1887

Abstract

Recent progress in molecular techniques has begun to alter traditional recognition of lichens as symbiotic organisms comprised of a fungus and photosynthetic partners (green algae and/or cyanobacteria). Diverse organisms, especially various non-photosynthetic bacteria, are now indicated to be integral components of lichen symbiosis. Although lichen-associated bacteria are inferred to have functions that could support the symbiosis, little is known about their physical and nutritional interaction with fungi and algae. In the present study, we identified specific interaction between a lichen-forming alga and a novel bacterium. alga was isolated from a lichen, , and kept as a strain for 8 years. Although no visible bacterial colonies were observed in this culture, high-throughput sequencing of DNA isolated from the culture revealed that the strain is composed of a alga and an species. hybridization showed that bacterial cells were localized on the surface of the algal cells. Physiological assays revealed that the bacterium was able to use ribitol, glucose and mannitol, all of which are known to exist abundantly in lichens. It was resistant to three antibiotics. Bacteria closely related to this species were also identified in lichen specimens, indicating that may commonly associate with this group of bacteria. These features of the novel bacterium suggest that it may be involved in carbon cycling of as a member of lichen symbiosis and less likely to have become associated with the alga after isolation from a lichen.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000461
2017-05-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/163/5/678.html?itemId=/content/journal/micro/10.1099/mic.0.000461&mimeType=html&fmt=ahah

References

  1. Nash TH. Lichen Biology, 2nd ed. New York: Cambridge University Press; 2008 [CrossRef]
    [Google Scholar]
  2. Grube M, Cardinale M, de Castro JV Jr, Müller H, Berg G. Species-specific structural and functional diversity of bacterial communities in lichen symbioses. Isme J 2009; 3:1105–1115 [View Article][PubMed]
    [Google Scholar]
  3. Farrar J. The lichen as an ecosystem: observation and experiment. Lichenology: Progress and Problems London: Academic Press; 1976 pp. 385–406
    [Google Scholar]
  4. Spribille T, Tuovinen V, Resl P, Vanderpool D, Wolinski H et al. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 2016; 353:488–492 [View Article][PubMed]
    [Google Scholar]
  5. Uphof JC. Purple bacteria as symbionts of a lichen. Science 1925; 61:67 [View Article][PubMed]
    [Google Scholar]
  6. Aschenbrenner IA, Cernava T, Berg G, Grube M. Understanding microbial multi-species symbioses. Front Microbiol 2016; 7:180 [View Article][PubMed]
    [Google Scholar]
  7. Sigurbjörnsdóttir MA, Andrésson ÓS, Vilhelmsson O. Nutrient scavenging activity and antagonistic factors of non-photobiont lichen-associated bacteria: a review. World J Microbiol Biotechnol 2016; 32:68 [View Article][PubMed]
    [Google Scholar]
  8. Cardinale M, Puglia AM, Grube M. Molecular analysis of lichen-associated bacterial communities. FEMS Microbiol Ecol 2006; 57:484–495 [View Article][PubMed]
    [Google Scholar]
  9. Bates ST, Cropsey GW, Caporaso JG, Knight R, Fierer N. Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 2011; 77:1309–1314 [View Article][PubMed]
    [Google Scholar]
  10. Grube M, Cernava T, Soh J, Fuchs S, Aschenbrenner I et al. Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics. Isme J 2015; 9:412–424 [View Article][PubMed]
    [Google Scholar]
  11. Sigurbjörnsdóttir MA, Andrésson ÓS, Vilhelmsson O. Analysis of the Peltigera membranacea metagenome indicates that lichen-associated bacteria are involved in phosphate solubilization. Microbiology 2015; 161:989–996 [View Article][PubMed]
    [Google Scholar]
  12. Cardinale M, Vieira de Castro J, Müller H, Berg G, Grube M. In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of alphaproteobacteria. FEMS Microbiol Ecol 2008; 66:63–71 [View Article][PubMed]
    [Google Scholar]
  13. Hodkinson BP, Gottel NR, Schadt CW, Lutzoni F. Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ Microbiol 2012; 14:147–161 [View Article][PubMed]
    [Google Scholar]
  14. Liba CM, Ferrara FI, Manfio GP, Fantinatti-Garboggini F, Albuquerque RC et al. Nitrogen-fixing chemo-organotrophic bacteria isolated from cyanobacteria-deprived lichens and their ability to solubilize phosphate and to release amino acids and phytohormones. J Appl Microbiol 2006; 101:1076–1086 [View Article][PubMed]
    [Google Scholar]
