Abstract
Successful re-lichenization between the two bionts of the lichen symbiosis, the fungal mycobiont and its specific photobiont, is a process that is not well understood yet. To assess potential signalling between the two bionts during initial pre-contact, exudates of the Trebouxia photobionts of Fulgensia bracteata, Fulgensia fulgens, and Xanthoria elegans, of the Asterochloris photobiont of Lecidea lurida, and of the non-lichenizing green alga Myrmecia bisecta were investigated. The compounds identified in these exudates were tested with respect to their influence on germination and early development of the Fulgensia bracteata mycobiont. Additionally, carbohydrates (glucose, sucrose, ribitol) were tested to appraise their effect on the mycobiont growth patterns. Three hypotheses were confirmed: (i) photobionts exude various substances, (ii) the photobiont exudation pattern varies with the identity of the photobiont, and (iii) a pre-contact influence induces changes in the early development of the mycobiont of F. bracteata. This study gives comparative insight to exudates of lichen photobionts. In vitro photobionts differentially release compounds belonging to several substance classes which include indole-3-carbaldehyde, two cyclic dipeptides, and rhamnose. Two compounds had inhibitory effects on germination and germ-tube growth of the mycobiont and one other enhanced spore germination. Additionally, ribitol was found to elicit a strong effect on the mycobiont’s growth. In general, photobiont-exudation, its effect on the mycobiont, and the response to ribitol suggest that complex pre-contact signalling has a crucial role in lichen biont recognition.
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Abbreviations
- CLT:
-
Cyclo-(L-leucyl-L-tyrosyl)
- CTT:
-
Cyclo-(L-tryptophyl-L-tryptophyl)
- EIMS:
-
Electron impact mass spectrometry
- HPLC:
-
High performance liquid chromatography
- IAA:
-
Indole-3-acetic acid
- ICA:
-
Indole-3-carbaldehyde
- ITS rDNA:
-
Internal transcribed spacer ribosomal DNA
- LCMS:
-
Liquid chromatography–mass spectrometry
- MeOH:
-
Methanol
- PPFD:
-
Photosynthetic photon flux density
- Rf :
-
Retardation factor
- TLC:
-
Thin layer chromatography
- TOM:
-
Trebouxia Organic Medium
- UV/VIS:
-
Ultraviolet/visible light
References
Ahmadjian V (1967) A guide to the algae occurring as lichen symbionts: isolation, culture, cultural physiology and identification. Phycologica 6:127–160
Ahmadjian V (1993) The lichen symbiosis. John Wiley & Sons, New York
Ahmadjian V, Jacobs JB (1981) Relationship between fungus and alga in the lichen Cladonia cristatella Tuck. Nature 289(5794):169–172
Ahmadjian V, Jacobs JB, Russell LA (1978) Scanning electron microscope study of early lichen synthesis. Science 200:1062–1064
Arakawa-Kobiyashi S, Kanaseki T (2004) A study of lipid secretion from the lichen symbionts, ascomycetous fungus Myelochroa leucotyliza and green alga Trebouxia sp. J Struct Biol 146:401–415
Bandurski RS, Cohen JD, Slovin JP, Reinecke DM (1995) Auxin biosynthesis and metabolism. In: Davies P (ed) Plant hormones—physiology, biochemistry & molecular biology, 2nd edition. Kluwer Academic Publishers: 44
Beck A (1999) Photobiont inventory of a lichen community growing on heavy-metal rich rock. Lichenologist 31:501–510
Beck A, Friedl T, Rambold G (1998) Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytol 139:709–720
Beck A, Kasalicky G, Rambold G (2002) Myco-photobiontal selection in a mediterranean cryptogram community with Fulgensia fulgens. New Phytol 153:317–326
Bohman-Lindgren G, Ragnarsson U (1972) Chemical studies on lichens—XXXIV. The synthesis of cyclo-(R-β-phenyl-β-alanyl-prolyl)2, a peptide isolated from Roccella canariensis. Tetrahedron 28:4631–4634
Bredenbruch F (2006) Einfluss des Pseudomonas Quinolon Signals auf die interbakterielle Kommunikation von Pseudomonas aeruginosa, Doctoral Thesis. Technische Universität Carolo-Wilhelma: 14
Bubrick P, Galun M, Frensdorff A (1985) Proteins from the lichen Xanthoria parietina which bind to phycobiont cell walls. Isolation and partial purification of an algal-binding protein. Symbiosis 1:85–92
