Nocardia casuarinae sp. nov., an actinobacterial endophyte isolated from root nodules of Casuarina glauca

Abstract

An actinobacterium strain BMG51109a was isolated from surface sterilized root nodules of Casuarina glauca collected in Tunisia. The 16S rRNA gene sequence of strain BMG51109a showed most similarity (96.53–96.55 %) to the type strains of Nocardia transvalensis, N. aobensis and N. elegans. Chemotaxonomic analysis supported the assignment of the strain to Nocardia genus. The major menaquinone was MK-8(H4c) while the polar lipid profile contained diphosphatidylglycerol, phosphatidylmonomethylethanolamine, glycophospholipid, phosphatidylinositol, one uncharacterized phospholipid and three glycolipids. Whole-cell sugar analysis revealed the presence of meso-diaminopimelic acid, arabinose and galactose as diagnostic sugars, complemented by glucose, mannose and ribose. The major cellular fatty acids were tuberculostearic, oleic, palmitoleic and stearic acids. Physiological and biochemical tests showed that strain BMG51109a could be clearly distinguished from its closest phylogenetic neighbours. On the basis of these results, strain BMG51109aT (= DSM 45978T = CECT 8469T) is proposed as the type strain of the novel species Nocardia casuarinae sp. nov.

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References

  1. Aoki H, Sakai H, Kohsaka M, Konomi T, Hosoda J (1976) Nocardicin A, a new monocyclic beta-lactam antibiotic I Discovery, isolation and characterization. J Antibiot 29:492–500

    CAS  PubMed  Article  Google Scholar 

  2. Baker D, O’Keefe D (1984) A modified sucrose fractionation procedure for the isolation of frankiae from actinorhizal root nodules and soil samples. Plant Soil 78:23–28

    Article  Google Scholar 

  3. Beaman BL, Beaman L (1994) Nocardia species: host-parasite relationships. Clin Microbiol Rev 7:213

    CAS  PubMed Central  PubMed  Google Scholar 

  4. Boiron P, Provost F, Dupont B (1993) Laboratory methods for the diagnosis of nocardiosis. Institut Pasteur, Paris 180

    Google Scholar 

  5. Brown-Elliott BA, Brown JM, Conville PS, Wallace RJ (2006) Clinical and laboratory features of the Nocardia spp based on current molecular taxonomy. Clin Microbiol Rev 19:259–282

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  6. Chapin KC, Murray PR (1999) Stains. In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH (eds) Manual of clinical microbiology. American Society for Microbiology, Washington, DC, p 1678

    Google Scholar 

  7. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37((Database issue)):D141–145. doi:10.1093/nar/gkn879

  8. Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230

    CAS  PubMed  Article  Google Scholar 

  9. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    CAS  PubMed  Article  Google Scholar 

  10. Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol 20:406–416

    Article  Google Scholar 

  11. Ghodhbane-Gtari F, Tisa LS (2014) Ecology and physiology of non-frankia actinobacteria from actinorhizal plants. Plasticity in plant-growth-promoting and phytopathogenic bacteria. Springer, New York, pp 27–42

    Google Scholar 

  12. Ghodhbane-Gtari F, Essoussi I, Chattaoui M, Chouaia B, Jaouani A, Daffonchio D, Boudabous A, Gtari M (2010) Isolation and characterization of non-Frankia actinobacteria from root nodules of Alnus glutinosa, Casuarina glauca and Elaeagnus angustifolia. Symbiosis 50:51–57

    CAS  Article  Google Scholar 

  13. Goodfellow M (1998) Nocardia and related genera. Topley and Wilson’s microbiology and microbial infections, 9th edn. Edward Arnold, London, pp 463–489

    Google Scholar 

  14. Goodfellow M, Maldonado LA (2010) Genus 1 Nocardia Trevisan 1889AL. In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology: the actinobacteria Part A, vol 5, 2nd edn. Springer, New York, pp 376–419

    Google Scholar 

  15. Gordon RE, Barnett DA, Handerhan JE, Pang CHN (1974) Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Bacteriol 24:54–63

    Article  Google Scholar 

  16. Hoshino Y, Mukai A, Yazawa K, Uno J, Ishikawa J, Ando A, Mikami Y (2004) Transvalencin A, a thiazolidine zinc complex antibiotic produced by a clinical isolate of Nocardia transvalensis I Taxonomy, fermentation, isolation and biological activities. J Antiobiot 57:797–802

    CAS  Article  Google Scholar 

  17. Hoshino Y, Watanabe K, Iida S, Suzuki SI, Kudo T, Kogure T, Mikami Y (2007) Nocardia terpenica sp nov, isolated from Japanese patients with nocardiosis. Int J Syst Evol Microbiol 57:1456–1460

    PubMed  Article  Google Scholar 

  18. Hosoda J, Konomi T, Tani N, Aoki H, Imanaka H (1977) Isolation of new nocardicins from Nocardia uniformis subsp tsuyamanensis Agri. Biol Chem 41:2013–2020

