Streptomyces corynorhini sp. nov., isolated from Townsend’s big-eared bats (Corynorhinus townsendii)

  • Paris S. HammEmail author
  • Nicole A. Caimi
  • Diana E. Northup
  • Ernest W. Valdez
  • Debbie C. Buecher
  • Christopher A. Dunlap
  • David P. Labeda
  • Andrea Porras-Alfaro
Original Paper


Four bacterial strains, with the capability of inhibiting Pseudogymnoascus destructans, the causative agent of white-nose syndrome, were isolated from male Townsend’s big-eared bats (Corynorhinus townsendii, Family: Vespertilionidae) in New Mexico. Isolates AC161, AC162, AC208, and AC230T were characterised as a novel clade using morphological, phenotypic and phylogenetic analysis. A draft genome of the type strain was completed to determine its taxonomy and secondary metabolite biosynthetic potential. Multi-locus sequence analysis nests AC230T with neighbours Streptomyces scopuliridis (NRRL B-24574T), Streptomyces lushanensis (NRRL B-24994T), Streptomyces odonnellii (NRRL B-24891T) and Streptomyces niveus (NRRL 2466T). Further phylogenetic analysis showed the MLSA distances between AC230T and its near neighbours are much greater than the generally accepted threshold (> 0.007) for bacterial species delineation. DNA–DNA relatedness between AC230T and its near neighbours ranged between 25.7 ± 2.1 and 29.9 ± 2.4%. The DNA G+C content of the genomic DNA of the type strain is 71.7 mol%. Isolate AC230T presents a white to ivory hue on most ISP media and its micromorphology exhibits ovoid spores with smooth surfaces in flexuous chains. Based on our study of AC230T, the strain warrants the assignment to a novel species, for which the name Streptomyces corynorhini sp. nov. is proposed. The type strain is AC230T (= JCM 33171T, = ATCC TSD155T).


Actinobacteria Bat Streptomyces Taxonomy White-nose syndrome 



PSH and APA thank support from Western Illinois University and their Research Inspiring Student Excellence (RISE) and Women in Science (WIS) programs. DPL and the ARS Culture Collection CRIS project was supported by ARS National Program 301. CAD was supported by ARS National Programs 303, 304 and 306. DEN and DCB gratefully acknowledge the support of the staff at El Malpais National Monument with logistical support and assistance with the NPS Materials Transfer Agreement implementation. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture. The mention of firm names or trade products does not imply that they are endorsed or recommended by the USDA or USGS over other firms or similar products not mentioned. USDA is an equal opportunity provider and employer.

Author contributions

PSH Wrote the paper, Collected the data, Conceived the design; NAC Contributed to writing the paper, Collected the data; DEN Provided funding, Collected the data, Conceived the design; EWV Provided funding, Collected the data, Conceived the design; DCB Provided funding, Collected the data, Conceived the design; CAD Wrote the paper, Performed the analysis; DPL Contributed to analysis tools; APA Provided funding, Collected the data, Conceived the design.

Funding information

Initial funding was provided by the Eppley Foundation and further provided by the National Park Service through the Colorado Plateau Cooperative Ecosystem Studies unit (CPCESU) and Western National Park Association for work in El Malpais National Monument. Additional funding was provided by the IDNR (PI: Porras-Alfaro), New Mexico Game and Fish Department Share with Wildlife Program, Cave Conservancy Foundation, National Speleological Society Rapid Response Fund, and T&E, Inc. The lead author (PSH) would like to thank the Mycological Society of America for funding to present her research.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interests in the manuscript.

Supplementary material

10482_2019_1261_MOESM1_ESM.pdf (673 kb)
Supplementary material 1 (PDF 673 kb)


