j.1469-8137.2002.00472.x
Insarova, 2016, Lichen symbiosis: Search and recognition of partners, Biol. Bull., 43, 408, 10.1134/S1062359016040038
Goldmann, 2015, Forest management type influences diversity and community composition of soil fungi across temperate forest ecosystems, Front. Microbiol., 6, 1300, 10.3389/fmicb.2015.01300
Spake, 2015, A meta-analysis of functional group responses to forest recovery outside of the tropics, Conserv. Biol., 29, 1695, 10.1111/cobi.12548
Thompson, 2018, Effects of secondary forest succession on amphibians and reptiles: A review and meta-analysis, Copeia, 106, 10, 10.1643/CH-17-654