Antonie van Leeuwenhoek

, Volume 101, Issue 1, pp 185–193

Verrucosispora maris sp. nov., a novel deep-sea actinomycete isolated from a marine sediment which produces abyssomicins

  • Michael Goodfellow
  • James E. M. Stach
  • Roselyn Brown
  • Avinash Naga Venkata Bonda
  • Amanda L. Jones
  • Joanne Mexson
  • Hans-Peter Fiedler
  • Tiago Domingues Zucchi
  • Alan T. Bull
Original Paper

Abstract

Verrucosispora isolate AB-18-032T, the abyssomicin- and proximicin-producing actinomycete, has chemotaxonomic and morphological properties consistent with its classification in the genus Verrucosispora. The organism formed a distinct phyletic line in the Verrucosispora 16S rRNA gene tree sharing similarities of 99.7%, 98.7% and 98.9% with Verrucosispora gifhornensis DSM 44337T, Verrucosispora lutea YIM 013T and Verrucosispora sediminis MS 426T, respectively. It was readily distinguished from the two latter species using a range of phenotypic features and from V. gifhornensis DSM 44337T, its nearest phylogenetic neighbor, by a DNA G+C content of 65.5 mol% obtained by thermal denaturation and fluorometry and DNA:DNA relatedness values of 64.0% and 65.0% using renaturation and fluorometric methods, respectively. It is apparent from the combined genotypic and phenotypic data that strain AB-18-032T should be classified in the genus Verrucosispora as a new species. The name Verrucosispora maris sp. nov. is proposed for this taxon with isolate AB-18-032T (= DSM 45365T = NRRL B-24793T) as the type strain.

