Cophylogenetic patterns in algal symbionts correlate with repeated symbiont switches during diversification and geographic expansion of lichen-forming fungi in the genus Sticta (Ascomycota: Peltigeraceae)
[en] Highlights
•
We explored cophylogenetic patterns of fungal and algal partners in the genus Sticta.
•
Sticta associates with green algae from five genera in Trebouxiophyceae.
•
Sticta are selective towards their algal symbionts.
•
Photosymbiodemes with green algae evolved multiple times in Sticta.
Abstract
Species in the fungal genus Sticta form symbiotic associations primarily with either green algae or cyanobacteria, but tripartite associations or photosymbiodemes involving both types of photobionts occur in some species. Sticta is known to associate with green algae in the genus Symbiochloris. However, previous studies have shown that algae from other genera, such as Heveochlorella, may also be suitable partners for Sticta. We examined the diversity of green algal partners in the genus Sticta and assessed the patterns of association between the host fungus and its algal symbiont.
We used multi-locus sequence data from multiple individuals collected in Australia, Cuba, Madagascar, Mauritius, New Zealand, Reunion and South America to infer phylogenies for fungal and algal partners and performed tests of congruence to assess coevolution between the partners. In addition, event-based methods were implemented to examine which cophylogenetic processes have led to the observed association patterns in Sticta and its green algal symbionts. Our results show that in addition to Symbiochloris, Sticta associates with green algae from the genera Chloroidium, Coccomyxa, Elliptochloris and Heveochlorella, the latter being the most common algal symbiont associated with Sticta in this study. Geography plays a strong role in shaping fungal-algal association patterns in Sticta as mycobionts associate with different algal lineages in different geographic locations. While fungal and algal phylogenies were mostly congruent, event-based methods did not find any evidence for cospeciation between the partners. Instead, the association patterns observed in Sticta and associated algae, were largely explained by other cophylogenetic events such as host-switches, losses of symbiont and failure of the symbiont to diverge with its host. Our results also show that tripartite associations with green algae evolved multiple times in Sticta.
Sérusiaux, Emmanuël ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Département de Biologie, Ecologie et Evolution
Nelsen, Matthew P
Mercado-Diaz, Joel P
Widhelm, Todd J
Lumbsch, H Thorsten
Language :
English
Title :
Cophylogenetic patterns in algal symbionts correlate with repeated symbiont switches during diversification and geographic expansion of lichen-forming fungi in the genus Sticta (Ascomycota: Peltigeraceae)
Ahmadjian, V., Coevolution in lichens. Ann. NY Acad. Sci. 503 (1987), 307–315.
Balbuena, J.A., Míguez-Lozano, R., Blasco-Costa, I., PACo: a novel Procrustes application to cophylogenetic analysis. PLoS ONE, 8, 2013, e61048.
Beck, A., Friedl, T., Rambold, G., Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytol. 139 (1998), 709–720.
Beck, A., Photobiont inventory of a lichen community growing on heavy-metal-rich rock. Lichenologist 31 (1999), 501–510.
Blaha, J., Baloch, E., Grube, M., High photobiont diversity associated with the euryecious lichen-forming ascomycete Lecanora rupicola (Lecanoraceae, Ascomycota). Biol. J. Linnean Soc. 88 (2006), 283–293.
Brodo, I.M., Sharnoff, S.D., Sharnoff, S., Lichens of North America. 2001, Yale University Press, New Haven.
Bubrick, B., Galun, M., Frensdorff, A., Observations on freeliving Trebouxia De Puymaly and Pseudotrebouxia Archibald, and evidence that both symbionts from Xanthoria parietina (L.) Th. Fr. can be found free living in nature. New Phytol. 97 (1984), 455–462.
Büdel, B., Meyer, A., Salazar, N., Zellner, H., Zotz, G., Lange, O.L., Macrolichens of montane rain forests in Panama, Province Chiriqui. Lichenologist 32 (2000), 539–551.
Conow, C., Fielder, D., Ovadia, Y., Liberskind-Hadas, R., Jane: a new tool for the cophylogeny reconstruction problem. Algorithm. Mol. Biol., 5, 2010, 16.
Dal Grande, F., Widmer, I., Wagner, H.H., Scheidegger, C., Vertical andhorizontal photobiont transmission within populations of a lichen symbiosis. Mol. Ecol. 21 (2012), 3159–3172.
Dal Grande, F., Beck, A., Cornejo, C., Singh, G., Cheenacharoen, S., Nelsen, M.P., Scheidegger, C., 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 (2014), 455–470.
