Abstract
Photobiont availability is one of the main factors determining the success of the lichenization process. Although multiple sources of photobionts have been proposed, there is no substantial evidence confirming that the substrates on which lichens grow are one of them. In this work, we obtained cyanobacterial 16S ribosomal RNA gene sequences from the substrates underlying 186 terricolous Peltigera cyanolichens from localities in Southern Chile and maritime Antarctica and compared them with the sequences of the cyanobionts of these lichens, in order to determine if cyanobacteria potentially available for lichenization were present in the substrates. A phylogenetic analysis of the sequences showed that Nostoc phylotypes dominated the cyanobacterial communities of the substrates in all sites. Among them, an overlap was observed between the phylotypes of the lichen cyanobionts and those of the cyanobacteria present in their substrates, suggesting that they could be a possible source of lichen photobionts. Also, in most cases, higher Nostoc diversity was observed in the lichens than in the substrates from each site. A better understanding of cyanobacterial diversity in lichen substrates and their relatives in the lichens would bring insights into mycobiont selection and the distribution patterns of lichens, providing a background for hypothesis testing and theory development for future studies of the lichenization process.
Similar content being viewed by others
References
Spribille T, Tuovinen V, Resl P, Vanderpool D, Wolinski H, Aime MC, Schneider K, Stabentheiner E, Toome-Heller M, Thor G, Mayrhofer H, Johannesson H, McCutcheon JP (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353:488–492. doi:10.1126/science.aaf8287
Cardinale M, Vieira de Castro J, Müller H, Berg G, Grube M (2008) In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol Ecol 66:63–71. doi:10.1111/j.1574-6941.2008.00546.x
Grube M, Cardinale M, de Castro JJ, Müller H, Berg G, de Castro JV, Müller H, Berg G (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J 3:1105–1115. doi:10.1038/ismej.2009.63
Hodkinson BP, Gottel NR, Schadt CW, Lutzoni F (2012) Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ Microbiol 14:147–161. doi:10.1111/j.1462-2920.2011.02560.x
Ramírez-Fernández L, Zúñiga C, Carú M, Orlando J (2014) Environmental context shapes the bacterial community structure associated to Peltigera cyanolichens growing in Tierra del Fuego, Chile. World J Microbiol Biotechnol 30:1141–1144. doi:10.1007/s11274-013-1533-8
Cernava T, Berg G, Grube M (2016) High life expectancy of bacteria on lichens. Microb Ecol:1–4. doi:10.1007/s00248–016–0818–5
Aschenbrenner IA, Cernava T, Berg G, Grube M (2016) Understanding microbial multi-species symbioses. Front Microbiol 7:1–9. doi:10.3389/fmicb.2016.00180
Piercey-Normore MD, De Priest PT (2001) Algal switching among lichen symbioses. Am J Bot 88:1490–1498. doi:10.2307/3558457
Yahr R, Vilgalys R, DePriest PT (2004) Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Mol Ecol 13:3367–3378. doi:10.1111/j.1365-294X.2004.02350.x
Hestmark G, Lutzoni F, Miadlikowska J (2016) Photobiont associations in co–occurring umbilicate lichens with contrasting modes of reproduction in coastal Norway. Lichenologist 48:545–557. doi:10.1017/S0024282916000232
Fernández-Martínez MA, de los Ríos A, Sancho LG, Pérez-Ortega S (2013) Diversity of endosymbiotic Nostoc in Gunnera magellanica (L) from Tierra del Fuego, Chile. Microb Ecol 66:335–350. doi:10.1007/s00248–013–0223–2
Cornejo C, Scheidegger C (2016) Cyanobacterial gardens: the liverwort Frullania asagrayana acts as a reservoir of lichen photobionts. Environ Microbiol Rep 8:352–357. doi:10.1111/1758-2229.12386
Gassmann A, Ott S (2000) Growth strategy and the gradual symbiotic interactions of the lichen Ochrolechia frigida. Plant Biol 2:368–378. doi:10.1055/s-2000-3711
Etges S, Ott S (2001) Lichen mycobionts transplanted into the natural habitat. Symbiosis 30:191–206
Fedrowitz K, Kaasalainen U, Rikkinen J (2011) Genotype variability of Nostoc symbionts associated with three epiphytic Nephroma species in a boreal forest landscape. Bryologist 114:220–230. doi:10.1639/0007-2745-114.1.220
Rikkinen J (2015) Cyanolichens. Biodivers Conserv 24:973–993. doi:10.1007/s10531-015-0906-8
Paulsrud P, Rikkinen J, Lindblad P (2001) Field investigations on cyanobacterial specificity in Peltigera aphthosa. New Phytol 152:117–123. doi:10.1046/j.0028-646x.2001.00234.x
Muggia L, Vancurova L, Škaloud P, Peksa O, Wedin M, Grube M (2013) The symbiotic playground of lichen thalli–a highly flexible photobiont association in rock-inhabiting lichens. FEMS Microbiol Ecol 85:313–323. doi:10.1111/1574-6941.12120
