Shotgun sequencing decades-old lichen specimens to resolve
phylogenomic placement of type material
| 1 | Department of Biology, Brigham Young University, 4102 Life Science
Building, Provo, UT 84602, USA |
| 2 | M. L. Bean Life Science Museum, Brigham Young University, 4102
Life Science Building, Provo, UT 84602, USA |
| 3 | Biology Department, Boise State University, 1910 West University
Drive, Boise, ID 83725, USA |
Publication date: 2019-12-16
Plant and Fungal Systematics 2019; 64(2): 237–247
KEYWORDS
ABSTRACT
Natural history collections, including name-bearing type specimens, are
an important source of genetic information. These data can be critical for appropriate taxonomic
revisions in cases where the phylogenetic position of name-bearing type specimens
needs to be identified, including morphologically cryptic lichen-forming fungal species.
Here, we use high-throughput metagenomic shotgun sequencing to generate genome-scale
data from decades-old (i.e., more than 30 years old) isotype specimens representing three
vagrant taxa in the lichen-forming fungal genus Rhizoplaca, including one species and
two subspecies. We also use data from high-throughput metagenomic shotgun sequencing
to infer the phylogenetic position of an enigmatic collection, originally identified
as R. haydenii, that failed to yield genetic data via Sanger sequencing. We were able to
construct a 1.64 Mb alignment from over 1200 single-copy nuclear gene regions for the
Rhizoplaca specimens. Phylogenomic reconstructions recovered an isotype representing
Rhizoplaca haydenii subsp. arbuscula within a clade comprising other specimens identified
as Rhizoplaca haydenii subsp. arbuscula, while an isotype of R. idahoensis was recovered
within a clade with substantial phylogenetic substructure comprising Rhizoplaca haydenii
subsp. haydenii and other specimens. Based on these data and morphological differences,
Rhizoplaca haydenii subsp. arbuscula is elevated to specific rank as Rhizoplaca arbuscula.
For the enigmatic collection, we were able to assemble the nearly complete nrDNA cistron
and over 50 Mb of the mitochondrial genome. Using these data, we identified this specimen
as a morphologically deviant form representing Xanthoparmelia aff. subcumberlandia.
This study highlights the power of high-throughput metagenomic shotgun sequencing in
generating larger and more comprehensive genetic data from taxonomically important
herbarium specimens.
REFERENCES (64)
1.
Anco, C., Kolokotronis, S. O., Henschel, P., Cunningham, S. W., Amato, G. & Hekkala, E. 2018. Historical mitochondrial diversity in African leopards (Panthera pardus) revealed by archival museum specimens. Mitochondrial DNA Part A 29: 455–473.
2.
Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S., Prjibelski, A. D., Pyshkin, A. V., Sirotkin, A. V., Vyahhi, N., Tesler, G., Alekseyev, M. A. & Pevzner, P. A. 2012. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology 19: 455–477.
3.
Bertels, F., Silander, O. K., Pachkov, M., Rainey, P. B. & van Nimwegen, E. 2014. Automated reconstruction of whole-genome phylogenies from short-sequence reads. Molecular Biology and Evolution 31: 1077–1088.
4.
Besnard, G., Bertrand, J. A., Delahaie, B., Bourgeois, Y. X., Lhuillier, E. & Thébaud, C. 2015. Valuing museum specimens: high-throughput DNA sequencing on historical collections of New Guinea crowned pigeons (Goura). Biological Journal of the Linnean Society 117: 71–82.
5.
Bolger, A. M., Lohse, M. & Usadel, B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120.
6.
Brandt, J. R., de Groot, P. J. V., Witt, K. E., Engelbrektsson, P. K., Helgen, K. M., Malhi, R. S., Ryder, O. A. & Roca, A. L. 2018. Genetic structure and diversity among historic and modern populations of the Sumatran rhinoceros (Dicerorhinus sumatrensis). Journal of Heredity 109: 553–565.
7.
Brock, P. M., Döring, H. & Bidartondo, M. I. 2009. How to know unknown fungi: the role of a herbarium. New Phytologist 181: 719–724.
8.
Bruns, T. D., Fogel, R. & Taylor, J. W. 1990. Amplification and sequencing of DNA from fungal herbarium specimens. Mycologia 82: 175–184.
9.
Burrell, A. S., Disotell, T. R. & Bergey, C. M. 2015. The use of museum specimens with high-throughput DNA sequencers. Journal of Human Evolution 79: 35–44.
10.