Clayden SR (1998) Thallus initiation and development in the lichen Rhizocarpon lecanorinum. New Phytol 139:685–695
Cordeiro LMC, Sassaki GL, Iacomini M (2007) First report on polysaccharides of Asterochloris and their potential role in the lichen symbiosis. Int J Biol Macromol 41:193–197
Darvill AG, McNeil M, Albersheim P (1978) Structure of plant cell walls. VIII. A new pectic polysaccharide. Plant Physiol 62:418–422
De Priest PR, Piercey-Normore M, Sikaroodi M, Kärkäinen K, Oksanen I, Yahr R, Ahti T (2000) Phylogenetic relationships among sections of Cladonia and Cladina. In: Book of Abstracts, 14. The fourth IAL symposium, progress and problems in lichenology at the turn of the millenium, Barcelona
De Vera JP, Horneck G, Rettberg P, Ott S (2003) The potential of lichen symbiosis to cope with extreme conditions of outer space—I. Influence of UV radiation and space vacuum on the vitality of lichen symbiosis and germination capacity. Int J Astrobiol 1(4):285–293
DNP (2007) Dictionary of Natural Products on CD-ROM, Version 15.1. Chapman & Hall/CRC
Duplessis S, Tagu D, Martin F (2002) Living together underground—a molecular glimpse of the ectomycorrhizal symbiosis. In: Osiewasz HD (ed) Molecular biology of fungal development. Marcel Dekker Inc., New York, pp 302–303
Epstein E, Sagee O, Cohen JD, Garty J (1986) Endogenous auxin and ethylene in the lichen Ramalina duriaei. Plant Physiol 82:1122–1125
Feige GB, Jensen M (1992) Basic carbon and nitrogen metabolism of lichens. In: Reisser W (ed) Algae and symbioses: plants, animals, fungi, viruses, interactions explored. Biopress, Bristol, pp 277–299
Friedl T (1995) Inferring taxonomic positions and testing genus level assignments in coccoid green lichen algae: a phylogenetic analysis of 18S ribosomal sequences from Dictyochloropsis reticulata and from members of the genus Myrmecia (Chlorophyta, Trebouxiophyceae cl. nov.). J Phycol 31:632–639
Friedl T, Büdel B (1996) Photobionts. In: Nash TH (ed) Lichen biology. Cambridge University Press, Cambridge, pp 8–23
Galun M (1988) Lichenization. In: Galun M (ed) Handbook of lichenology, vol II. CRC Press, Boca Raton, pp 153–169
Gazarin IG, Lagrimini LM, Mellon FA, Naldrett MJ, Ashby GA, Thorneley RN (1998) Identification of skatolylhydroperoxide and its role in the peroxidase-catalysed oxidation of indol-3-yl acetic acid. Biochem J 333(1):223–232
Giovanetti M (2002) Survival strategies in arbuscularmycorrhizal symbionts. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer Academic Publishing, Dordrecht, pp 295–305
Hansen SA (1975) Thin-layer chromatographic method for the identification of mono-, di and trisaccharides. J Chromatogr 107:224–226
Hawksworth DL (1988) The variety of fungal-algal symbioses, their evolutionary significance, and the nature of lichens. Bot J Linn Soc 96:3–20
Helms G, Friedl T, Rambold G, Mayrhofer H (2001) Identification of photobionts from lichen family Physciaceae using algal-specific IST rDNA sequencing. Lichenol 33(1):73–86
Henssen A, Jahns HM (1974) Lichenes. Eine Einführung in die Flechtenkunde. Georg Thieme Verlag, Stuttgart
Holden MTG, Chhabra SR, de Nys R, Stead P, Bainton NJ, Hill PJ, Manefield M, Kumar N, Labatte M, England D, Rice S, Givskov M, Salmond GPC, Stewart GSAB, Bycroft BW, Kjelleberg S, Williams P (1999) Quorum sensing cross talk: isolation and chemical characrerization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol Microbiol 33:1254–1266
Honegger R (1998) The lichen symbiosis—what is so spectacular about it? Lichenol 30(3):193–212
Huneck S, Yoshimura I (1996) Identification of lichen substances. 3.2 N-containing substances. Springer-Verlag Berlin, Heidelberg, p 129
Jacobs WP, Falkenstein K, Hamilton RH (1985) Nature and amount of auxin in algae. Plant Physiol 78:844–848
Jahns HM (1988) The lichen thallus. In: Galun M (ed) CRC handbook of lichenology, vol 1. CRC Press, Boca Ranton, pp 95–143