    CAS  Google Scholar 

  19. Kaewkla O, Franco CM (2010) Nocardia callitridis sp nov, an endophytic actinobacterium isolated from a surface-sterilized root of an Australian native pine tree. J Syst Evol Microbiol 60:1532–1536

    CAS  Article  Google Scholar 

  20. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120

    CAS  PubMed  Article  Google Scholar 

  21. Kinoshita N, Homma Y, Igarashi M, Ikeno S, Hori M, Hamada M (2001) Nocardia vinacea sp. nov. Actinomycetologica 15:1–5

    CAS  Article  Google Scholar 

  22. Klatte S, Kroppenstedt RM, Rainey FA (1994) Rhodococcus opacus sp. nov., an unusual nutritionally versatile Rhodoccus species. Syst Appl Microbiol 17:355–360

    Article  Google Scholar 

  23. Kroppenstedt RM (1982) Separation of bacterial menaquinones by HPLC using reverse phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chromatogr 5:2359–2367

    CAS  Article  Google Scholar 

  24. Kroppenstedt RM, Goodfellow M (2006) The family Thermomonosporaceae: Actinocorallia, Actinomadura, Spirillospora and Thermomonospora. The prokaryotes, vol 3. Springer, New York, pp 682–724

    Google Scholar 

  25. Lechevalier MP, Lechevalier H (1970) Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol 20:435–443

    CAS  Article  Google Scholar 

  26. McNeil MM, Brown JM (1994) The medically important aerobic actinomycetes: epidemiology and microbiology. Clin Microbiol Rev 7:357

    CAS  PubMed Central  PubMed  Google Scholar 

  27. Meier-Kolthoff JP, Göker M, Spröer C, Klenk HP (2013) When should a DDH experiment be mandatory in microbial taxonomy? Arch Microbiol 195:413–418

    CAS  PubMed  Article  Google Scholar 

  28. Minnikin DE, O’donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241

    CAS  Article  Google Scholar 

  29. Nemoto A, Hoshino Y, Yazawa K, Ando A, Mikami Y, Komaki H, Graefe U (2002) Asterobactin, a new siderophore group antibiotic from Nocardia asteroids. J Antibiot 55:593–597

    CAS  PubMed  Article  Google Scholar 

  30. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  31. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 20:1–6

    Google Scholar 

  32. Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407

    CAS  PubMed Central  PubMed  Google Scholar 

  33. Shirling EB, Gottlieb D (1966) Methods for characterization of streptomyces species. Int J Syst Bacteriol 16:313–340

    Article  Google Scholar 

  34. Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 28:226–231

    CAS  PubMed Central  PubMed  Google Scholar 

  35. Sun W, Zhang YQ, Huang Y, Zhang YQ, Yang ZY, Liu ZH (2009) Nocardia jinanensis sp nov, an amicoumacin B-producing actinomycete. Int J Syst Evol Microbiol 59:417–420

    CAS  PubMed  Article  Google Scholar 

  36. 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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  37. Tanaka Y, Komaki H, Yazawa K, Mikami Y, Nemoto A, Tojyo T, Kadowaki K, Shigemori H, Kobayashi J (1997) Brasilinolide A, a new macrolide antibiotic produced by Nocardia brasiliensis: producing strain, isolation and biological activity. J Antibiot 50:1036–1041

    CAS  PubMed  Article  Google Scholar 

  38. Xing K, Qin S, Fei SM, Lin Q, Bian GK, Miao Q, Li WJ (2011) Nocardia endophytica sp. nov., an endophytic actinomycete isolated from the oil-seed plant Jatropha curcas L. Int J Syst Evol Microbiol 61:1854–1858

    CAS  PubMed  Article  Google Scholar 

  39. Zhao GZ, Li J, Zhu WY, Klenk HP, Xu LH, Li WJ (2011) Nocardia artemisiae sp. nov., an endophytic actinobacterium isolated from a surface-sterilized stem of Artemisia annua L. Int J Syst Evol Microbiol 61:2933–2937

    CAS  PubMed  Article  Google Scholar 

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Acknowledgments

The authors would like to gratefully acknowledge Prof. Manfred Rohde (Helmholz Centre for Infection Biology, Braunschweig, Germany) for providing the Scanning EM Photo in Fig. 2b. This research was supported by The Ministère de l’Enseignement Supérieur et de la Recherche Scientifique, Tunisie.

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Correspondence to Maher Gtari.

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Ghodhbane-Gtari, F., Nouioui, I., Salem, K. et al. Nocardia casuarinae sp. nov., an actinobacterial endophyte isolated from root nodules of Casuarina glauca . Antonie van Leeuwenhoek 105, 1099–1106 (2014). https://doi.org/10.1007/s10482-014-0168-6

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Keywords

  • Nocardia casuarinae
  • Casuarina
  • Root nodule
  • Sp. nov