Rikkinen J, Oksanen I, Lohtander K (2002) Lichen guilds share related cyanobacterial symbionts. Science 297:357. doi:10.1126/science.1072961
Hedenås H, Ericson L (2004) Aspen lichens in agricultural and forest landscapes: the importance of habitat quality. Ecography 27:521–531. doi:10.1111/j.0906-7590.2004.03866.x
Oksanen I, Lohtander K, Paulsrud P, Rikkinen J (2002) A molecular approach to cyanobacterial diversity in a rock-pool community involving gelatinous lichens and free-living Nostoc colonies. Annales Botanici Fennici 39:93–99
Rikkinen J (2013) Molecular studies on cyanobacterial diversity in lichen symbioses. MycoKeys 6:3–32. doi:10.3897/mycokeys.6.3869
Piercey-Normore MD, Deduke C (2011) Fungal farmers or algal escorts: lichen adaptation from the algal perspective. Mol Ecol 20:3708–3710. doi:10.1111/j.1365-294X.2011.05191.x
Stenroos S, Högnabba F, Myllys L, Hyvönen J, Thell A (2006) High selectivity in symbiotic associations of lichenized ascomycetes and cyanobacteria. Cladistics 22:230–238. doi:10.1111/j.1096-0031.2006.00101.x
Vargas-Castillo R, Beck A (2012) Photobiont selectivity and specificity in Caloplaca species in a fog–induced community in the Atacama Desert, northern Chile. Fungal Biol 116:665–676. doi:10.1016/j.funbio.2012.04.001
Leavitt SD, Kraichak E, Nelsen MP, Altermann S, Divakar PK, Alors D, Esslinger TL, Crespo A, Lumbsch T (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 24:3779–3797. doi:10.1111/mec.13271
Romeike J, Friedl T, Helms G, Ott S (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 19:1209–1217
Wirtz N, Lumbsch HT, Green TGA, Türk R, Pintado A, Sancho L, Schroeter B (2003) Lichen fungi have low cyanobiont selectivity in maritime Antarctica. New Phytol 160:177–183. doi:10.1046/j.1469-8137.2003.00859.x
Domaschke S, Fernández-Mendoza F, García MA, Martín MP, Printzen C (2012) Low genetic diversity in Antarctic populations of the lichen forming ascomycete Cetraria aculeata and its photobiont. Polar Res 31:17353. doi:10.3402/polar.v31i0.17353
Pérez-Ortega S, Ortiz-Álvarez R, TGA G, de Los Ríos A (2012) Lichen myco– and photobiont diversity and their relationships at the edge of life (McMurdo Dry Valleys, Antarctica). FEMS Microbiol Ecol 82:429–448. doi:10.1111/j.1574-6941.2012.01422.x
Peksa O, Škalaoud P (2011) Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Mol Ecol 20:3936–3948. doi:10.1111/j.1365-294X.2011.05168.x
Dal Grande F, Widmer I, Wagner HH, Scheidegger C (2012) Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. Mol Ecol 21:3159–3172. doi:10.1111/j.1365-294X.2012.05482.x
O’Brien HE, Miadlikowska J, Lutzoni F (2013) Assessing population structure and host specialization in lichenized cyanobacteria. New Phytol 198:557–566. doi:10.1111/nph.12165
Orlando J, Zúñiga C, Carú M (2015) Cyanolichens, the choice of the partner determines the success of the relationship (in Spanish). Boletín Antártico Chileno 34:13–16
Magain N, Miadlikowska J, Goffinet B, Sérusiaux E, Lutzoni F (2016) Macroevolution of specificity in cyanolichens of the genus Peltigera section Polydactylon (Lecanoromycetes, Ascomycota). Systematic Biology syw065. doi: 10.1093/sysbio/syw065
Rikkinen J (2009) Relations between cyanobacterial symbionts in lichens and plants. In: Pawlowski K (ed) Prokaryotic Symbionts in Plants, Microbiology Monographs 8. Springer Verlag, Berlin, pp. 265–270
Martínez I, Burgaz AR, Vitikainen O, Escudero A (2003) Distribution patterns in the genus Peltigera Willd. Lichenologist 35:301–323. doi:10.1016/S0024-2829(03)00041-0
Quilhot W, Cuellar M, Díaz R, Riquelme F, Rubio C (2012) Lichens of Aisen, Southern Chile (in Spanish). Gayana Bot 69:57–87
Ramírez-Fernández L, Zúñiga C, Méndez M, Carú M, Orlando J (2013) Genetic diversity of terricolous Peltigera cyanolichen communities in different conservation states of native forest from southern Chile. Int Microbiol 16:243–252. doi:10.2436/20.1501.01.200
Zúñiga C, Leiva D, Ramírez-Fernández L, Carú M, Yahr R, Orlando J (2015) Phylogenetic diversity of Peltigera cyanolichens and their photobionts in Southern Chile and Antarctica. Microbes Environ 30:172–179. doi:10.1264/jsme2.ME14156
Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi:10.1093/nar/gkh340
Penn O, Privman E, Ashkenazy H, Landan G, Graur D, Pupko T (2010) GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Res 38:23–28. doi:10.1093/nar/gkq443
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98. doi:10.1021/bk-1999-0734.ch008
O’Brien H (2013) Another perspective on diversity of symbiotic cyanobacteria: 16S. 10.6084/m9.figshare.806242/. Accessed 28 March 2016