Darienko, T., Gustavs, L., Mudimu, O., Rad Menendez, C., Schumann, R., Karsten, U., Friedl, T., Pröschold, T., Chloroidium, a common terrestrial coccoid green alga previously assigned to Chlorella (Trebouxiophyceae, Chlorophyta). Eur. J. Phycol. 45 (2010), 79–95.
Darienko, T., Gustavs, L., Pröschold, T., Species concept and nomenclature change within the genera Elliptochloris and Pseudochlorella (Trebouxiophyceae) based on an integrative approach. J. Phycol. 52 (2016), 1125–1145.
Darriba, D., Taboada, G.L., Doallo, R., Posada, D., jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods, 9, 2012, 772.
Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29 (2012), 1969–1973.
Ertz, D., Guzow-Krzemińska, B., Thor, G., Łubek, A., Kukwa, M., Photobiont switching causes changes in the reproduction strategy and phenotypic dimorphism in the Arthoniomycetes. Sci. Reports, 8(1), 2018, 4952.
Fernández-Mendoza, F., Domaschke, S., Garcia, M.A., Jordan, P., Martín, M.P., Printzen, C., Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol. Ecol. 20 (2011), 1208–1232.
Funk, D.J., Helbling, L., Wernegreen, J.J., Moran, N.A., Intraspecific phylogenetic congruence among multiple symbiont genomes. Proc. R. Soc. Lond. B. 267 (2000), 2517–2521.
Galloway, D.J., Studies on the lichen genus Sticta (Schreber) Ach.: V. Australian species. Trop. Bryol. 15 (1998), 117–160.
Galloway, D.J., 2001. Sticta. In: McCarthy, P.M. (Ed.), Flora of Australia. Volume 58A, Lichens 3. ABRS/CSIRO Australia, Melbourne, pp. 78–97.
Galun, M., Bubrick, P., Physiological interactions between the partners of the lichen symbiosis. Linskens, H.F., Heslop-Harrison, J., (eds.) Cellular interactions, 1984, Springer-Verlag, Berlin Heidelberg, Germany, 362–401.
Green, T.G.A., Smith, D.C., Lichen physiology. 14. Differences between lichen algae in symbiosis and in isolation. New Phytol. 73 (1974), 753–766.
Green, T.G.A., Horstman, J., Bonnett, H., Wilkins, A., Silvester, W.B., Nitrogen fixation by members of the Stictaceae (Lichenes) in New Zealand. New Phytol. 84 (1980), 339–348.
Green, T.G.A., Büdel, B., Heber, U., Meyer, A., Zellner, H., Lange, O.L., Differences in photosynthetic performance between cyanobacterial and green algal components of lichen photosymbiodemes measured in the field. New Phytol. 125 (1993), 723–731.
Guindon, S., Gascuel, O., A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst. Biol. 52 (2003), 696–704.
Gustavs, L., Schiefelbein, U., Darienko, T., Pröschold, T., Symbioses of the green algal genera Coccomyxa and Elliptochloris (Trebouxiophyceae, Chlorophyta). Grube, M., Seckbach, J., Muggia, L., (eds.) Algal and cyanobacterial symbioses, 2017, World Scientific Publishing Europe Ltd., London, UK, 169–208.
Hawksworth, D.L., Co-evolution and detection of ancestry in lichens. J. Hattori Botan. Lab. 52 (1982), 323–329.
Herre, E.A., Knowlton, N., Mueller, U.G., Rehner, S.A., The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol. Evol. 14 (1999), 49–53.
Högnabba, F., Stenroos, S., Thell, A., Phylogenetic relationships and evolution of photobiont associations in the Lobariaceae (Peltigerales, Lecanoromycetes, Ascomycota). Bibl. Lichenol. 100 (2009), 157–187.
Katoh, K., Misawa, K., Kuma, K., Miyata, T., MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30 (2002), 3059–3066.
Katoh, K., Standley, D.M., MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol. Biol. Evol. 30 (2013), 772–780.
Kraichak, E., Huang, J.-P., Nelsen, M., Leavitt, S.D., Lumbsch, H.T., A revised classification of orders and families in the two major subclasses of Lecanoromycetes (Ascomycota) based on a temporal approach. Bot. J. Linn. Soc. 188 (2018), 233–249.
Kranner, I., Cram, W.J., Zorn, M., Wornik, S., Yoshimura, I., Stabentheiner, E., Pfeifhofer, H.W., Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. PNAS 102 (2005), 3141–3146.
Krog, H., Corticolous macrolichens of low montane rainforests and moist woodlands of eastern Tanzania. Sommerfeltia 28 (2000), 1–75.
