Article | Published:

Streptosporangium minutum sp. nov., isolated from garden soil exposed to microwave radiation

The Journal of Antibioticsvolume 71pages564574 (2018) | Download Citation

Abstract

The actinobacterium, strain M26T, was isolated from garden soil that was pre-treated with microwave radiation. The soil sample was collected in Roodepoort, Gauteng Province, South Africa as part of an antibiotic-screening programme. The isolate produced branched vegetative mycelium with sporangiophores bearing small sporangia ranging from 3 to 6 μm in diameter. Rapid genus identification revealed that the isolate belongs to the genus Streptosporangium. To confirm this result, the strain was subjected to polyphasic taxonomic characterisation. Chemotaxonomic characteristics were as follows: meso-DAP in the peptidoglycan, the whole-cell hydrolysate yielded madurose, predominant menaquinones were MK9 (21%), MK9(H2) (40%), MK9(H4) (31%) and MK9(H6) (3%); the polar lipid profile included an aminolipid, phosphoglycolipids, phosphatidylethanolamine, and phosphatidylmonomethylethanolamine. In addition, the fatty acid profile showed the presence of C16:0 (12.8%), C17:1ω8c (14.2%), and 10-methyl-C17:0 (15.8%). Furthermore, 16S rRNA gene sequence phylogenetic analysis showed that the strain is closely related to members of the genus Streptosporangium, which supports its classification within the family Streptosporangiaceae. Strain M26T exhibited antibiosis against a range of pathogenic bacteria, including, but not limited to Acinetobacter baumannii ATCC 19606T, Enterobacter cloacae subsp. cloacae ATCC BAA-1143, Enterococcus faecalis ATCC 51299 (vancomycin resistant), Escherichia coli ATCC 25922, Listeria monocytogenes ATCC 19111, Mycobacterium tuberculosis H37RvT, Pseudomonas aeruginosa ATCC 27853, Salmonella enterica subsp. arizonae ATCC 13314T, and the methicillin-resistant Staphylococcus aureus subsp. aureus ATCC 33591 (MRSA). The name Streptosporangium minutum is proposed with the type strain M26T (=LMG 28850T =NRRL B-65295T).

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from $8.99

All prices are NET prices.

References

  1. 1.

    Couch JN. A new genus and family of the Actinomycetales, with a revision of the genus Actinoplanes. J Elisha Mitchell Sci Soc Chapel Hill N C. 1955;71:148–55.

  2. 2.

    Parte. A List of prokaryotic names with standing in nomenclature. http://www.bacterio.net. Accessed July 2017.

  3. 3.

    Mertz FP, Yao RC. Streptosporangium carneum sp. nov. isolated from soil. Int J Syst Bacteriol. 1990;40:247–53.

  4. 4.

    Boubetra D, et al. Streptosporangium algeriense sp. nov., an actinobacterium isolated from desert soil. Int J Syst Evol Microbiol. 2016;66:1034–8.

  5. 5.

    Chaouch FC, et al. Streptosporangium becharense sp. nov., an actinobacterium isolated from desert soil. Int J Syst Evol Microbiol. 2016;66:2484–90.

  6. 6.

    Zhang X, et al. Streptosporangium shengliensis sp. nov., a novel actinomycete isolated from a lake sediment. Antonie Van Leeuwenhoek. 2014;105:237–43.

  7. 7.

    Inahashi Y, Matsumoto A, Õmura S, Takahashi Y. Streptosporangium oxazolinicum sp. nov., a novel endophytic actinomycete producing new antitrypanosomal antibiotics, spoxazomicins. J Antibiot (Tokyo). 2011;64:297–302.

  8. 8.

    Fang B, et al. Streptosporangium lutulentum sp. nov., Streptosporangium fenghuangense sp. nov. and Streptosporangium corydalis sp. nov., three novel actinobacterial species isolated from National forest park of Fenghuang mountain. Antonie Van Leeuwenhoek. 2016;109:439–48.

  9. 9.

    Zhao J, et al. Streptosporangium jiaoheense sp. nov. and Streptosporangium taraxaci sp. nov., actinobacteria isolated from soil and dandelion root (Taraxacum mongolicum Hand. _Mazz). Int J Syst Evol Microbiol. 2016;66:2370–6.

  10. 10.

    Platas G, et al. Nutritional preferences of a group of Streptosporangium soil isolates. J Biosci Bioeng. 1999;88:269–75.