Cappellini, E., Gentry, A., Palkopoulou, E., Ishida, Y., Cram, D., Roos, A. M., Watson, M., Johansson, U. S., Fernholm, B., Agnelli, P., Barbagli, F., Littlewood, D. T. J., Kelstrup, C. D., Olsen, J. V., Lister, A. M., Roca, A. L., Dalen, L. & Gilbert, M. T. P. 2014. Resolution of the type material of the Asian elephant, Elephas maximus Linnaeus, 1758 (Proboscidea, Elephantidae). Zoological Journal of the Linnean Society 170: 222–232.
11.
Chambers, E. A. & Hebert, P. D. N., 2016. Assessing DNA barcodes for species identification in North American reptiles and amphibians in natural history collections. PlosONE 11: e0154363.
12.
Cooper, A. 1994. DNA from Museum Specimens. In: Herrmann, B. & Hummel, S. (eds), Ancient DNA: Recovery and Analysis of Genetic Material from Paleontological, Archaeological, Museum, Medical, and Forensic Specimens, pp. 149–165. Springer New York, New York, NY.
13.
Crespo, A. & Pérez-Ortega, S., 2009. Cryptic species and species pairs in lichens: A discussion on the relationship between molecular phylogenies and morphological characters. Anales del Jardin Botanico de Madrid 66: 71–81.
14.
Funk, V. A., Gostel, M., Devine, A., Kelloff, C. L., Wurdack, K., Tuccinardi, C., Radosavljevic, A., Peters, M. & Coddington, J. 2017. Guidelines for collecting vouchers and tissues intended for genomic work (Smithsonian Institution): Botany Best Practices. Biodiversity Data Journal 5: e11625.
15.
Green, R. E., Krause, J., Ptak, S. E., Briggs, A. W., Ronan, M. T., Simons, J. F., Du, L., Egholm, M., Rothberg, J. M., Paunovic, M. & Pääbo, S. 2006. Analysis of one million base pairs of Neanderthal DNA. Nature 444: 330.
16.
Grewe, F., Huang, J.-P., Leavitt, S. D. & Lumbsch, H. T. 2017. Reference-based RADseq resolves robust relationships among closely related species of lichen-forming fungi using metagenomic DNA. Scientific Reports 7(1): 9884.
17.
Gueidan, C., Aptroot, A., Cáceres, M. E.d.S. & Binh, N. Q. 2015. Molecular phylogeny of the tropical lichen family Pyrenulaceae: contribution from dried herbarium specimens and FTA card samples. Mycological Progress 15: 7.
18.
Hale, M. E. 1990. A synopsis of the lichen genus Xanthoparmelia (Vainio) Hale (Ascomycotina, Parmeliaceae). Smithsonian Institution Press, Washington D.C.
20.
Hawksworth, D. L. 2008. The need for a more effective biological nomenclature for the 21st century. Botanical Journal of the Linnean Society 109: 543–567.
21.
Hawksworth, D. L. 2013. The oldest sequenced fungal specimen. The Lichenologist 45: 131–132.
22.
Heckeberg, N. S., Erpenbeck, D., Worheide, G. & Rossner, G. E. 2016. Systematic relationships of five newly sequenced cervid species. PeerJ 4: e2307.
23.
Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. 2018. UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35: 518–522.
24.
Holmes, M. W., Hammond, T. T., Wogan, G. O., Walsh, R. E., LaBarbera, K., Wommack, E. A., Martins, F. M., Crawford, J. C., Mack, K. L., Bloch, L. M. & Nachman, M. W. 2016. Natural history collections as windows on evolutionary processes. Molecular Ecology 25: 864–881.
25.
Hundsdoerfer, A. K., Packert, M., Kehlmaier, C., Strutzenberger, P. & Kitching, I. J. 2017. Museum archives revisited: Central Asiatic hawkmoths reveal exceptionally high late Pliocene species diversification (Lepidoptera, Sphingidae). Zoologica Scripta 46: 552–570.
26.
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K., von Haeseler, A. & Jermiin, L. S. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587.
27.
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.
28.
Keuler, R. A., Garretson, A., Saunders, T., Erickson, R., St. Andre, N., Grewe, F., Smith, H., Lumbsch, H., St Clair, L., Leavitt, S. 2019. Genome-scale data reveal the potential role of hybrid speciation in lichen-forming fungi. Botany 2019 – Sky Islands & Desert Seas, Tucson, Arizona, July 27–31. Botanical Society of America. Abstract ID: 190.
29.
Kistenich, S., Halvorsen, R., Schrøder-Nielsen, A., Thorbek, L., Timdal, E. & Bendiksby, M. 2019. DNA sequencing historical lichen specimens. Frontiers in Ecology and Evolution 7: 5.
30.