  15. Printzen C, Fernández-Mendoza F, Muggia L, Berg G, Grube M. Alphaproteobacterial communities in geographically distant populations of the lichen Cetraria aculeata. FEMS Microbiol Ecol 2012; 82:316–325 [View Article][PubMed]
    [Google Scholar]
  16. Fuentes JL, Garbayo I, Cuaresma M, Montero Z, González-del-Valle M et al. Impact of microalgae-bacteria interactions on the production of algal biomass and associated compounds. Mar Drugs 2016; 14:100 [View Article][PubMed]
    [Google Scholar]
  17. Ramanan R, Kim BH, Cho DH, Hm O, Kim HS et al. Algae-bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv 2016; 34:14–29 [CrossRef]
    [Google Scholar]
  18. Amin SA, Green DH, Hart MC, Küpper FC, Sunda WG et al. Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism. Proc Natl Acad Sci USA 2009; 106:17071–17076 [View Article][PubMed]
    [Google Scholar]
  19. Croft MT, Warren MJ, Smith AG. Algae need their vitamins. Eukaryot Cell 2006; 5:1175–1183 [View Article][PubMed]
    [Google Scholar]
  20. Kazamia E, Czesnick H, Nguyen TT, Croft MT, Sherwood E et al. Mutualistic interactions between vitamin B12-dependent algae and heterotrophic bacteria exhibit regulation. Environ Microbiol 2012; 14:1466–1476 [View Article][PubMed]
    [Google Scholar]
  21. Watanabe K, Takihana N, Aoyagi H, Hanada S, Watanabe Y et al. Symbiotic association in chlorella culture. FEMS Microbiol Ecol 2005; 51:187–196 [View Article][PubMed]
    [Google Scholar]
  22. Biosca EG, Flores R, Santander RD, Díez-Gil JL, Barreno E. Innovative approaches using lichen enriched media to improve isolation and culturability of lichen associated bacteria. PLoS One 2016; 11:e0160328 [View Article][PubMed]
    [Google Scholar]
  23. Kon Y, Kashiwadani H, Masada M, Tamura G. Artificial syntheses of mycobionts of Usnea confusa ssp. kitamiensis and Usnea orientalis with their natural and nonnatural phycobiont. J Jpn Bot 1993; 68:129–137
    [Google Scholar]
  24. Ichimura T. editor Sexual cell division and conjugation-papilla formation in sexual reproduction of Closterium strigosum. International Symposium on Seaweed Research, 7th, Sapporo Tokyo: University of Tokyo Press; 1971
    [Google Scholar]
  25. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article][PubMed]
    [Google Scholar]
  26. Helms G, Friedl T, Rambold G, Mayrhofer H. Identification of photobionts from the lichen family Physciaceae using algal-specific ITS rDNA sequencing. Lichenologist 2001; 33:73–86 [View Article]
    [Google Scholar]
  27. Friedl T, Rokitta C. Species relationships in the lichen alga Trebouxia (Chlorophyta, Trebouxiophyceae): molecular phylogenetic analyses of nuclear-encoded large subunit rRNA gene sequences. Symbiosis 1997; 23:125–148
    [Google Scholar]
  28. Ohmura Y, Kawachi M, Kasai F, Watanabe MM, Takeshita S. Genetic combinations of symbionts in a vegetatively reproducing lichen, Parmotrema tinctorum, based on ITS rDNA sequences. Bryologist 2006; 109:43–59 [View Article]
    [Google Scholar]
  29. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  30. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425[PubMed]
    [Google Scholar]
  31. Tanabe H, Müller S, Neusser M, von Hase J, Calcagno E et al. Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates. Proc Natl Acad Sci USA 2002; 99:4424–4429 [View Article][PubMed]
    [Google Scholar]
  32. Kawamura R, Tanabe H, Wada T, Saitoh S, Fukushima Y et al. Visualization of the spatial positioning of the SNRPN, UBE3A, and GABRB3 genes in the normal human nucleus by three-color 3D fluorescence in situ hybridization. Chromosome Res 2012; 20:659–672 [View Article][PubMed]
    [Google Scholar]
  33. Gish W, States DJ. Identification of protein coding regions by database similarity search. Nat Genet 1993; 3:266–272 [View Article][PubMed]
    [Google Scholar]
  34. Beck A, Divakar PK, Zhang N, Molina MC, Struwe L. Evidence of ancient horizontal gene transfer between fungi and the terrestrial alga Trebouxia. Org Divers Evol 2015; 15:235–248 [View Article]
    [Google Scholar]
  35. Richardson DHS, Smith DC, Ix LP. Lichen physiology. IX. carbohydrate movement from the Trebouxia symbiont of Xanthoria aureola to the fungus. New Phytologist 1968; 67:61–68 [View Article]
    [Google Scholar]
  36. Aubert S, Juge C, Boisson AM, Gout E, Bligny R. Metabolic processes sustaining the reviviscence of lichen Xanthoria elegans (Link) in high mountain environments. Planta 2007; 226:1287–1297 [View Article][PubMed]
    [Google Scholar]
