[en] Premise of the Study
Factors shaping spatiotemporal patterns of associations in mutualistic systems are poorly understood. We used the lichen‐forming fungi Peltigera and their cyanobacterial partners Nostoc to investigate the spatial structure of this symbiosis at an intrabiome scale and to identify potential factors shaping these associations.
Methods
Ninety‐three thalli were sampled in Québec, Canada, along a south–north and an east–west transect of ~1300 km each. We identified the two main partners (Peltigera species and Nostoc phylogroups) using molecular markers and modeled the effects of environmental variables and partner occurrence on Peltigera–Nostoc distributions.
Key Results
Peltigera species showed a high degree of specialization toward cyanobionts, whereas two Nostoc phylogroups dominated both transects by associating with several Peltigera species. Peltigera species had narrower ranges than these two main cyanobionts. Distributions of three Peltigera species were highly associated with precipitation and temperature variables, which was not detected for Nostoc phylogroups at this spatial scale.
Conclusions
For these cyanolichens, factors driving patterns of symbiotic associations are scale dependent. Contrary to global‐scale findings, generalist Peltigera species were not more widespread within the boreal biome than specialists. Nostoc availability was not the only driver of Peltigera species’ geographic ranges; environmental factors also contributed to their intrabiome distributions. Climatic conditions (especially precipitation) limited the range of some Peltigera species more than the range of their cyanobacterial partners at an intrabiome (boreal) scale.
Magain, Nicolas ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et de la conservation - aCREA-Ulg
Miadlikowska, Jolanta; Duke University > Biology
Coyle, Jessica R.; Stanford > Biology
Truong, Camille; Duke University > Biology
Lutzoni, François; Duke University > Biology
Language :
English
Title :
Bioclimatic factors at an intrabiome scale are more limiting than cyanobiont availability for the lichen‐forming genus Peltigera
Publication date :
12 July 2018
Journal title :
American Journal of Botany
ISSN :
0002-9122
eISSN :
1537-2197
Publisher :
Botanical Society of America, United States - Missouri
Baloch, E., H. T. Lumbsch, and M. Wedin. 2010. Major clades and phylogenetic relationships between lichenized and non-lichenized lineages in Ostraples (Ascomycota: Lecanoromycetes). Taxon 59: 1483–1494.
Beck, A., T. Kasalicky, and G. Rambold. 2002. Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida. New Phytologist 153: 317–326.
Blaha, J., E. Baloch, and M. Grube. 2006. High photobiont diversity associated with the euryoecious lichen-forming ascomycete Lecanora rupicola (Lecanoraceae, Ascomycota). Biological Journal of the Linnean Society 88: 283–293.
Boucher, D. H., S. James, and K. H. Keeler. 1982. The ecology of mutualism. Annual Review of Ecology and Systematics 13: 315–347.
Carpenter, B., A. Gelman, M. D. Hoffman, D. Lee, B. Goodrich, M. Betancourt, M. Brubaker, et al. 2017. Stan: A probabilistic programming language. Journal of Statistical Software 76: 1–32.
Chagnon, P.-L., N. Magain, J. Miadlikowska, and F. Lutzoni. 2018. Strong specificity and network modularity at a very fine phylogenetic scale in the lichen genus Peltigera. Oecologia 187: 767–782.
Clement, M., D. Posada, and K. A. Crandall. 2000. TCS: A computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1660.
Cornelissen, J. H. C., T. V. Callaghan, J. M. Alatalo, A. Michelsen, E. Graglia, A. E. Hartley, D. S. Hik, et al. 2001. Global change and arctic ecosystems: Is lichen decline a function of increases in vascular plant biomass? Journal of Ecology 89: 984–994.