Legendre, P., Desdevises, Y., Bazin, E., A statistical test for host-parasite coevolution. Syst. Biol. 51 (2002), 217–234.
Leigh, E.G., The evolution of mutualism. J. Evol. Biol. 23 (2010), 2507–2528.
Letsch, M.R., Muller-Parker, G., Friedl, T., Lewis, L., Elliptochloris marina sp. nov. (Trebouxiophyceae, Chlorophyta), symbiotic green alga of the temperate pacific sea anemones Anthopleura xanthogrammica and A. elegantissima (Anthozoa, Cnidaria). J. Phycol. 45 (2009), 1127–1135.
Lücking, R., Lawrey, J.D., Sikaroodi, M., Gillevet, P.M., Chaves, J.L., Sipman, H.J., Bungartz, F., Do lichens domesticate photobionts like farmers domesticate crops? Evidence from a previously unrecognized lineage of filamentous cyanobacteria. Am J Bot 96 (2009), 1409–1418.
Lücking, R., Stop the abuse of time! Strict temporal banding is not the future of rank-based classifications in fungi (including lichens) and other organisms. Crit. Rev. Plant Sci. 38 (2019), 199–253.
Magain, N., Sérusiaux, E., Do photobiont switch and cephalodia emancipation act as evolutionary drivers in the lichen symbiosis? A case study in the Pannariaceae (Peltigerales). PLoS One, 9(2), 2014, e89876, 10.1371/journal.pone.0089876.
Magain, N., Sérusiaux, E., Dismantling the treasured flagship lichen Sticta fuliginosa (Peltigerales) into four species in Western Europe. Mycol. Prog., 14, 2015, 97.
Miadlikowska, J., Lutzoni, F., Phylogenetic classification of peltigeralean fungi (Peltigerales, Ascomycota) based on ribosomal RNA small and large subunits. Am. J. Bot. 91 (2004), 449–464.
Miadlikowska, J., Kauff, F., Hofstetter, V., Fraker, E., Grube, M., Hafellner, J., Reeb, V., Hodkinson, B.P., Kukwa, M., Lücking, R., Hestmark, G., Otálora, M.G., Rauhut, A., Büdel, B., Scheidegger, C., Timdal, E., Stenroos, S., Brodo, I.M., Perlmutter, G.B., Ertz, D., Diederich, P., Lendemer, J.C., May, P.F., Schoch, C., Arnold, A.E., Gueidan, C., Tripp, E., Yahr, R., Robertson, C., Lutzoni, F., New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes. Mycologia 98 (2006), 1088–1103.
Miadlikowska, J., Kauff, F., Högnabba, F., Oliver, J.C., Molnar, K., Fraker, E., Gaya, E., Hafellner, J., Hofstetter, V., Gueidan, C., Otalora, M.A., Hodkinson, B., Kukwa, M., Lucking, R., Björk, C., Sipman, H.J., Burgaz, A.R., Thell, A., Passo, A., Myllys, L., Goward, T., Fernandez-Brime, S., Hestmark, G., Lendemer, J., Lumbsch, H.T., Schmull, M., Schoch, C.L., Sérusiaux, E., Maddison, D.R., Arnold, A.E., Lutzoni, F., Stenroos, S., A multigene phylogenetic synthesis for the class Lecanoromycetes (Ascomycota): 1307 fungi representing 1139 infrageneric taxa, 317 genera and 66 families. Mol. Phylogenet. Evol. 79 (2014), 132–168.
Millanes, A.M., Truong, C., Westberg, M., Diederich, P., Wedin, M., Host switching promotes diversity in host-specialized mycoparasitic fungi: uncoupled evolution in the Biatoropsis-Usnea system. Evolution 68 (2014), 1576–1593.
Miller, M.A., Pfeiffer, W., Schwartz, T., 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA, pp. 1–8.
Moncada, B., Lücking, R., Betancourt-Macuase, L., Phylogeny of the Lobariaceae (lichenized Ascomycota: Peltigerales), with a reappraisal of the genus Lobariella. Lichenologist 45 (2013), 203–263.
Moncada, B., Coca, L.F., Lücking, R., Neotropical members of Sticta (lichenized Ascomycota: Lobariaceae) forming photosymbiodemes, with the description of seven new species. The Bryologist 116 (2013), 169–201.
Moncada, B., Lücking, R., Suárez, A., Molecular phylogeny of the genus Sticta (lichenized Ascomycota: Lobariaceae) in Colombia. Fungal Divers. 64 (2014), 205–231.
Moncada, B., Mercado-Díaz, J.A., Lücking, R., The identity of Sticta damicornis (Ascomycota: Lobariaceae): a presumably widespread taxon is a Caribbean endemic. The Lichenologist 50 (2018), 591–597.