  37. Richardson DHS, Smith DC. Lichen physiology. X. The isolated algal and fungal symbionts of Xanthoria aureola. New Phytologist 196869–77 [CrossRef]
    [Google Scholar]
  38. Lines CEM, Ratcliffe RG, Rees TAV, Southon TE. A 13C NMR study of photosynthate transport and metabolism in the lichen Xanthoria calcicola oxner. New Phytologist 1989; 111:447–456 [View Article]
    [Google Scholar]
  39. Lewis DH, Smith DC. Sugar alcohols (polyols) in fungi and green plants II. New Phytologist 1967; 66:185–204 [CrossRef]
    [Google Scholar]
  40. Tysiaczny M, Kershaw K. Physiological-environmental interactions in lichens. VII. The environmental control of glucose movement from alga to fungus in Peltigera canina v. Praetextata hue. New Phytologist 1979; 83:137–146 [CrossRef]
    [Google Scholar]
  41. Hill DJ. The movement of carbohydrate from the alga to the fungus in the lichen Peltigera polydactyla. New Phytologist 1972; 71:31–39 [View Article]
    [Google Scholar]
  42. Drew EA, Smith DC. Studies in the physiology of lichens. VIII. Movement of glucose from alga to fungus during photosynthesis in the thallus of Peltigera polydactyla. New Phytologist 1967; 66:389–400 [CrossRef]
    [Google Scholar]
  43. Negm FB, Loescher WH. Detection and characterization of sorbitol dehydrogenase from apple callus tissue. Plant Physiol 1979; 64:69–73 [View Article][PubMed]
    [Google Scholar]
  44. Sashidhar B, Podile AR. Mineral phosphate solubilization by rhizosphere bacteria and scope for manipulation of the direct oxidation pathway involving glucose dehydrogenase. J Appl Microbiol 2010; 109:1–12 [View Article][PubMed]
    [Google Scholar]
  45. Chhabra S, Brazil D, Morrissey J, Burke JI, O'Gara F et al. Characterization of mineral phosphate solubilization traits from a barley rhizosphere soil functional metagenome. Microbiologyopen 2013; 2:717–724 [View Article][PubMed]
    [Google Scholar]
  46. Schneider T, Schmid E, de Castro JV, Cardinale M, Eberl L et al. Structure and function of the symbiosis partners of the lung lichen (Lobaria pulmonaria L. Hoffm.) analyzed by metaproteomics. Proteomics 2011; 11:2752–2756 [View Article][PubMed]
    [Google Scholar]
  47. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 2000; 407:81–86 [View Article][PubMed]
    [Google Scholar]
  48. Moran NA, Degnan PH. Functional genomics of Buchnera and the ecology of aphid hosts. Mol Ecol 2006; 15:1251–1261 [View Article][PubMed]
    [Google Scholar]
  49. Bourque DP, Mc Millan P, Clingenpeel WJ, Naylor AW. Comparative effects of several inhibitors of chloroplast thylakoid membrane synthesis in greening jack bean. Bot Gaz 1976; 137:279–284 [View Article]
    [Google Scholar]
  50. Bashir KM, Cho MG. The effect of kanamycin and tetracycline on growth and photosynthetic activity of two chlorophyte algae. Biomed Res Int 2016; 2016:1–8 [View Article]
    [Google Scholar]
  51. Mentewab A, Matheson K, Adebiyi M, Robinson S, Elston B. RNA-seq analysis of the effect of kanamycin and the ABC transporter AtWBC19 on Arabidopsis thaliana seedlings reveals changes in metal content. PLoS One 2014; 9:e109310 [View Article][PubMed]
    [Google Scholar]
  52. Cardinale M, Steinová J, Rabensteiner J, Berg G, Grube M. Age, sun and substrate: triggers of bacterial communities in lichens. Environ Microbiol Rep 2012; 4:23–28 [View Article][PubMed]
    [Google Scholar]
  53. Cernava T, Müller H, Aschenbrenner IA, Grube M, Berg G. Analyzing the antagonistic potential of the lichen microbiome against pathogens by bridging metagenomic with culture studies. Front Microbiol 2015; 6:620 [View Article][PubMed]
    [Google Scholar]
  54. Eisenreich W, Knispel N, Beck A. Advanced methods for the study of the chemistry and the metabolism of lichens. Phytochem Rev 2011; 10:445–456 [View Article]
    [Google Scholar]
  55. Kosanić M, Ranković B. Lichen secondary metabolites. In Ranković B. (editor) Lichen Secondary Metabolites Springer; 2015 pp. 81–104
    [Google Scholar]
  56. Kon Y, Kashiwadani H, Kurokawa S. Induction of lichen thalli of Usnea confusa asah. ssp. kitamiensis asah.) asah. in vitro. J Jpn Bot 1990; 65:26–32
    [Google Scholar]
  57. Hill DJ, Smith DC. Lichen physiology XII. The ‘inhibition technique’. New Phytologist 1972; 71:15–30 [CrossRef]
    [Google Scholar]
  58. Aschenbrenner IA, Cardinale M, Berg G, Grube M. Microbial cargo: do bacteria on symbiotic propagules reinforce the microbiome of lichens?. Environ Microbiol 2014; 16:3743–3752 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000461
Loading
/content/journal/micro/10.1099/mic.0.000461
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error