Jimbo M, Usui R, Sakai R, Muramato K, Kamiya H (2007) Purification, cloning and characterization of egg lectins from the teleost Tribolodon brandti. Comp Biochem Physiol B Biochem Mol Biol [Epub ahead of print]
Jonesson S, Armaleo D, Lutzoni F (2011) Fungal and Algal gene expression in early developmental stages of lichen-symbiosis. Mycologia 103(2):291–306
Kardish N, Silberstein L, Fleminger G, Galun M (1991) Lectin from the lichen Nephroma laevigatum Ach. Localization and function. Symbiosis 11:47–62
Klose KE (2006) Increased chatter: cyclic dipeptides as molecules of chemical communication in Vibrio ssp. J Bacteriol 188(6):2025–2026
Kopple KD, Ghazarian HG (1968) A convenient synthesis of 2,5-piperazinediones. J Org Chem 33:862–864
Lallemant R, Bernard T (1977) Obtention de cultures pure des mycosymbiotes du Lobaria laetevirens (Light.) Zahlbr.et du Lobaria pulmonaria (L.) Hoffm.: le role des gonides. Rev Bryol Lichenol 43:303–308
Lawrey JD (1984) Biology of lichenized fungi. Praeger Scientific, New York, p 193
Legaz ME, Fontaniella B, Millanes AM, Vicente C (2004) Secreted arginases from phylogenetically far related lichen species act as cross-regocnition factors for two different algae. Eur J Cell Biol 83:1–12
Lehr H, Galun M, Ott S, Jahns HM, Fleminger G (2000) Cephalodia of the lichen Peltigera aphthosa (L.) Willd. Specific recognition of the compatible photobiont. Symbiosis 29:357–365
Lockhart CM, Rowell P, Stewart WDP (1978) Phytohemagglutinins from the nitrogen-fixing lichens Peltigeracanina and P. polydactyla. FEMS Microbiol Lett 3:127–130
Long SR (1996) Rhizobium symbiosis. Nod factors in perspective. Plant Cell 8:1885–1898
Marcuccio SM, Elix JA (1983) A structural revision of picroroccellin. Tetrahedron 24:1445–1448
Martins MB, Carvalho I (2007) Diketopiperazines: biological activity and synthesis. Tetrahedron 63:9923–9932
Mc Kay MJ, Caroll AR, Quinn RJ, Hooper JN (2002) 1,2-bis(1H-indol-3-yl)ethane-1,2-dione, an indole alkaloid from the marine sponge Smenospongia sp. J Nat Prod 65(4):595–597
Miao VPW, Manoharan SS, Snæbjarnarson V, Andrésson ÓS (2012) Expression of lec-1, a mycobiont gene encoding a galectin-like protein in the lichen Peltigera membranacea. Symbiosis. doi:10.1007/s13199-012-0175-1
Milne PJ, Hunt AL, Rostoll K, Van der Walt JJ, Graz CJ (1998) The biological activity of selected cyclic dipeptides. J Pharm Pharmacol 50(12):1331–1337
Molina MC, Muñiz E, Vicente C (1993) Enzymatic activities of algal-binding protein and its algal cell wall receptor in the lichen Xanthoria parietina. An approach to the parasitic basis of mutualism. Plant Physiol Biochem 31:131–142
Mosbach K (1973) Biosynthesis of lichen substances. In: Ahmadjian V, Hale ME (eds) The lichens. Academic Press, New York, p 540
Nelsen MP, Gargas A (2006) Actin type I introns offer potential for increasing phylogenetic resolution in Asterochloris (Chlorophyta: Trebouxiophyceae). Lichenol 38(5):435–440
Okamato M, Tsutsui S, Tasumi S, Suetake H, Kikuchi K, Suzuki Y (2005) Tandem repeat L-rhamnose-binding lectin from the skin mucus of ponyfish, Leiognathus nuchalis. Biochem Biophys Res Commun 333(2):463–469
Olvera C, Goldberg JB, Sanchez R, Soberon-Chavez G (1999) The Pseudomonas aeruginosa algC gene product participates in rhamnolipid biosynthesis. FEMS Microbiol Lett 179(1):85–90
Ott S (1987) Sexual reproduction and developmental adaptations in Xanthoria parietina. Nord J Bot 7:219–228
Ott S, Meier T, Jahns HM (1995) Development, regeneration, and parasitic interactions between the lichens Fulgensia bracteata and Toninia caerulonigricans. Can J Bot 73(suppl 1):595–602
Ott S, Krieg T, Spanier U, Schieleit P (2000) Phytohormones in lichens with emphasis on ethylene biosynthesis and functional aspects on lichen symbiosis. Phyton 40:83–94
Papin JP, Udiman M (1975) Chromatographie sur couche mince des polyols. J Chromat 115:267–272
Rai AN, Söderbäck E, Bergmann B (2000) TansleyReview No. 116. Cyanobacterium-plant symbioses. New Phytol 147:449–481
Remmer SV, Ahmadjian V, Livdahl TP (1986) Effects of IAA (indole-3-acetic acid) and kinetin (6-furfurylamino-purine) on the synthetic lichen Cladonia cristatella and its isolated bionts. Lichen Physiol Biochem 1:1–15