Keywords

Verrucosispora maris Polyphasic taxonomy Marine sediment Actinomycete 

References

  1. Bister B, Bischoff D, Ströbele M, Riedlinger J, Reicke A, Bull AT, Zähner H, Fiedler H-P, Süssmuth RD (2004) Abyssomicin C— a novel polycyclic antibiotic from a marine Verrucosispora strain as an inhibitor of the p-aminobenzoic acid/tetrahydrofolate biosynthesis pathway. Angew Chem Int Ed 43:2574–2576CrossRefGoogle Scholar
  2. Bredholdt H, Tjaervik E, Johnson G, Zotchev SB (2008) Actinomycetes from sediments in the Trondheim fjord, Norway: diversity and biological activity. Mar Drugs 6:12–14CrossRefGoogle Scholar
  3. Collins MD (1994) Isoprenoid quinones. In: Goodfellow M, O’Donnell AG (eds) Chemical methods in prokaryotic systematics. Wiley, Chichester, pp 265–309Google Scholar
  4. Dai H-Q, Wang J, Xin Y-H, Pei G, Tang S-K, Ren B, Ward A, Ruan J-S, Wen-Jun Li, Zhang L-X (2010) Verrucosispora sediminis sp nov., a cyclodipeptide-producing actinomycete from deep-sea sediment. Int J Syst Evol Microbiol 60:1807–1812PubMedCrossRefGoogle Scholar
  5. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376PubMedCrossRefGoogle Scholar
  6. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  7. Felsenstein J (1993) PHYLIP (Phylogenetic Inference Package), version 3.5c Department of Genetics. University of Washington, Seattle, USAGoogle Scholar
  8. Fiedler H-P, Bruntner C, Riedlinger J, Bull AT, Knutsen G, Goodfellow M, Jones AL, Maldonado L, Pathom-aree W, Beil W, Schneider K, Keller S, Süssmuth RD (2008) Proximicin A, B and C, novel aminofuran antibiotic and anticancer compounds isolated from marine strains of the actinomycete Verrucosispora. J Antibiot 61:158–163PubMedCrossRefGoogle Scholar
  9. Fitch WM, Margoliash E (1967) Construction of phylogenetic trees: a method based on mutation distances as estimated from cytochrome c sequences is one of general applicability. Science 155:279–284PubMedCrossRefGoogle Scholar
  10. Gonzalez JM, Saiz-Jimenez C (2002) A fluorimetric method for the estimation of G+C mol% content in microorganisms by thermal denaturation temperature. Environ Microbiol 4:770–773PubMedCrossRefGoogle Scholar
  11. Gonzalez JM, Saiz-Jimenez C (2005) A simple fluorimetric method for the estimation of DNA–DNA relatedness between closely related microorganisms by thermal denaturation temperatures. Extremophiles 9:75–79PubMedCrossRefGoogle Scholar
  12. Goodfellow M, Fiedler H-P (2010) A guide to successful bioprospecting: informed by actinobacterial systematics. Antonie van Leeuwenhoek 98:119–142PubMedCrossRefGoogle Scholar
  13. Gordon RE (1967) The taxonomy of soil bacteria. In: Gray TRG, Parkinson D (eds) Ecology of soil bacteria. Liverpool University Press, Liverpool, pp 293–321Google Scholar
  14. Gordon RE, Mihm JM (1962) Identification of Nocardia caviae nov comb. Ann NY Acad Sci 98:628–636CrossRefGoogle Scholar
  15. Gordon RE, Barnett DA, Handerhan JE, Pang CH-N (1974) Nocardia coeliaca, Nocardia autotrophica and the nocardin strain. Int J Syst Bacteriol 24:54–63CrossRefGoogle Scholar
  16. Hong K, Gao A-H, Xie Q-Y, Gao H, Zhuang L, Lin H-P, Yu H-P, Yao X-S, Goodfellow M, Ruan J-S (2009) Actinomycetes for marine drug discovery isolated from mangrove soils and plants in China. Mar Drugs 7:24–44PubMedCrossRefGoogle Scholar
  17. Hsu SC, Lockwood JL (1975) Powdered chitin as a selective medium for enumeration of actinomycetes in water and soil. Appl Microbiol 29:442–443Google Scholar
  18. Jiang S, Sun W, Chen M, Dai S, Zheng L, Liu Y, Lee KL, Li X (2007) Diversity of culturable actinobacteria isolated from marine sponge Haliclona sp. Antonie van Leeuwenhoek 92:405–416PubMedCrossRefGoogle Scholar
  19. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: H.N Munro (ed) Mammalian protein metabolism, vol 3. Academic Press, New York, pp 21–132Google Scholar
  20. Keller S, Nicholson G, Drahl C, Sorensen E, Fiedler H-P, Sűssmuth RD (2007a) Abyssomicins G and H and atrop-abyssomicin C from the marine Verrucosispora strain AB-18-032. J Antibiot 60:391–394PubMedCrossRefGoogle Scholar
  21. Keller S, Schadt HS, Ortel I, Sűssmuth RD (2007b) Action of atrop-abyssomicin C as an inhibitor of 4-amino-4-deoxychorismate synthase Pa bB. Angeo Chem Int Ed 46:8254–8286CrossRefGoogle Scholar