Lan, T. & Lindqvist, C. 2019. Technical advances and challenges in genome-scale analysis of ancient DNA. In: Lindqvist, C. & Rajora, O. P. (eds), Paleogenomics: Genome-Scale Analysis of Ancient DNA, pp. 3–29. Springer International Publishing, Cham.
31.
Lane, M. A. 1996. Roles of natural history collections. Annals of the Missouri Botanical Garden 83: 536–545.
32.
Langmead, B. & Salzberg, S. L. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9: 357–359.
33.
Leavitt, S. D., Fankhauser, J. D., Leavitt, D. H., Porter, L. D., Johnson, L. A. & St. Clair, L. L. 2011a. Complex patterns of speciation in cosmopolitan “rock posy” lichens – Discovering and delimiting cryptic fungal species in the lichen-forming Rhizoplaca melanophthalma species-complex (Lecanoraceae, Ascomycota). Molecular Phylogenetics and Evolution 59: 587–602.
34.
Leavitt, S. D., Johnson, L. A., Goward, T. & St. Clair, L. L. 2011b. Species delimitation in taxonomically difficult lichen-forming fungi: An example from morphologically and chemically diverse Xanthoparmelia (Parmeliaceae) in North America. Molecular Phylogenetics and Evolution 60: 317–332.
35.
Leavitt, S. D., Fernández-Mendoza, F., Pérez-Ortega, S., Sohrabi, M., Divakar, P. K., Lumbsch, H. T. & St. Clair, L. L. 2013a. DNA barcode identification of lichen-forming fungal species in the Rhizoplaca melanophthalma species-complex (Lecanorales, Lecanoraceae), including five new species. MycoKeys 7: 1–22.
36.
Leavitt, S. D., Fernández-Mendoza, F., Pérez-Ortega, S., Sohrabi, M., Divakar, P. K., Vondrák, J., Thorsten Lumbsch, H. & St. Clair, L. L. 2013b. Local representation of global diversity in a cosmopolitan lichen-forming fungal species complex (Rhizoplaca, Ascomycota). Journal of Biogeography 40: 1792–1806.
37.
Leavitt, S. D., Lumbsch, H. T., Stenroos, S. & St. Clair, L. L. 2013c. Pleistocene speciation in North American lichenized fungi and the impact of alternative species circumscriptions and rates of molecular evolution on divergence estimates. PLoS ONE 8: e85240.
38.
Leavitt, S. D., Grewe, F., Widhelm, T., Muggia, L., Wray, B. & Lumbsch, H. T. 2016. Resolving evolutionary relationships in lichen-forming fungi using diverse phylogenomic datasets and analytical approaches. Scientific Reports 6: 22262.
39.
Leavitt, S. D., Kirika, P. M., Amo De Paz, G., Huang, J.-P., Hur, J.-S., Elix, J. A., Grewe, F., Divakar, P. K. & Lumbsch, H. T. 2018. Assessing phylogeny and historical biogeography of the largest genus of lichen-forming fungi, Xanthoparmelia (Parmeliaceae, Ascomycota). The Lichenologist 50: 299–312.
40.
Lindahl, T. 1993. Instability and decay of the primary structure of DNA. Nature 362: 709–715.
41.
Lofgren, L. A., Uehling, J. K., Branco, S., Bruns, T. D., Martin, F. & Kennedy, P. G. 2019. Genome-based estimates of fungal rDNA copy number variation across phylogenetic scales and ecological lifestyles. Molecular Ecology.
42.
Lozier, J. D. & Cameron, S. A. 2009. Comparative genetic analyses of historical and contemporary collections highlight contrasting demographic histories for the bumble bees Bombus pensylvanicus and B. impatiens in Illinois. Molecular Ecology 18: 1875–1886.
43.
McCormack, J. E., Tsai, W. L. & Faircloth, B. C. 2016. Sequence capture of ultraconserved elements from bird museum specimens. Molecular Ecology Resources 16: 1189–1203.
44.
McCune, B. & Rosentreter, R. 2007. Biotic Soil Crust Lichens of the Columbia Basin. Monographs in North American Lichenology 1: 1–105.
45.
McGuire, J. A., Cotoras, D. D., O’Connell, B., Lawalata, S. Z. S., Wang-Claypool, C. Y., Stubbs, A., Huang, X., Wogan, G. O. U., Hykin, S. M., Reilly, S. B., Bi, K., Riyanto, A., Arida, E., Smith, L. L., Milne, H., Streicher, J. W. & Iskandar, D. T. 2018. Squeezing water from a stone: high-throughput sequencing from a 145-year old holotype resolves (barely) a cryptic species problem in flying lizards. PeerJ 6: e4470.
46.
Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. 2014. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32: 268–274.
