Phylogenetic placement, species delimitation, and cyanobiont identity of endangered aquatic Peltigera species (lichen-forming Ascomycota, Lecanoromycetes)
[en] Premise of this study: Aquatic cyanolichens from the genus Peltigera section Hydrothyriae are subject to anthropogenic threats and, therefore, are considered endangered. In this study we addressed the phylogenetic placement of section Hydrothyriae within Peltigera. We delimited species within the section and identified their symbiotic cyanobacteria.
• Methods: Species delimitation and population structure were explored using monophyly as a grouping criterion (RAxML) and Structurama based on three protein-coding genes in combination with two nuclear ribosomal loci. The 16S and rbcLX sequences for the cyanobionts were analyzed in the broad phylogenetic context of free-living and symbiotic cyanobacteria.
• Key results: We confirm with high confidence the placement of section Hydrothyriae within the monophyletic genus Peltigera; however, its phylogenetic position within the genus remains unsettled. We recovered three distinct monophyletic groups corresponding to three species: P. hydrothyria, P. gowardii s.s., and P. aquatica Miadl. & Lendemer, the latter being formally introduced here. Each species was associated with an exclusive set of Nostoc haplotypes.
• Conclusions: The ITS region alone provides sufficient genetic information to distinguish the three morphologically cryptic species within section Hydrothyriae. Section Hydrothyriae seems to be associated with a monophyletic lineage of Nostoc, that has not been found in symbiotic association with other members of Peltigera. Capsosira lowei should be transferred to the genus Nostoc. Potential threats to P. aquatica should be re-examined based on the recognition of two aquatic species in western North America.
Magain, Nicolas ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et de la conservation - aCREA-Ulg
Ball, Bernard
Anderson, Frances
Cameron, Robert
Lendemer, James
Truong, Camille
Lutzoni, François; Duke University > Biology
Language :
English
Title :
Phylogenetic placement, species delimitation, and cyanobiont identity of endangered aquatic Peltigera species (lichen-forming Ascomycota, Lecanoromycetes)
Publication date :
July 2014
Journal title :
American Journal of Botany
ISSN :
0002-9122
eISSN :
1537-2197
Publisher :
Botanical Society of America, St Louis, United States - Missouri
AYLOR, D. L., E. W. PRICE, AND I. CARBONE. 2006. SNAP: Combine and Map modules for multilocus population genetic analysis. Bioinformatics 22: 1399-1401.
CASAMATTA, D. A., S. R. GOMEZ, AND J. R. JOHANSEN. 2006. Rexia erecta gen. et sp. nov. and Capsosira loweisp. nov., two newly described cyanobacterial taxa from the Smoky Mountains National Park (USA). Hydrobiologia 561: 13-26.
COSEWIC. 2013a. COSEWIC status report on the eastern waterfan (Peltigera hydrothyria)in Canada. Committee on the Status of Endangered Wildlife in Canada, Ottawa, Ontario, Canada. viii + 45 pp.
COSEWIC. 2013b. COSEWIC status report on the Western Waterfan (Peltigera gowardii)in Canada. Committee on the Status of Endangered Wildlife in Canada, Ottawa, Ontario, Canada. vii + 37 pp.
ELVEBAKK, A., D. PAPAEFTHIMIOU, E. H. ROBERTSEN, AND A. LIAIMER. 2008. Phylogenetic patterns among Nostoccyanobionts within bi-and tripartite lichens of the genus Pannaria. Journal of Phycology 44: 1049-1059.
ESSLINGER, T. L. 2010. A cumulative checklist for the lichen-forming, lichenicolous and allied fungi of the continental United States and Canada. North Dakota State University, Fargo, North Dakota, USA. Available at http://www.ndsu.edu/pubweb/~esslinge/chcklst/chcklst7.htm [First posted 1 December 1997, most recent version #18, 13 December 2012].
FERNÁNDEZ-MENDOZA, F., S. DOMASCHKE, M. A. GARCÍA, P. JORDAN, M. P. MARTÍN, AND C. PRINTZEN. 2011. Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Molecular Ecology 20: 1208-1232.
GAYA, E., F. HÖGNABBA, A. HOLGUIN, K. MOLNAR, S. FERNÁNDEZ-BRIME, S. STENROOS, U. ARUP, ET AL. 2012. Implementing a cumulative supermatrix approach for a comprehensive phylogenetic study of the Teloschistales (Pezizomycotina, Ascomycota). Molecular Phylogenetics and Evolution 63: 374-387.
GOFFINET, B., AND R. I. HASTINGS. 1995. To new sorediate taxa of Peltigera. Lichenologist 27: 43-58.
GOFFINET, B., AND J. M IADLIKOWSKA. 1999. Peltigera phyllidiosa (Peltigeraceae, Ascomycotina), a new species from the Southern Appalachians corroborated by ITS sequences. Lichenologist 31: 247-256.
GOFFINET, B., J. MIADLIKOWSKA, AND T. GOWARD. 2003. Phylogenetic inferences based on nrDNA sequences support five morphospecies within the Peltigera didactylacomplex (lichenized Ascomycota). Bryologist 106: 349-364.