Darnajoux, R., X. Zhang, D. L. McRose, J. Miadlikowska, F. Lutzoni, A. M. L. Kraepiel, and J.-P. Bellenger. 2017. Biological nitrogen fixation by alternative nitrogenases in boreal cyanolichens: Importance of molybdenum availability and implications for current biological nitrogen fixation estimates. New Phytologist 213: 680–689.
de Vienne, D. M., G. Refregier, M. Lopez-Villavicencio, A. Tellier, M. E. Hood, and T. Giraud. 2013. Cospeciation vs host-shift speciation: Methods for testing, evidence from natural associations and relation to coevolution. New Phytologist 198: 347–385.
Gardes, M., and T. D. Bruns. 1993. ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113–118.
Hodkinson, B. P., J. L. Allen, L. Forrest, B. Goffinet, E. Sérusiaux, Ó. S. Andrésson, V. Miao, et al. 2014. Lichen-symbiotic cyanobacteria associated with Peltigera have an alternative vanadium-dependent nitrogen fixation system. European Journal of Phycology 49: 11–19.
Hodkinson, B. P., N. R. Gottel, C. W. Schadt, and F. Lutzoni. 2012. Photoautotrophic symbiont and geography are major factors affecting highly-structured and diverse bacterial communities in the lichen microbiome. Environmental Microbiology 14: 147–161.
Hodkinson, B. P., and F. Lutzoni. 2009. A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49: 163–180.
Li, L. A., and L. R. Tabita. 1997. Maximum activity of recombinant ribulose 1,5 bisphosphate carboxylase/oxygenase of Anabaena sp. strain CA requires the product of the rbcX gene. Journal of Bacteriology 179: 3793–3796.
Lutzoni, F., M. Pagel, and V. Reeb. 2001. Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411: 937–940.
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., and W. Maddison. 2005. MacClade v. 4.08. Sinauer Associates, Sunderland, Massachusetts, USA.
Magain, N., J. Miadlikowska, B. Goffinet, E. Sérusiaux, and F. Lutzoni. 2017a. Macroevolution of specificity in cyanolichens of the genus Peltigera section Polydactylon (Lecanoromycetes, Ascomycota). Systematic Biology 66: 74–99.
Magain, N., J. Miadlikowska, O. Mueller, M. Gajdeczka, C. Truong, A. Salamov, I. Dubchak, et al. 2017b. Conserved genomic collinearity as a source of broadly applicable, fast evolving, markers to resolve species complexes: A case study using the lichen-forming genus Peltigera section Polydactylon. Molecular Phylogenetics and Evolution 117: 10–29.
Miadlikowska, J., and F. Lutzoni. 2000. Phylogenetic revision of the genus Peltigera (lichen-forming ascomycetes) 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 canina species complex. Mycologia 95: 1181–1203.
Miadlikowska, J., D. Richardson, N. Magain, B. Ball, F. Anderson, R. Cameron, J. Lendemer, et al. 2014. Phylogenetic placement, species delimitation, and cyanobiont identity of endangered aquatic Peltigera species (lichen-forming Ascomycota, Lecanoromycetes). American Journal of Botany 101: 1141–1156.
Miller, M. A., W. Pfeiffer, and T. Schwartz. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE), 2010, IEEE.
Myllys, L., S. Stenroos, A. Thell, and M. Kuusinen. 2006. High cyanobiont selectivity of epiphytic lichens in old growth boreal forest in Finland. New Phytologist 173: 621–629.
Nash, T. H. 2008. Lichen biology. Cambridge University Press, Cambridge, UK.
Nelsen, M. P., and A. Gargas. 2009. Symbiont flexibility in (Pertusariales: Icmadophilaceae). The Bryologist 112: 404–417.
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 fungus 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. Aragón, I. Martínez, and M. Wedin. 2013. Cardinal characters on a slippery slope: A re-evaluation of phylogeny, character evolution, and evolutionary rates in the jelly lichens (Collemataceae s. str). Molecular Phylogenetics and Evolution 68: 185–198.
Otálora, M. A., I. Martínez, H. O'Brien, M. C. Molina, G. Aragon, 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.
Paulsrud, P., and P. Lindblad. 1998. Sequence variation of the tRNA Leu Intron as a marker for genetic diversity and specifcity of symbiotic cyanobacteria in some lichens. Applied and Environmental Microbiology 64: 310–315.