  11. 11.

    Terekhova L. Isolation of actinomycetes with the use of microwaves and electric. In Kurtböke I, editor. Selective isolation of rare actinomycetes. Queensland: Queensland Complete Printing Services; 2003. pp. 82–101.

  12. 12.

    Nonomura H, Ohara Y. Distribution of actinomycetes in soil. VIII. Green spore group of Microtetraspora, its preferential isolation and taxonomic characteristics. J Ferment Technol. 1971;49:1–7.

  13. 13.

    Quintana ET, Goodfellow M. Genus Streptosporangium. In Whitman W, et al., editors. Bergey’s manual of systematic bacteriology: the Actinobacteria. Vol 5. Springer Science and Business Media, New York; 2012. pp. 1811–25.

  14. 14.

    Locci R. In Williams ST, et al., editors. Bergey’s manual of systematic bacteriology. Baltimore: The Williams & Wilkins Co.; 1989. pp. 2451–508.

  15. 15.

    Shirling EB, Gottlieb D. Methods for characterisation of Streptomyces species. Int J Syst Bacteriol. 1966;16:313–40.

  16. 16.

    Atlas RM. Handbook of Microbiological Media. 3rd ed. Boca Raton, FL: CRC Press; 2004.

  17. 17.

    Gordon RE, Barnett DA, Handerhan JE, Pang C. H-N. Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Bacteriol. 1974;24:54–63.

  18. 18.

    Hasegawa T, Takizawa M, Tanida S. A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol. 1983;29:319–22.

  19. 19.

    Pfefferle C, Theobald U, Gürtler H, Fiedler H-P. Improved secondary metabolite production in the genus Streptosporangium by optimization of the fermentation conditions. J Biotechnol. 2000;80:135–42.

  20. 20.

    Cook AE, Meyers PR. Rapid identification of filamentous actinomycetes to the genus level using genus-specific 16S rRNA gene restriction fragment patterns. Int J Syst Evol Microbiol. 2003;53:1907–15.

  21. 21.

    Altschul SF, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402.

  22. 22.

    Yoon SH, et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol. 2017;67:1613–7.

  23. 23.

    Tamura K, et al. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–9.

  24. 24.

    Kumar S, Nei M, Dudley J, Tamura K. MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform. 2008;9:299–306.

  25. 25.

    Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–25.

  26. 26.

    Takahashi K, Nei M. Efficiencies of fast algorithms of phylogenetic inference under the criteria of maximum parsimony, minimum evolution, and maximum likelihood when a large number of sequences are used. Mol Biol Evol. 2000;17:1251–8.

  27. 27.

    Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.

  28. 28.

    Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981;17:368–79.

  29. 29.

    Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16:111–20.

  30. 30.

    Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution. 1985;39:783–91.

  31. 31.

    Marmur J. A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol. 1961;3:208–15.

  32. 32.

    Coil D, Jospin G, Darling AE. A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics. 2015;31:587–9.

  33. 33.

    Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29:1072–5.

  34. 34.

    Blin K, et al. The antiSMASH database, a comprehensive database of microbial secondary metabolite biosynthetic gene clusters. Nucleic Acids Res. 2017;45:D555–D559.

  35. 35.

    Grant JR, Arantes AS, Stothard P. Comparing thousands of circular genomes using the CGView Comparison Tool. BMC Genom. 2012;13:202.

  36. 36.

    Stothard P, Grant JR, Van Domselaar G. Visualizing and comparing circular genomes using the CGView family of tools. Brief Bioinform. 2017. https://doi.org/10.1093/bib/bbx081.

  37. 37.

    Meier-Kolthoff JP, et al. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinforma. 2013;14:60.

  38. 38.

    Gevers D, Huys G, Swings J. Application of rep-PCR fingerprinting of Lactobacillus species. FEMS Microbiol Lett. 2001;205:31–36.

  39. 39.

    Goris J, et al. Evaluation of a microplate DNA-DNA hybridization method compared with the initial renaturation method. Can J Microbiol. 1998;44:1148–53.

  40. 40.

    Cleenwerck I, Vandermeulebroecke K, Janssens D, Swings J. Re-examination of the genus Acetobacter, with descriptions of Acetobacter cerevisiae sp. nov. and Acetobacter malorum sp. nov. Int J Syst Evol Microbiol. 2002;52:1551–8.