Rezanka T, Gushina IA (2000) Glycosidic compounds of murolic, protocontipatic and allo-murolic acids from lichens of Central Asia. Phytochemistry 54:635–645
Rezanka T, Gushina IA (2001a) Glycosides esters fromlichens of Central Asia. Phytochemistry 58:509–516
Rezanka T, Gushina IA (2001b) Macrolactones glycosides of three lichen acids from Acarospora gobiensis, a lichen of Central Asia. Phytochemistry 58:1281–1287
Richardson DHS (1973) Photosynthesis and carbohydrate movement. In: Ahmadjian V, Hale ME (eds) The lichens. Academic Press, New York, pp 249–288
Richardson DHS, Hill DH, Smith DC (1968) Lichen physiology. XI. The role of the alga in determining the pattern of carbohydrate movement between lichen symbionts. New Phytol 67:469–486
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(8):1209–1215
Schaper GM, Ott S (2003) Photobiont selectivity and interspecific interactions in lichen communities. Plant Biol 5:441–450
Schwarz RA, Hodes-Villamar L, Fitzpatrick K, Fain MG, Hughes AL, Cadavid LF (2007) A gene family of putative immune recognition molecules in the hydroid Hydractinia. Immunogenetics 59(3):233–246
Scott GD (1973) Evolutionary aspects of symbiosis. In: Ahmadjian V, Hale ME (eds) The lichens. Academic Press, New York, pp 587–588
Skorpil P, Broughton WJ (2006) Molecular interactions between Rhizobium and Legumes. In: Overmann J (ed) Molecular basis of symbiosis. Springer-Verlag, Berlin, pp 143–156
Tan J, Bednarek P, Liu J, Schneider B, Svatos A, Hahlbrock K (2004) Universally occuring phenylpropanoid and species-specific indolic metabolites in infected and uninfected Arabidopsis thaliana roots and leaves. Phytochemistry 65(6):691–699
Tateno H, Ogawa T, Muramato K, Kamiya H, Saneyoshi M (2002) Distribution and molecular evolution of rhamnose-binding lectins in Salmonidae: isolation and characterization of two lectins from white-spotted charr (Salvelinus leucomaenis) eggs. Biosci Biotechnol Biochem 66(6):1356–1365
Wu SJ, Fotso S, Li F, Qin S, Laatsch H (2007) Amorphane sesquiterpenes from a marine Streptomyceces sp. J Nat Prod 70(2):304–306
Yahr R, Vilgalys R, De Priest PT (2004) Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Mol Ecol 13:3367–3378
Yoshida Y, Ganguly S, Bush CA, Cisar JO (2006) Molecular basis of L-rhamnose branch formation in streptococcal coaggregation polysaccharides. J Bacteriol 188(11):4125–4130
Yoshimura I, Yamamoto Y, Nakano T, Finnie J (2002) Isolation and culture of lichen photobionts and mycobionts. In: Krammer I, Beckett R, Varma A (eds) Protocols in lichenology. Culturing, biochemistry, ecophysiology and use in biomonitoring. Springer-Verlag, Berlin, pp 3–33
Acknowledgments
Our special thanks are due to the members of the Institute of Pharmaceutical Biology and Biotechnology (HHU Düsseldorf) for their friendly and invaluable support, namely Pharmacist Julia Kjer, Dr. Ru Angelie Edrada-Ebel, and Prof. Dr. Reinhard Ebel. We thank Ralf Bürgel from the Institute of Inorganic and Structural Chemistry (HHU Düsseldorf) for EIMS-analysis and the group of Prof. M. Braun at the Institute of Organic and Makromolecular Chemistry (HHU Düsseldorf) for the synthesis of cyclo-(leu-tyr). Thanks are also due to the anonymous reviewers for their helpful comments. Finally, the authors are very grateful for financial support by the Düsseldorf Entrepreneurs Foundation. The results are included in the doctoral thesis of Joachim Meeßen.
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Dedicated to Margalith Galun. In honour of her inspiring work.
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Meeßen, J., Eppenstein, S. & Ott, S. Recognition mechanisms during the pre-contact state of lichens: II. Influence of algal exudates and ribitol on the response of the mycobiont of Fulgensia bracteata . Symbiosis 59, 131–143 (2013). https://doi.org/10.1007/s13199-012-0219-6
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DOI: https://doi.org/10.1007/s13199-012-0219-6