Peksa, O., and P. Škaloud. 2011. Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Molecular Ecology 20: 3936–3948.
Pérez-Ortega, S., R. Ortiz-Álvarez, T. G. A. Green, and A. de Los Ríos. 2012. Lichen myco-and photobiont diversity and their relationships at the edge of life (McMurdo Dry Valleys, Antarctica). FEMS Microbiology Ecology 82: 429–448.
Rodríguez, F. J., J. L. Oliver, A. Marín, and J. R. Medina. 1990. The general stochastic model of nucleotide substitution. Journal of Theoretical Biology 142: 485–501.
Rudi, K., O. M. Skulberg, and K. S. Jakobsen. 1998. Evolution of cyanobacteria by exchange of genetic material among phyletically related strains. Journal of Bacteriology 180: 3453–3461.
Schoch, C. L., K. A. Seifert, S. Huhndorf, V. Robert, J. L. Spouge, C. A. Levesque, and W. Chen. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences USA 109: 6241–6246.
Singh, G., F. Dal Grande, P. K. Divakar, J. Otte, A. Crespo, and I. Schmitt. 2016. Fungal-algal association patterns in lichen symbiosis linked to macroclimate. New Phytologist 214: 317–329.
Spribille, T., V. Tuovinen, P. Resl, D. Vanderpool, H. Wolinski, M. C. Aime, K. Schneider, et al. 2016. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353: 488–492.
Stamatakis, A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.
Stamatakis, A., P. Hoover, and J. Rougemont. 2008. A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology 57: 758–771.
Stan Development Team. 2017. RStan: The R interface to Stan. R package version 2.16.2. http://mc-stan.org.
Thompson, J. N. 2005. The geographic mosaic of evolution. University of Chicago Press, Chicago, Illinois, USA.
Vasquez, D. P., C. J. Melián, N. M. Williams, N. Blüthen, B. R. Krasnov, and R. Poulin. 2007. Species abundance and asymmetrical interaction strength in ecological networks. Oikos 116: 1120–1127.
Vermeji, G. J. 1999. Inequality and the directionality of history. The American Naturalist 153: 243–253.
Vermeji, G. J. 2004. Nature: An economic history. Princeton University Press, Princeton, New Jersey, USA.
Wedin, M., H. Döring, and G. Gilenstam. 2004. Saprotrophy and lichenization as options for the same fungal species on different substrata: Environmental plasticity and fungal lifestyles in the Stictis-Conotrema complex. New Phytologist 164: 459–465.
Werth, S., and D. Fontaneto. 2011. Biogeography and phylogeography of lichen fungi and their photobionts. In D. Fontaneto [ed.], Biogeography of micro-organisms: Is everything small everywhere? 191–208. Cambridge University Press, Cambridge, UK.
Wheeler, D. L., T. Barrett, D. A. Benson, S. H. Bryant, K. Canese, V. Chetvernin, D. M. Church, et al. 2007. Database resources of the national center for biotechnology information. Nucleic Acids Research 35: D5–D12.
White, T. J., T. Bruns, S. Lee, and J. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications 18: 315–322.
Wilson, D. S., and J. Yoshimura. 1994. On the coexistence of specialists and generalists. American Naturalist 144: 692–707.
Wirtz, N., H. T. Lumbsch, T. G. Green, R. Türk, A. Pintado, L. Sancho, and B. Schroeter. 2003. Lichen fungi have low cyanobiont selectivity in maritime Antarctica. New Phytologist 160: 177–183.
Yahr, R., R. Vilgalys, and P. T. Depriest. 2004. Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Molecular Ecology 13: 3367–3378.
Zolan, M., and P. Pukkila. 1986. Inheritance of DNA methylation in Coprinus cinereus. Molecular and Cellular Biology 6: 195–200.
Zúñiga, C., D. Leiva, M. Carú, and J. Orlando. 2017. Substrates of Peltigera lichens as a potential source of cyanobionts. Microbial Ecology 74: 561–569.