GOWARD, T., AND B. GOFFINET. 2000. Peltigera chionophila, a new lichen (Ascomycetes) from the western cordillera of North America. Bryologist 103: 493-498.
HAN, L.-F., Y.-Y. ZHANG, AND S.-Y. GUO. 2013. Peltigera wulingensis, a new lichen (Ascomycota) from north China. Lichenologist 45: 329-336.
HOFSTETTER, V., J. MIADLIKOWSKA, F. KAUFF, AND F. LUTZONI. 2007. Phylogenetic comparison of protein-coding versus ribosomal RNAcoding sequence data: A case study of the Lecanoromycetes (Ascomycota). Molecular Phylogenetics and Evolution 44: 412-426.
HROUZEK, P., A. LUKESOVÁ, J. MARES, AND S. VENTURA. 2013. Description of the cyanobacterial genus Desmonostocgen. nov. including D. muscorumcomb. nov. as a distinct, phylogenetically coherent taxon related to the genus Nostoc. Fottea 13: 201-213.
HUELSENBECK, J. P., P. ANDOLFATTO, AND E. T. E. EDNA. 2011. Structurama: Bayesian inference of population structure. Evolutionary Bioinformatics Online 7: 55-59.
KIRK, P. M., P. F. CANNON, D. W. MINTER, AND J. A. STALPERS [eds.]. 2008. Ainsworth & Bisby's Dictionary of the Fungi, 10th ed. CABI, Wallingford, UK.
KORELUSOVÁ, J. 2008. Phylogeny of heterocystous Cyanobacteria (Nostocales and Stigonematales). M. Sc. thesis, University of South Bohemia, Ceské Budejovice, Czech Republic.
KROKEN, S., AND J. W. TAYLOR. 2000. Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxiaforming lichens with the fungal genus Letharia. Bryologist 103: 645-660.
LANFEAR, R., B. CALCOTT, S. Y. W. HO, AND S. GUINDON. 2012. PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29: 1695-1701.
LENDEMER, J. C., AND F. ANDERSON. 2012. Molecular data confirm the identity of populations of the water fan lichen from eastern Canada as Peltigera hydrothyrias. str. Opuscula Philolichenum 1 1: 139-140.
LENDEMER, J. C., AND H. O ' BRIEN. 2011. How do you reconcile molecular and non-molecular datasets? A case study where new molecular data prompts a revision of Peltigera hydrothyria s.l. in North America and the recognition of two species. Opuscula Philolichenum 9: 99-110.
LI, L.-A., AND F. R. TABITA. 1997. Maximum activity of recombinant ribulose 1,5-bisphosphate carboxylase/oxygenase of Anabaenasp. strain CA requires the product of the rbcX gene. Journal of Bacteriology 179: 3793-3796.
LUTZONI, F., F. KAUFF, C. COX, D. MCLAUGHLIN, G. CELIO, B. DENTINGER, M. PADAMSEE, ET AL. 2004. Assembling the fungal tree of life: Progress, classification, and evolution of subcellular traits. American Journal of Botany 91: 1446-1480.
LUTZONI, F., P. WAGNER, V. REEB, AND S. ZOLLER. 2000. Integrating ambiguously aligned regions of DNA sequences in phylogenetic analyses without violating positional homology. Systematic Biology 49: 628-651.
MADDISON, D. R., AND W. P. MADDISON. 2003. McClade: Analysis of phylogeny and character evolution, 4.07. Sinauer, Sunderland, Massachusetts, USA.
MAGAIN, N., AND E. SÉRUSIAUX. 2014. Do photobiont switch and cephalodia emancipation act as evolutionary drivers in the lichen symbiosis? A case study in the Pannariaceae (Peltigerales). PLoS ONE 10.1371/ journal. pone.0089876.
MARTÍNEZ, I., A. R. BURGAZ, O. VITIKAINEN, AND A. ESCUDERO. 2003. Distribution patterns in the genus Peltigera Willd. Lichenologist 35: 301-323.
MASON-GAMER, R., AND E. KELLOGG. 1996. Testing for phylogenetic conflict among molecular datasets in the tribe Triticeae (Gramineae). Systematic Biology 45: 524-545.
MIADLIKOWSKA, J., AND F. LUTZONI. 2000. Phylogenetic revision of the genus Peltigera(lichen-forming Ascomycota) based on morphological, chemical, and large subunit nuclear ribosomal DNA data. International Journal of Plant Sciences 161: 925-958.
MIADLIKOWSKA, J., AND F. LUTZONI. 2004. Phylogenetic classification of Peltigeralean fungi (Peltigerales, Ascomycota) based on ribosomal RNA small and large subunits. American Journal of Botany 91: 449-464.
MIADLIKOWSKA, J., F. LUTZONI, T. GOWARD, S. ZOLLER, AND D. POSADA. 2003. New approach to an old problem: Incorporating signal from gap-rich regions of ITS and nrDNA large subunit into phylogenetic analyses to resolve the Peltigera caninaspecies complex. Mycologia 95: 1181-1203.
