Morphological and phylogenetic study of algal partners associated with the lichen-forming fungus Porpidia crustulata from the Guancen Mountains, northern China

Symbiosis - Tập 61 - Trang 37-46 - 2013
Bo Li1, Jia Feng1, Shu-lian Xie1
1School of Life Science, Shanxi University, Taiyuan, People’s Republic of China

Tóm tắt

The algal photobiont of the lichen Porpidia crustulata from the Guancen Mountains was successfully cultivated under axenic conditions and tentatively designated as Chlorella sp. GC. The phylogenetic analysis of ribulose bisphosphate carboxylase (rbcL) and internal transcribed spacer (ITS) nucleotide sequence data revealed that this alga is closely related to C. sorokiniana. There are clear morphological differences between Chlorella sp. GC associated with Porpidia crustulata and the free-living C. sorokiniana, the former having a larger central pyrenoid. Based on our genetic and morphological characterization, the Chlorella photobiont of Porpidia crustulata is distinct from closely related Chlorella species.

Tài liệu tham khảo

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, Kasalick T, Rambold G (2002) Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida. New Phytol 153:317–326 Bhattacharya D, Friedl T, Dambergerz S (1996) Nuclear-encoded rDNA Group I introns: origin and phylogenetic relationships of insertion site lineages in the green algae. Mol Biol Evol 13:978–989 Bi LJ, Hu ZY (2004) Flora algarum sinicarum aquae dulcis. Volume VIII. Chlorophyta chlorococcales. Science Press, Beijing, pp 5–32 Bock C, Krienitz L, Pröschold T (2011) Taxonomic reassessment of the genus Chlorella (Trebouxiophyceae) using molecular signatures (barcodes), including description of seven new species. Fottea 11:293–312 Coleman AW (2000) The significance of a coincidence between evolutionary landmarks found in mating affinity and a DNA sequence. Protist 151:1–9 Coleman AW (2003) ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends Genet 19:370–375 De Rijk P, Wuyts J, De Wachter R (2003) RnaViz 2: an improved representation of RNA secondary structure. Bioinformatics 19:299–300 Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:1–15 Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791 Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704 Habetha M, Erxleben FA, Neumann K, Bosch TCG (2003) The Hydra viridis/Chlorella symbiosis. Growth and sexual differentiation in polyps without symbionts. Zoology 106:101–108 Hayden HS, Waaland JR (2002) Phylogenetic systematics of the Ulvaceae (Ulvales, Ulvophyceae) using chloroplast and nuclear DNA sequences. J Phycol 38:1 200–212 Helms G, Friedl T, Rambold G, Mayrhofer H (2001) Identification of photobionts from the lichen family Physciaceae using algal-specific ITS rDNA sequencing. Lichenologist 33:73–86 Honegger R (2000) Simon Schwender (1829–1919) and the dual hypothesis in lichens. Bryologist 103:307–313 Honegger R (2009) Lichen-forming fungi and their photobionts. In: Deising HB (ed) Plant relationships. Springer, Berlin, pp 307–333 Hoshina R, Fujiwara Y (2013) Molecular characterization of Chlorella cultures of the National Institute for Environmental Studies culture collection with description of Micractinium inermum sp. nov., Didymogenes sphaerica sp. nov., and Didymogenes soliella sp. nov. (Chlorellaceae, Trebouxiophyceae). Phycol Res 61:124–132 Hoshina R, Imamura N (2008) Multiple origins of the symbioses in Paramecium bursaria. Protist 159:53–63 Hoshina R, Kamako SI, Imamura N (2004) Phylogenetic position of endosymbiotic green algae in Paramecium bursaria Ehrenberg from Japan. Plant Biol 6:447–453 Huss VA, Sogin ML (1989) Primary structure of the Chlorella vulgaris small subunit ribosomal RNA coding gene. Nucleic Acids Res 17:1255 Huss VAR, Sogin ML (1990) Phylogenetic position of some Chlorella species within the Chlorococcales based upon complete small-subunit ribosomal RNA sequences. J Mol Evol 31:432–442 Huss VAR, Holweg C, Seidel B, Reich V, Rahat M, Kessler E (1994) There is an ecological basis for host/symbiont specificity in Chlorella/Hydra symbioses. Endocytobiosis Cell Res 10:35–46 Huss VAR, Frank C, Hartmann EC, Hirmer M, Kloboucek A, Seidel BM, Wenzeler P, Kessler E (1999) Biochemical taxonomy and molecular phylogeny of the genus Chlorella sensu lato (Chlorophyta). J Phycol 35:587–598 Karakashian MW, Karakashian SJ (1973) Intracellular digestion and symbiosis in Paramecium bursaria. Exp Cell Res 81:111–119 Kawaida H, Ohba K, Koutake Y et al (2013) Symbiosis between Hydra and Chlorella: molecular phylogenetic analysis and experimental study provide insight into its origin and evolution. Mol Phylogenet Evol 66:906–914 Kirk PM, Cannon PF, Minger DW, Stalpers JA (2008) Dictionary of the fungi, 10th edn. CAB International, Oxon Krienitz L, Bock C, Luo W, Pröschold T (2010) Polyphyletic origin of the Dictyosphaerium morphotype