Skip to main content

Substrates of Peltigera Lichens as a Potential Source of Cyanobionts

Microbial Ecology volume 74, pages 561–569 (2017)Cite this article

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.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  1. 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

    CAS  Article  PubMed  Google Scholar 

  2. 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

    CAS  Article  PubMed  Google Scholar 

  3. 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

    Article  PubMed  Google Scholar 

  4. 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

    CAS  Article  PubMed  Google Scholar 

  5. 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

    Article  PubMed  Google Scholar 

  6. 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

  7. 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

    Article  Google Scholar 

  8. Piercey-Normore MD, De Priest PT (2001) Algal switching among lichen symbioses. Am J Bot 88:1490–1498. doi:10.2307/3558457

    CAS  Article  PubMed  Google Scholar 

  9. 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

    CAS  Article  PubMed  Google Scholar 

  10. 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

    Article  Google Scholar 

  11. 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

    Article  PubMed  Google Scholar 

  12. 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

    CAS  Article  PubMed  Google Scholar 

  13. 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

    Article  Google Scholar 

  14. Etges S, Ott S (2001) Lichen mycobionts transplanted into the natural habitat. Symbiosis 30:191–206

    Google Scholar 

  15. 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

    Article  Google Scholar 

  16. Rikkinen J (2015) Cyanolichens. Biodivers Conserv 24:973–993. doi:10.1007/s10531-015-0906-8

    Article  Google Scholar 

  17. 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

    Article  Google Scholar 

  18. 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

    CAS  Article  PubMed  Google Scholar 

  19. Rikkinen J, Oksanen I, Lohtander K (2002) Lichen guilds share related cyanobacterial symbionts. Science 297:357. doi:10.1126/science.1072961

    CAS  Article  PubMed  Google Scholar 

  20. 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

    Article  Google Scholar 

  21. 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

    CAS  Google Scholar 

  22. Rikkinen J (2013) Molecular studies on cyanobacterial diversity in lichen symbioses. MycoKeys 6:3–32. doi:10.3897/mycokeys.6.3869

    Article  Google Scholar 

  23. 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

    Article  PubMed  Google Scholar 

  24. 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

    Article  Google Scholar 

  25. 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

    Article  PubMed  Google Scholar 

  26. 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

    Article  PubMed  Google Scholar 

  27. 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

    CAS  Article  PubMed  Google Scholar 

  28. 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

    Article  Google Scholar 

  29. 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

    Article  Google Scholar 

  30. 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

    Article  PubMed  Google Scholar 

  31. 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

    Article  PubMed  Google Scholar 

  32. 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

    CAS  Article  PubMed  Google Scholar 

  33. 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

    Article  PubMed  Google Scholar 

  34. 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

    Google Scholar 

  35. 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

  36. 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

    Google Scholar 

  37. 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

    Article  Google Scholar 

  38. Quilhot W, Cuellar M, Díaz R, Riquelme F, Rubio C (2012) Lichens of Aisen, Southern Chile (in Spanish). Gayana Bot 69:57–87

    Article  Google Scholar 

  39. 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

    PubMed  Google Scholar 

  40. 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

    Article  PubMed  PubMed Central  Google Scholar 

  41. Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332

    PubMed  PubMed Central  Google Scholar 

  42. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi:10.1093/nar/gkh340

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 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

    Article  Google Scholar 

  45. 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

    CAS  Article  PubMed  Google Scholar 

  46. 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

    CAS  Google Scholar 

  47. O’Brien H (2013) Another perspective on diversity of symbiotic cyanobacteria: 16S. 10.6084/m9.figshare.806242/. Accessed 28 March 2016

  48. 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

    Article  PubMed  Google Scholar 

  49. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. 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

  51. 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

    Article  Google Scholar 

  52. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180

    CAS  Article  PubMed  Google Scholar 

  53. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. http://beast.bio.ed.ac.uk/Tracer/. Accessed 28 March 2016

  54. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. 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

    Article  PubMed  PubMed Central  Google Scholar 

  56. 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

  57. 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

    Article  PubMed  Google Scholar 

  58. 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

  59. 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

    CAS  Article  PubMed  Google Scholar 

  60. 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

    Article  PubMed  Google Scholar 

  61. 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

    Article  PubMed  PubMed Central  Google Scholar 

  62. 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

    CAS  Article  PubMed  Google Scholar 

  63. 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

    CAS  Article  PubMed  Google Scholar 

  64. 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

    Article  Google Scholar 

  65. 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

    Article  Google Scholar 

  66. 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

    Article  Google Scholar 

  67. 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

    Article  PubMed  Google Scholar 

  68. 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

    Article  PubMed  Google Scholar 

  69. 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

    Article  Google Scholar 

Download references

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

Author notes

  1. Catalina Zúñiga and Diego Leiva contributed equally to this work and are considered joint first authors.

Affiliations

  1. Laboratory of Microbial Ecology, Department of Ecological Sciences, Faculty of Sciences, Universidad de Chile, Las Palmeras 3425, Ñuñoa, Santiago, Chile

    Catalina Zúñiga, Diego Leiva, Margarita Carú & Julieta Orlando

Authors
  1. Catalina Zúñiga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Diego Leiva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Margarita Carú
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Julieta Orlando
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Julieta Orlando.

Electronic supplementary material

ESM 1

(PDF 4236 kb)

ESM 2

(PDF 231 kb)

ESM 3

(PDF 80 kb)

ESM 4

(PDF 51 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-0969-z

Keywords

  • Cyanobacteria
  • Nostoc
  • Peltigera
  • Photobiont availability
  • Terricolous lichens