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. doi:10.1080/10635150390235520
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. doi:10.1038/nmeth.2109
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. http://www.phylo.org/. Accessed 28 March 2016
Boc A, Diallo-Alpha B, Makarenkov V (2012) T–REX: a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucleic Acids Res 40:573–579. doi:10.1093/nar/gks485
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180
Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. http://beast.bio.ed.ac.uk/Tracer/. Accessed 28 March 2016
Lefort V, Desper R, Gascuel O (2015) FastME 2.0: a comprehensive, accurate and fast distance–based phylogeny inference program. Mol Biol Evol 32:2798–2800. doi:10.1093/molbev/msv150
Stöver BC, Müller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11:7. doi:10.1186/1471-2105-11-7
Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9. http://purl.oclc.org/estimates. Accessed 13 March 2017
Massana R (2015) Getting specific: making taxonomic and ecological sense of large sequencing data sets. Mol Ecol 24:2904–2906. doi:10.1111/mec.13210
Leiva D, Clavero-León C, Carú M, Orlando J (2016) Intrinsic factors of Peltigera lichens influence the structure of the associated soil bacterial microbiota. FEMS Microbiol Ecol 92:fiw178. doi:10.1093/femsec/fiw178
Elvebakk A, Papaefthimiou D, Robertsen EH, Liaimer A (2008) Phylogenetic patterns among Nostoc cyanobionts within bi- and tripartite lichens of the genus Pannaria. J Phycol 44:1049–1059. doi:10.1111/j.1529-8817.2008.00556.x
Papaefthimiou D, Hrouzek P, Mugnai MA, Lukesova A, Turicchia S, Rasmussen U, Ventura S (2008) Differential patterns of evolution and distribution of the symbiotic behaviour in nostocacean cyanobacteria. Int J Syst Evol Microbiol 58:553–564. doi:10.1099/ijs.0.65312-0
Kaasalainen U, Olsson S, Rikkinen J (2015) Evolution of the tRNALeu (UAA) intron and congruence of genetic markers in lichen-symbiotic Nostoc. PLoS One 10:e0131223. doi:10.1371/journal.pone.0131223
Yahr R, Vilgalys R, DePriest PT (2006) Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytol 171:847–860. doi:10.1111/j.1469-8137.2006.01792.x
Yergeau E, Newsham KK, Pearce DA, Kowalchuk GA (2007) Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environ Microbiol 9:2670–2682. doi:10.1111/j.1462-2920.2007.01379.x
Namsaraev Z, Mano MJ, Fernandez R, Wilmotte A (2010) Biogeography of terrestrial cyanobacteria from Antarctic ice–free areas. Ann Glaciol 51:171–177. doi:10.3189/172756411795931930
Micheli C, Cianchi R, Paperi R, Belmonte A, Pushparaj B (2014) Antarctic cyanobacteria biodiversity based on ITS and trnL sequencing and its ecological implication. Open J Ecol 4:456. doi:10.4236/oje.2014.48039
Manoharan-Basil SS, Miadlikowska J, Goward T, Andresson OS, Miao VP (2016) Peltigera islandica, a new cyanolichen species in section Peltigera (‘P. canina group’). Lichenologist 48:451–467. doi:10.1017/S0024282916000414
Wornik S, Grube M (2010) Joint dispersal does not imply maintenance of partnerships in lichen symbioses. Microb Ecol 59:150–157. doi:10.1007/s00248–009–9584–y
Otálora MAG, Salvador C, Martínez I, Aragón G (2013) Does the reproductive strategy affect the transmission and genetic diversity of bionts in cyanolichens? A case study using two closely related species. Microb Ecol 65:517–530. doi:10.1007/s00248–012–0136–5
Law R, Lewis DH (1983) Biotic environments and the maintenance of sex: some evidence from mutualistic symbioses. Biol J Linnean Soc 20:249–276. doi:10.1111/j.1095-8312.1983.tb01876.x
Acknowledgements
We want to thank J.L. Parraguez, M. Chacón, V. Bauk, A. Kromer, M. Presa, D. Lozano, A. Pradilla, F. Farías, and others from INACH-ECAs 48-49 and BAE Gabriel de Castilla for their fieldwork assistance. In addition, we wish to thank the editor’s and reviewers’ comments for significantly improving previous versions of this work and M. Handford for language support. Finally, we acknowledge the logistical support of the Wildlife Conservation Society Chile (WCS-Chile), Universidad de Magallanes (venue Puerto Williams), Corporación Nacional Forestal (CONAF), and Instituto Antártico Chileno (INACH). The Antarctic campaign was funded by INACH F_02-10 and the experimental procedures by Fondo Nacional de Desarrollo Científico y Tecnológico (FONDECYT) 11100381.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zúñiga, C., Leiva, D., Carú, M. et al. Substrates of Peltigera Lichens as a Potential Source of Cyanobionts. Microb Ecol 74, 561–569 (2017). https://doi.org/10.1007/s00248-017-0969-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-017-0969-z