within Chlorellaceae (Trebouxiophyceae). J Phycol 46:559–563 Kuhl A, Lorenzen H (1964) Handling and culturing of Chlorclla. Academic, New York, pp 152–187 Lakatos M, Lange-Bertalot H, Budel B (2004) Diatoms living inside the thallus of the green algal lichen Coenogonium linkii in neotropical lowland rain forests. J Phycol 40:70–73 Luo W, Pröschold T, Bock C, Krienitz L (2010) Generic concept in Chlorella-related coccoid green algae (Chlorophyta, Trebouxiophyceae). Plant Biol 12:545–553 Mai JC, Coleman AW (1997) The internal transcribed spacer 2 exhibits a common secondary structure in green algae and flowering plants. J Mol Evol 44:258–271 Manhart JR (1994) Phylogenetic analysis of green plant rbcL sequences. Mol Phylogenet Evol 3:114–127 Muggia L, Zellnig G, Rabensteiner J, Grube M (2010) Morphological and phylogenetic study of algal partners associated with the lichen-forming fungus Tephromela atra from the Mediterranean region. Symbiosis 51:149–160 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 Müller J, Friedl T, Hepperle D et al (2005) Distinction between multiple isolates of Chlorella vulgaris (Chlorophyta, Trebouxiophyceae) and testing for conspecificity using amplified fragment length polymorphism and ITS rDNA sequences. J Phycol 41:1236–1247 Muscatine L, Lenhoff HM (1965) Symbiosis of Hydra and algae. II. Effects of limited food and starvation on growth of symbiotic and aposymbiotic Hydra. The Biol Bull 129:316–328 Nash TH, Ryan BD, Diederich P et al (2004) Lichen flora of the greater sonoran desert region: most of the microlichens, balance of the macrolichens, and the lichenicolous fungi, vol II. Lichens Unlimited, Arizona Nyati S, Beck A, Honegger R (2007) Fine structure and phylogeny of green algal photobionts in the microfilamentous genus Psoroglaena (Verrucariaceae, Lichen-forming ascomycetes). Plant Biol 9:390–399 Opanowicz M, Grube M (2004) Photobiont genetic variation in Flavocetraria nivalis from Poland (Parmeliaceae, Lichenized Ascomycota). Lichenologist 36:125–162 Posada D (2008) Modeltest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256 Pröschold T, Darienko T, Silva PC, Reisser W, Krienitz L (2011) The systematics of Zoochlorella revisited employing an integrative approach. Environ Microbiol 13:350–364 Reisser W, Vietze S, Widowski M (1988) Taxonomic studies on endocytobiotic chlorophycean algae isolated from different American and European strains of Paramecium bursaria. Symbiosis 6:253–270 Rikkinen J (1995) What’s behind the pretty colors? A study on the photobiology of lichens. Bryobrothera 4:1–226 Rippka R, Herdman H (1992) Pasteur culture collection of cyanobacteria: catalogue and taxonomic handbook. Catalogue of strains. Institut Pasteur, Paris 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 Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574 Rosentreter R, Bowker M, Belnap J (2007) A field guide to biological soil crusts of western US drylands: Common lichens and bryophytes. Bureau of Land Management, pp 103 Seckbach J (2002) Symbiosis: mechanisms and model systems. Kluwer Academic Publishers, Dordrecht Shihira I, Krauss RW (1965) Chlorella: physiology and taxonomy of forty-one isolates. University of Maryland Press, Baltimore, pp 30–31 Skaloud P, Peksa O (2010) Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta). Mol Phylogenet Evol 54(1):36–46 Stanier RY, Kunisawa R et al (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35:171 Summerer M, Sonntag B, Sommaruga R (2007) An experimental test of the symbiosis specificity between the ciliate Paramecium bursaria and strains of the unicellular green alga Chlorella. Environ Microbiol 9:2117–2122 Summerer M, Sonntag B, Sommaruga R (2008) Ciliate-symbiont specificity of freshwater endosymbiotic Chlorella (Trebouxiophyceae, Chlorophyta). J Phycol 44:77–84 Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*: and other methods), ver. 4. Sinauer Associates, Massachusetts Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882 Thüs H, Muggia L, Pérez-Ortega S et al (2011) Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota). Eur J Phycol 46:399–415 Tschermak-Woess E (1976) Algal taxonomy and the taxonomy of lichens: the phycobiont of Verrucaria adriatica. Academic, New York, pp 79–88 Tschermak-Woess E (1988) The algal partner. In: Galun M (ed) Handbook of lichenology, vol I. CRC, Boca Raton, pp 39–91 Ueno R, Huss VAR, Urano N et al (2007) Direct evidence for redundant segmental replacement between multiple 18S rRNA genes in a single Prototheca strain. Microbiology 153:3879–3893 Yoshinaga K, Ohta T, Suzuki Y, Sugiura M (1988) Chlorella chloroplast DNA sequence containing a gene for the large subunit of ribulose-1, 5-bisphosphate carboxylase/oxygenase and a part of a possible gene for the β′ subunit of RNA polymerase. Plant Mol Biol 10:245–250 Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415