  22. Kim SB, Brown R, Oldfield C, Gilbert SC, Goodfellow M (1999) Gordonia desulphuricans sp nov., a benzothiophene-desulphurizing actinomycete. Int J Syst Bacteriol 49:1845–1851PubMedCrossRefGoogle Scholar
  23. Kluge AG, Farris FS (1969) Quantitative phyletics and the evolution of anurans. Syst Zool 18:1–32CrossRefGoogle Scholar
  24. Lechevalier MP, Lechevalier HA (1970) Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol 20:435–443CrossRefGoogle Scholar
  25. Lechevalier MP, de Biévre C, Lechevalier HA (1977) Chemotaxonomy of aerobic actinomycetes: Phospholipid composition. Biochem Syst Evol 5:249–260CrossRefGoogle Scholar
  26. Liao Z-L, Tang S-K, Guo L, Zhang Y-Q, Tian X-P, Jiang C-L, Xu L-H, Li W-J (2009) Verrucosispora lutea sp nov., isolated from a mangrove sediment sample. Int J Syst Evol Microbiol 59:2269–2273PubMedCrossRefGoogle Scholar
  27. Mexson J (2001) Selective isolation and taxonomic analysis of the genus Micromonospora. Ph.D. Thesis, University of Kent, Canterbury, UKGoogle Scholar
  28. Minnikin DE, Alshamaony L, Goodfellow M (1975) Differentiation of Mycobacterium, Nocardia and related taxa by thin-layer chromatographic analyses of whole-cell methanolysates. J Gen Microbiol 88:200–204PubMedGoogle Scholar
  29. 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 2:233–241CrossRefGoogle Scholar
  30. Rheims H, Schumann P, Rohde M, Stackebrandt E (1998) Verrucosispora gifhornensis gen nov., sp. nov., a new member of the actinobacterial family Micromonosporaceae. Int J Syst Bacteriol 48:1119–1127PubMedCrossRefGoogle Scholar
  31. Riedlinger J, Reicke A, Krismer B, Zähner H, Bull AT, Maldonado LA, Ward AC, Goodfellow M, Bister B, Bischoff D, Süssmuth RD, Fiedler H-P (2004) Abyssomicins, inhibitors of the para-aminobenzoic acid pathway produced by the marine Verrucosispora strain AB-18-032. J Antibiot 57:271–279PubMedGoogle Scholar
  32. Roh H, Uguru GC, Ko H-J, Kim S, Kim B-Y, Goodfellow M, Bull AT, Kim K-H, Bibb MJ, Choi I-G, Stach JEM (2011) Genome sequence of the abyssomicin- and proximicin-producing marine actinomycete Verrucosispora maris AB-18-032. J Bact 193:3391–3392PubMedCrossRefGoogle Scholar
  33. Saitou N, Nei M (1987) The neighbor-joining method: a new method for constructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  34. Schneider K, Keller S, Wolter FE, Roglin L, Beil W, Seitz O, Nicholson G, Bruntner C, Riedlinger J, Fiedler H-P, Sűssmuth RD (2008) Proximicins A, B and C-antitumor furan analogues of netropsin from the marine actinomycete Verrucosispora induced upregulatioin of p53 and the cyclin kinase inhibitor p21. Angew Chem Int Ed 47:3258–3261CrossRefGoogle Scholar
  35. Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340CrossRefGoogle Scholar
  36. Stevenson IL (1967) Utilization of aromatic hydrocarbons by Arthrobacter spp. Can J Microbiol 13:205–211PubMedCrossRefGoogle Scholar
  37. Tan GYA, Robinson S, Lacey E, Goodfellow M (2006) Evaluation of Amycolatopsis diversity in soil using genus-specific primers and novel selective media. Syst Appl Microbiol 29:557–569PubMedCrossRefGoogle Scholar
  38. Wayne LG, Brenner DJ, Colwell RR & 9 other authors (1987) International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37: 463–464Google Scholar
  39. Williams ST, Goodfellow M, Alderson G, Wellington EMH, Sneath PHA, Sackin MJ (1983) Numerical classification of Streptomyces and related genera. J Gen Microbiol 129:1743–1813PubMedGoogle Scholar
  40. Xie QY, Hong K, Goodfellow M (2011) Genus-specific primers targeting the 16S rRNA gene for PCR detection of members of the genus Verrucosispora. Antonie van Leeuwenhoek 100:117–128PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Michael Goodfellow
    • 1
  • James E. M. Stach
    • 1
  • Roselyn Brown
    • 1
  • Avinash Naga Venkata Bonda
    • 1
  • Amanda L. Jones
    • 1
    • 2
  • Joanne Mexson
    • 3
  • Hans-Peter Fiedler
    • 4
  • Tiago Domingues Zucchi
    • 1
    • 5
  • Alan T. Bull
    • 1
    • 3
  1. 1.School of BiologyUniversity of NewcastleNewcastle upon TyneUK
  2. 2.School of Life Sciences, Ellison BuildingNorthumbria UniversityNewcastle upon TyneUK
  3. 3.School of BiosciencesUniversity of KentCanterburyUK
  4. 4.Mikrobiologisches InstitutUniversität TübingenTuebingenGermany
  5. 5.Departamento de Entomologia e Acarologia, ESALQUniversidade de São PauloPiracicabaBrazil

Personalised recommendations