MONACELL, J. T., AND I. CARBONE. 2014. Mobyle SNAP Workbench: A web-based analysis portal for population genetics and evolutionary genomics. Bioinformatics 10.1093/bioinformatics/btu055.
MUGGIA, L., P. NELSON, T. WHEELER, L. S. YAKOVCHENKO, T. TØNSBERG, AND T. SPRIBILLE. 2011. Convergent evolution of a symbiotic duet: The case of the lichen genus Polychidium(Peltigerales, Ascomycota). American Journal of Botany 98: 1647-1656.
NASH, T. H. 2008. Lichen biology. Cambridge University Press, New York, New York, USA.
O ' BRIEN, H. E., J. MIADLIKOWSKA, AND F. LUTZONI. 2005. Assessing host specialization in symbiotic cyanobacteria associated with four closely related species of the lichen fungus Peltigera. European Journal of Phycology 40: 363-378.
O ' BRIEN, H. E., J. MIADLIKOWSKA, AND F. LUTZONI. 2009. Assessing reproductive isolation in highly diverse communities of the lichen-forming fungal genus Peltigera. Evolution 63: 2076-2086.
O ' BRIEN, H. E., J. MIADLIKOWSKA, AND F. LUTZONI. 2013. Assessing population structure and host specialization in lichenized cyanobacteria. New Phytologist 198: 557-566.
OTÁLORA, M. A. G., I. MARTÍNEZ, H. E. O'BRIEN, M. C. MOLINA, G. ARAGÓN, AND F. LUTZONI. 2010. Multiple origins of high reciprocal symbiotic specificity at an intercontinental spatial scale among gelatinous lichens (Collemataceae, Lecanoromycetes). Molecular Phylogenetics and Evolution 56: 1089-1095.
PETERSON, E. B. 2010. Conservation assessment with management guidelines for Peltigera hydrothyriaMiadlikowska & Lutzoni (a.k.a. Hydrothyria venosaJ.L. Russell. Report for U.S. Forest Service, Region 5, Vallejo, California, USA.
POULSEN, B., AND T. CARLBERG. 2007. Peltigera hydrothyria, sponsorship for the CALS Conservation Committee. Bulletin of the Californian Lichen Society 14: 15-18.
REEB, V., F. LUTZONI, AND C. ROUX. 2004. Multilocus phylogenetic circumscription of the lichen-forming fungi family Acarosporaceae and its position within the Ascomycota. Molecular Phylogenetics and Evolution 32: 1036-1060.
RIVASPLATA, E., S. PARNMEN, B. STAIGER, A. MANGOLD, A. FRISCH, G. WEERAKOON, J. E. HERNÁNDEZ, ET AL. 2013. A molecular phylogeny of Graphidaceae (Ascomycota, Lecanoromycetes, Ostropales) including 428 species. MycoKeys 6: 55-94.
RODRÍGUEZ, F., J. L. OLIVER, A. MARÍN, AND J. R. MEDINA. 1990. The general stochastic model of nucleotide substitution. Journal of Theoretical Biology 142: 485-501.
RUSSELL, J. L. 1856. Hydrothyria venosa, a new genus and species of the Collemataceae. Proceedings of the Essex Institute 1: 1 88.
SCHEIDEGGER, C., AND S. WERTH. 2009. Conservation strategies for lichens: Insights from population biology. Fungal Biology Reviews 23: 55-66.
SÉRUSIAUX, E., B. GOFFINET, J. MIADLIKOWSKA, AND O. VITIKAINEN. 2009. Taxonomy, phylogeny and biogeography of the lichen genus Peltigera in Papua New Guinea. Fungal Diversity 38: 185-224.
SPRIBILLE, T., AND L. MUGGIA. 2012. Expanded taxon sampling disentangles evolutionary relationships and reveals a new family in Peltigerales (Lecanoromycetidae, Ascomycota). Fungal Diversity 59: 10.1007/ s13225-012-0206-5.
STAMATAKIS, A. 2006. Phylogenetic models of rate heterogeneity: A high performance computing perspective. In Proceedings of 20th IEEE/ACM International Parallel and Distributed Processing Symposium (IPDPS2006), Rhodos, Greece. Available at http://sco.h-its.org/exelixis/ pubs/HICOMB2006.pdf [accessed 23 June 2013].
TURNER, S., K. M. PRYER, V. P. W. MIAO, AND J. D. PALMER. 1999. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. Journal of Eukaryotic Microbiology 46: 327-338.
VITIKAINEN, O. 2006. Peltigera tartarea, a new species from arctic America. Journal of the Hattori Botanical Laboratory 100: 853-854.
WILLDENOW, C. L. 1787. Florae berolinensis prodromus. Wilhelm Vieweg, Berlin, Germany.
ZOLAN, M. E., AND P. J. PUKKILA. 1986. Inheritance of DNA methylation in Coprinus cinereus. Molecular and Cellular Biology 6: 195-200.