47.
Orange, A, James, P. W. & White, F. J. 2001. Microchemical methods for the identification of lichens. Twayne Publishers.
48.
Pääbo, S. 1988. Ancient DNA: Extraction, characterization, molecular cloning, and enzymatic amplification. Proceedings of the Nattional Academy of Sciences 86: 1939–1943.
49.
Paul, F., Otte, J., Schmitt, I. & Dal Grande, F. 2018. Comparing Sanger sequencing and high-throughput metabarcoding for inferring photobiont diversity in lichens. Scientific Reports 8: 8624.
50.
Redchenko, O., Vondrák, J. & Košnar, J. 2012. The oldest sequenced fungal herbarium sample. The Lichenologist 44: 715–718.
51.
Rittmeyer, E. N. & Austin, C. C. 2015. Combined next-generation sequencing and morphology reveal fine-scale speciation in Crocodile Skinks (Squamata: Scincidae: Tribolonotus). Molecular Ecology 24: 466–483.
52.
Rowe, K. C., Singhal, S., Macmanes, M. D., Ayroles, J. F., Morelli, T. L., Rubidge, E.M, Bi, K. E. & Moritz, C. C. 2011. Museum genomics: low‐cost and high‐accuracy genetic data from historical specimens. Molecular Ecology Resources 11: 1082–1092.
53.
Rozewicki, J., Yamada, K. D. & Katoh, K. 2017. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics: bbx108.
54.
Schilthuizen, M., Vairappan, C. S., Slade, E. M., Mann, D. J. & Miller, J. A. 2015. Specimens as primary data: museums and ‘open science’. Trends in Ecology and Evolution 30: 237–238.
55.
Schmid, S., Neuenschwander, S., Pitteloud, C., Heckel, G., Pajkovic, M., Arlettaz, R. & Alvarez, N. 2018. Spatial and temporal genetic dynamics of the grasshopper Oedaleus decorus revealed by museum genomics. Ecology and Evolution 8: 1480–1495.
56.
Silva, P. C., Malabarba, M. C. & Malabarba, L. R. 2017. Using ancient DNA to unravel taxonomic puzzles: the identity of Deuterodon pedri (Ostariophysi: Characidae). Neotropical Ichthyology 15: e160141.
57.
Sohrabi, M., Myllys, L. & Stenroos, S. 2010. Successful DNA sequencing of a 75 year-old herbarium specimen of Aspicilia aschabadensis (J. Steiner) Mereschk. The Lichenologist 42: 626–628.
58.
Spurgin, L. G., Wright, D. J., van der Velde, M., Collar, N. J., Komdeur, J., Burke, T. & Richardson, D. S. 2014. Museum DNA reveals the demographic history of the endangered Seychelles warbler. Evolution Applications 7: 1134–1143.
59.
Staats, M., Erkens, R. H. J., van de Vossenberg, B., Wieringa, J. J., Kraaijeveld, K., Stielow, B., Geml, J., Richardson, J. E. & Bakker, F. T. 2013. Genomic treasure troves: Complete genome sequencing of herbarium and insect museum specimens. PlosONE 8: e69189.
60.
Tonini, J., Moore, A., Stern, D., Shcheglovitova, M. & Orti, G. 2015. Concatenation and species tree methods exhibit statistically indistinguishable accuracy under a range of simulated conditions. PLoS Currents 7.
61.
Wen, J., Ickert‐Bond, S. M., Appelhans, M. S., Dorr, L. J. & Funk, V. A. 2015. Collections‐based systematics: Opportunities and outlook for 2050. Journal of Systematics and Evolution 53: 477–488.
62.
Wheeler, D. L., Barrett, T., Benson, D. A., Bryant, S. H., Canese, K., Chetvernin, V., Church, D. M., DiCuccio, M., Edgar, R., Federhen, S., Geer, L. Y., Kapustin, Y., Khovayko, O., Landsman, D., Lipman, D. J., Madden, T. L., Maglott, D. R., Ostell, J., Miller, V., Pruitt, K. D., Schuler, G. D., Sequeira, E., Sherry, S. T., Sirotkin, K., Souvorov, A., Starchenko, G., Tatusov, R. L., Tatusova, T. A., Wagner, L. & Yaschenko, E. 2006. Database resources of the National Center for Biotechnology Information. Nucleic Acids Research: gkl1031.
63.
Wood, H. M., González, V. L., Lloyd, M., Coddington, J. & Scharff, N. 2018. Next-generation museum genomics: Phylogenetic relationships among palpimanoid spiders using sequence capture techniques (Araneae: Palpimanoidea). Molecular Phylogenetics and Evolution 127: 907–918.