Muggia, L., Baloch, E., Stabentheiner, E., Grube, M., Wedin, M., Photobiont association and genetic diversity of the optionally lichenized fungus Schizoxylon albescens. FEMS Microbiol. Ecol. 75 (2011), 255–272.
Muggia, L., Pérez-Ortega, S., Kopun, T., Zellnig, G., Grube, M., Photobiont selectivity leads to ecological tolerance and evolutionary divergence in a polymorphic complex of lichenized fungi. Ann. Botany 114 (2014), 463–475.
Mukhtar, A., Garty, J., Galun, M., Does the lichen alga Trebouxia occur free-living in nature: further immunological evidence. Symbiosis 17 (1994), 247–253.
Nash, T.H. III, Nitrogen, its metabolism and potential contribution to ecosystems. Nash, T.H., (eds.) Lichen biology, 2008, Cambridge University Press, Cambridge, UK, 216–233.
Nelsen, M.P., Gargas, A., Dissociation and horizontal transmission of codispersing lichen symbionts in the genus Lepraria (Lecanorales: Stereocaulaceae). New Phytol. 177 (2008), 264–275.
Nelsen, M.P., Rivas Plata, E., Andrew, C.J., Lücking, R., Lumbsch, H.T., Phylogenetic diversity of trentepohlialean algae associated with lichen-forming fungi. J. Phycol. 47 (2011), 282–290.
O'Brien, H.E., Miadlikowska, J., Lutzoni, F., Assessing population structure and host specialization in lichenized cyanobacteria. New Phytol. 198 (2013), 557–566.
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R, O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, E., Wagner, H., 2018. Vegan: Community Ecology Package. R package version 2.4-6. https://cran.r-project.org/web/packages/vegan/index.html.
Otálora, M.A.G., Martínez, I., O'Brien, H., Molina, M.C., Aragón, G., Lutzoni, F., Multiple origins of high reciprocal symbiotic specificity at an intercontinental spatial scale among gelatinous lichens (Collemataceae, Lecanoromycetes). Mol. Phylogenet. Evol. 56 (2010), 1089–1095.
Otálora, M.A.G., Salvador, C., Martínez, I., Aragón, G., Does the reproductive strategy affect the transmissionand genetic diversity of bionts in cyanolichens? A case study using two closely related species. Microb. Ecol. 65 (2013), 517–530.
Pagel, M., Meade, A., Barker, D., Bayesian estimation of ancestral character states on phylogenies. Syst. Biol. 53 (2004), 673–684.
Paradis, E., Claude, J., Strimmer, K., APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20 (2004), 289–290.
Pardo-De la Hoz, C.J., Magain, N., Lutzoni, F., Goward, T., Restrepo, S., Miadlikowska, J., Contrasting symbiotic patterns in two closely related lineages of trimembered lichens of the genus Peltigera. Front. Microbiol., 9, 2018, 2770, 10.3389/fmicb.2018.02770.
Piercey-Normore, M.D., DePriest, P.T., Algal switching among lichen symbioses. Am. J. Bot. 88 (2001), 1490–1498.
Ranft, H., Moncada, B., De Lange, P., Lumbsch, H.T., Lücking, R., The Sticta filix morphodeme (Ascomycota: Lobariaceae) in New Zealand with the newly recognized species S. dendroides and S. menziesii: indicators of forest health in a threatened island biota?. Lichenologist 50 (2018), 185–210.
Rambold, G., Friedl, T., Beck, A., Photobionts in lichens: possible indicators of phylogenetic relationships?. Bryologist 101 (1998), 392–397.
Sanders, W.B., Pérez-Ortega, S., Nelsen, M.P., Lücking, R., de los Ríos, A., Heveochlorella (Trebouxiophyceae): A little-known genus of unicellular green algae outside the Trebouxiales emerges unexpectedly as a major clade of lichen photobionts in foolicolous communities. J. Phycol. 52 (2016), 840–853.
Schwartz, M.W., Hoeksema, J.D., Specialization and resource trade: biological markets as a model of mutualisms. Ecology 79 (1998), 1029–1038.
Simon, A., Goffinet, B., Magain, N., Sérusiaux, E., High diversity, high insular endemism and recent origin in the lichen genus Sticta (lichenized Ascomycota, Peltigerales) in Madagascar and the Mascarenes. Mol. Phylogenet. Evol. 122 (2018), 15–28.
Singh, G., Dal Grande, F., Divakar, P.K., Otte, J., Crespo, A., Schmitt, I., Fungal-algal association patterns in lichen symbiosis linked to macroclimate. New Phytol. 214 (2017), 317–329.