  41. 41.

    Ezaki T, Hashimoto Y, Yabuuchi E. Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Evol Microbiol. 1989;39:224–9.

  42. 42.

    Sambrook J, et al. Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1989.

  43. 43.

    Eckwall EC, Schottel JL. Isolation and characterization of an antibiotic produced by the scab disease-suppressive Streptomyces diastatochromogenes strain Pon SS II. J Ind Microbiol Biot. 1997;19:2202–25.

  44. 44.

    Betina V. Bioautography in paper and thin-layer chromatography and its scope in the antibiotic field. J Chromatogr. 1973;78:41–51.

  45. 45.

    Meyers PR. Gyrase subunit B amino acid signatures for the actinobacterial family Streptosporangiaceae. Syst Appl Microbiol. 2014;37:252–60.

  46. 46.

    Meyers PR. Molecular-signature analyses support the establishment of the actinobacterial genus Sphaerimonospora (Mingma et al. 2016). Syst Appl Microbiol. 2017;40:423–9.

  47. 47.

    Meyers PR. Analysis of recombinase A (recA/RecA) in the actinobacterial family Streptosporangiaceae and identification of molecular signatures. Syst Appl Microbiol. 2015;38:567–77.

  48. 48.

    Wayne LG, et al. International committee on systematic bacteriology. report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol. 1987;37:463–4.

  49. 49.

    Lechevalier MP, Lechevalier H. Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol. 1970;20:435–43.

  50. 50.

    Ohnishi Y, et al. Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J Bacteriol. 2008;190:4050–60.

  51. 51.

    Funabashi M, Funa N, Horinouchi S. Phenolic lipids synthesized by type III polyketide synthase confer penicillin resistance on Streptomyces griseus. J Biol Chem. 2008;283:13983–91.

  52. 52.

    Hirano S, et al. Conditionally positive effect of the TetR-family transcriptional regulator AtrA on streptomycin production by Streptomyces griseus. Microbiology. 2008;154:905–14.

  53. 53.

    Tian J, et al. Discovery of pentangular polyphenols hexaricins A–C from marine Streptosporangium sp. CGMCC 4.7309 by genome mining. Appl Microbiol Biot. 2016;100:4189–99.

  54. 54.

    Bentley SD, et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature. 2002;417:141–7.

  55. 55.

    Redenbach M, et al. A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3 (2) chromosome. Mol Microbiol. 1996;21:77–96.

Download references

Acknowledgements

Thank you to Di James for DNA sequencing and Miranda Waldron of the Electron Microscope Unit, University of Cape Town (UCT) for help with scanning electron microscopy. Thank you to Hans G. Trüper for assistance with Latin in deriving the specific epithet for strain M26T. The authors also wish to acknowledge the assistance of Dr Kirby-McCullough (University of the Western Cape) in the sequencing of the genome of strain M26T.

Funding:

Marilize le Roes-Hill held a research grant from the National Research Foundation (NRF) of South Africa (grant number: 90304). Paul Meyers was the recipient of research grants from the Medical Research Council of South Africa, and the University Research Committee (UCT). Any opinion, findings and conclusions or recommendations expressed in this material are those of the authors and therefore the NRF does not accept any liability in regard thereto.

Author information

Affiliations

  1. Biocatalysis and Technical Biology Research Group, Institute of Biomedical and Microbial Biotechnology, Cape Peninsula University of Technology, PO Box 1906, Bellville, 7535, South Africa

    • Marilize Le Roes-Hill
    • , Kim Durrell
    •  & Alaric Prins
  2. Department of Microbiology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa

    • Kim Durrell
  3. Institute for Microbial Biotechnology and Metagenomics, University of the Western Cape, Bellville, 7535, South Africa

    • Alaric Prins
  4. Department of Molecular and Cell Biology, University of Cape Town, Private Bag X3, Rondebosch, 7701, Cape Town, South Africa

    • Paul R. Meyers

Authors

  1. Search for Marilize Le Roes-Hill in:

  2. Search for Kim Durrell in:

  3. Search for Alaric Prins in:

  4. Search for Paul R. Meyers in:

Conflict of interest:

The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Marilize Le Roes-Hill.

Electronic supplementary material

About this article

Publication history

Received

Revised

Accepted

Published

DOI

https://doi.org/10.1038/s41429-018-0036-0