64.
Zeng, Q., Cui, Z., Wang, J., Childs, K. L., Sundin, G. W., Cooley, D. R., Yang, C. H., Garofalo, E., Eaton, A., Huntley, R. B., Yuan, X. & Schultes, N. P. 2018. Comparative genomics of Spiraeoideae-infecting Erwinia amylovora strains provides novel insight to genetic diversity and identifies the genetic basis of a low-virulence strain. Molecular Plant Pathology 19: 1652–1666.
CITATIONS (9):
1.
Metagenomic data reveal diverse fungal and algal communities associated with the lichen symbiosis
Hayden Smith, Grande Dal, Lucia Muggia, Rachel Keuler, Pradeep Divakar, Felix Grewe, Imke Schmitt, H. Lumbsch, Steven Leavitt
Symbiosis
Hayden Smith, Grande Dal, Lucia Muggia, Rachel Keuler, Pradeep Divakar, Felix Grewe, Imke Schmitt, H. Lumbsch, Steven Leavitt
Symbiosis
2.
Metagenomic data reveal diverse fungal and algal communities associated with the lichen symbiosis
Hayden Smith, Grande Dal, Lucia Muggia, Rachel Keuler, Pradeep Divakar, Felix Grewe, Imke Schmitt, H. Lumbsch, Steven Leavitt
Hayden Smith, Grande Dal, Lucia Muggia, Rachel Keuler, Pradeep Divakar, Felix Grewe, Imke Schmitt, H. Lumbsch, Steven Leavitt
3.
Institutional Differences in the Stewardship and Research Output of United States Herbaria
Alexis Garretson
Alexis Garretson
4.
Genome-scale data reveal the role of hybridization in lichen-forming fungi
Rachel Keuler, Alexis Garretson, Theresa Saunders, Robert Erickson, Andre St., Felix Grewe, Hayden Smith, H. Lumbsch, Jen-Pan Huang, Clair St., Steven Leavitt
Scientific Reports
Rachel Keuler, Alexis Garretson, Theresa Saunders, Robert Erickson, Andre St., Felix Grewe, Hayden Smith, H. Lumbsch, Jen-Pan Huang, Clair St., Steven Leavitt
Scientific Reports
5.
Characterizing the ribosomal tandem repeat and its utility as a DNA barcode in lichen-forming fungi
Michael Bradshaw, Felix Grewe, Anne Thomas, Cody Harrison, Hanna Lindgren, Lucia Muggia, Clair St., H. Lumbsch, Steven Leavitt
BMC Evolutionary Biology
Michael Bradshaw, Felix Grewe, Anne Thomas, Cody Harrison, Hanna Lindgren, Lucia Muggia, Clair St., H. Lumbsch, Steven Leavitt
BMC Evolutionary Biology
6.
Cora timucua (Hygrophoraceae), a new and potentially extinct, previously misidentified basidiolichen of Florida inland scrub documented from historical collections
Robert Lücking, Laurel Kaminsky, Gary Perlmutter, James Lawrey, Manuela Forno
The Bryologist
Robert Lücking, Laurel Kaminsky, Gary Perlmutter, James Lawrey, Manuela Forno
The Bryologist
7.
Genomic library preparation and hybridization capture of formalin‐fixed tissues and allozyme supernatant for population genomics and considerations for combining capture‐ and RADseq‐based single nucleotide polymorphism data sets
Kyle O’Connell, Kevin Mulder, Addison Wynn, Kevin Queiroz, Rayna Bell
Molecular Ecology Resources
Kyle O’Connell, Kevin Mulder, Addison Wynn, Kevin Queiroz, Rayna Bell
Molecular Ecology Resources
8.
Interpreting phylogenetic conflict: Hybridization in the most speciose genus of lichen-forming fungi
Rachel Keuler, Jacob Jensen, Alejandrina Barcena-Peña, Felix Grewe, Lumbsch Thorsten, Jen-Pan Huang, Steven Leavitt
Molecular Phylogenetics and Evolution
Rachel Keuler, Jacob Jensen, Alejandrina Barcena-Peña, Felix Grewe, Lumbsch Thorsten, Jen-Pan Huang, Steven Leavitt
Molecular Phylogenetics and Evolution
9.
Anderson and Shushan: Lichens of Western North America Fascicle VIII
Hailey Jones, Clair St., Jason Hollinger, Laura Cooper, Roger Rosentreter, Rachel Keuler, Steven Leavitt
Evansia
Hailey Jones, Clair St., Jason Hollinger, Laura Cooper, Roger Rosentreter, Rachel Keuler, Steven Leavitt
Evansia
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.