Škaloud, P., Friedl, T., Hallman, C., Beck, A., Dal Grande, F., Taxonomic revision and species delimitation of coccoid green algae currently assigned to the genus Dictyochloropsis (Trebouxiophyceae, Chlorophyta). J. Phycol. 52 (2016), 599–617.
Smith, D.C., The lichen symbiosis. 1973, Oxford University Press, London.
Smith, D.C., Douglas, A.E., The Biology of Symbiosis. 1987, Edward Arnold, London.
Stamatakis, A., RAxML Version 8: A tool for Phylogenetic Analysis and Post-Analysis of Large Phylogenies. Bioinformatics 30 (2014), 1312–1313.
Steinová, J., Škaloud, P., Yahr, R., Bestová, H., Muggia, L., Reproductive and dispersal strategies shape the diversity of mycobiont-photobiont association in Cladonia lichens. Mol. Phylogenet. Evol. 134 (2019), 226–237.
Tschermak-Woess, E., The algal partner. Galun, M., (eds.) Handbook of lichenology, Vol. I, 1988, CRC Press, Boca Raton, Florida, 39–92.
Thüs, H., Muggia, L., Pérez-Ortega, S., Favero-Longo, S.E., Joneson, S., O'Brien, H., Nelsen, M.P., Duque-Thüs, R., Grube, M., Friedl, T., Brodie, J., Andrew, C.J., Lücking, R., Lutzoni, F., Gueidan, C., Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota). Eur. J. Phycol. 46 (2011), 399–415.
Vančurová, L., Muggia, L., Peksa, O., Řídká, T., Škaloud, P., 2017. The complexity of symbiotic interactions influences the ecological amplitude of the host: A case study in Stereocaulon (lichenized Ascomycota). Mol. Ecol. DOI: 10.1111/mec.14764.
de Vienne, D.M., Giraud, T., Shykoff, J.A., When can host shifts produce congruent host and parasite phylogenies? A simulation approach. J. Evol. Biol. 20 (2007), 1428–1438.
de Vienne, D.M., Refregier, G., Lopez-Villavicencio, M., Tellier, A., Hood, M.E., Giraud, T., Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytol. 198 (2013), 347–385.
Voytsekhovich, A., Dymytrova, L., Nadyeina, O., Photobiont composition of some taxa of the genera Micarea and Placynthiella (Lecanoromycetes, lichenized Ascomycota) from Ukraine. Folia Cryptog. Estonica 48 (2011), 135–148.
Werth, S., Sork, V.L., Ecological specialization in Trebouxia (Trebouxiophyceae) photobionts of Ramalina menziesii (Ramalinaceae) across six range-covering ecoregions of western North America. Am. J. Bot. 101 (2014), 1127–1140.
Widhelm, T.J., Bertoletti, F.R., Aztalos, M.J., Mercado-Díaz, J.A., Huang, J.-P., Moncada, B., Lücking, R., Magain, N., Sérusiaux, E., Goffinet, B., Crouch, N., Mason-Gamer, R., Lumbsch, H.T., Oligocene origin and drivers of diversification in the genus Sticta (Lobariaceae, Ascomycota). Mol. Phylogenet. Evol. 126 (2018), 58–73.
Widhelm, T.J., Grewe, F., Huang, J.P., Mercado, J., Goffinet, B., Lücking, R., Schmitt, I., Moncada, B., Mason-Gamer, R., Lumbsch, H.T., Multiple historical processes obscure phylogenetic relationships in a taxonomically difficult group (Lobariaceae, Ascomycota). Scientific Reports, 9, 2019, 8968.
Wirtz, N., Lumbsch, H.T., Green, T.G.A., Turk, R., Pintado, A., Sancho, L., Schroeter, B., Lichen fungi have low cyanobiont selectivity in maritime Antarctica. New Phytol. 160 (2003), 177–183.
Wornik, S., Grube, M., Joint dispersal does not imply maintenance of partnership in lichen symbioses. Microb. Ecol. 59 (2010), 150–157.
Yahr, R., Vilgalys, R., DePriest, P., Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Mol. Ecol. 13 (2004), 3367–3378.
Yahr, R., Florence, A., Škaloud, P., Voytsekhovich, A., Molecular and morphological diversity in photobionts associated with Micarea s. str. (Lecanorales, Ascomycota). Lichenologist 47 (2015), 403–414.
Yu, Y., Harris, A.J., Blair, C., He, X., RASP (Reconstruct Ancestral State inPhylogenies): a tool for historical biogeography. Mol. Phylogenet. Evol. 87 (2015), 46–49.