  1. Auch AF, von Jan M, Klenk HP, Goker M (2010) Digital DNA–DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2:117–134CrossRefGoogle Scholar
  2. Barona-Gómez F, Wong U, Giannakopulos AE, Derrick PJ, Challis GL (2004) Identification of a cluster of genes that directs desferrioxamine biosynthesis in Streptomyces coelicolor M145. J Am Chem Soc 126:16282–16283CrossRefGoogle Scholar
  3. Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JT, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323:227CrossRefGoogle Scholar
  4. Blin K, Wolf T, Chevrette MG, Lu X, Schwalen CJ, Kautsar SA, Suarez Duran HG, de Los Santos ELC, Kim HU, Nave M, Dickschat JS, Mitchell DA, Shelest E, Breitling R, Takano E, Lee SY, Weber T, Medema MH (2017) antiSMASH 4.0-improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res 45:W36–W41CrossRefGoogle Scholar
  5. Brautaset T, Sekurova ON, Sletta H, Ellingsen TE, Strøm AR, Valla S, Zotchev SB (2000) Biosynthesis of the polyene antifungal antibiotic nystatin in Streptomyces noursei ATCC 11455: analysis of the gene cluster and deduction of the biosynthetic pathway. Chem Biol 7:395–403CrossRefGoogle Scholar
  6. Cryan PM, Meteyer CU, Boyles JG, Blehert DS (2010) Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. BMC Biol 8:135CrossRefGoogle Scholar
  7. Ellison LE, Valdez EW, Cryan PM, O’Shea TJ, Bogan MA (2013) Standard operating procedure for the study of bats in the field. FORT IACUC SOP#: 2013-01 (Revision 2), Fort Collins Science Center, 40 ppGoogle Scholar
  8. Farris MH, Duffy C, Findlay RH, Olson JB (2011) Streptomyces scopuliridis sp. nov., a bacteriocin-producing soil streptomycete. Int J Syst Evol Microbiol 61:2112–2116CrossRefGoogle Scholar
  9. Frick WF, Pollock JF, Hicks AC, Langwig KE, Reynolds DS, Turner GG, Butchkoski CM, Kunz TH (2010) An emerging disease causes regional population collapse of a common North American bat species. Science 329:679–682CrossRefGoogle Scholar
  10. Hamm PS, Caimi NA, Northup DE, Valdez EW, Buecher DC, Dunlap CA, Labeda DP, Lueschow SR, Porras-Alfaro A (2017) Western bats as a reservoir of novel Streptomyces species with antifungal activity. Appl Environ Microbiol 83:e03057CrossRefGoogle Scholar
  11. Harris DA, Reagan MA, Ruger M, Wallick H, Woodruff HB (1955) Discovery and antimicrobial properties of cathomycin, a new antibiotic produced by Streptomyces spheroides n. sp. Antibiotics Ann 3:909–917Google Scholar
  12. Hayakawa M, Nonomura H (1987) Humic acid-vitamin agar, a new medium for the selective isolation of soil actinomycetes. J Ferment Technol 65:501–509CrossRefGoogle Scholar
  13. Huang E, Guo Y, Yousef AE (2014) Biosynthesis of the new broad-spectrum lipopeptide antibiotic paenibacterin in Paenibacillus thiaminolyticus OSY-SE. Res Microbiol 165:243–251CrossRefGoogle Scholar
  14. Jolley KA, Maiden MC (2010) BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinform 11:595CrossRefGoogle Scholar
  15. Kersten RD, Yang YL, Xu Y, Cimermancic P, Nam SJ, Fenical W, Fischbach MA, Moore BS, Dorrestein PC (2011) A mass spectrometry-guided genome mining approach for natural product peptidogenomics. Nat Chem Biol 7:794–802CrossRefGoogle Scholar
  16. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549CrossRefGoogle Scholar
  17. Labeda DP, Dunlap CA, Rong X, Huang Y, Doroghazi JR, Ju K-S, Metcalf WW (2017) Phylogenetic relationships in the family Streptomycetaceae using multi-locus sequence analysis. Antonie Leeuwenhoek 110:563–583CrossRefGoogle Scholar
  18. Meier-Kolthoff JP, Auch AF, Klenk HP, Goker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60CrossRefGoogle Scholar
  19. Meier-Kolthoff JP, Klenk HP, Göker M (2014) Taxonomic use of DNA G+C content and DNA–DNA hybridization in the genomic age. Int J Syst Evol Microbiol 64:352–356CrossRefGoogle Scholar
  20. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New YorkGoogle Scholar
  21. Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T, Kyrpides NC, Pukall R, Klenk H-P, Goodfellow M, Göker M (2018) Genome-based taxonomic classification of the Phylum actinobacteria. Front Microbiol 9:2007CrossRefGoogle Scholar
  22. Onaka H, Taniguchi S, Igarashi Y, Furumai T (2002) Cloning of the staurosporine biosynthetic gene cluster from Streptomyces sp. TP-A0274 and its heterologous expression in Streptomyces lividans. J Antibiot (Tokyo) 55:1063–1071CrossRefGoogle Scholar
  23. Pereira PHF, Macrae A, Reinert F, de Souza RF, Coelho RRR, Potter G, Klenk HP, Labeda DP (2017) Streptomyces odonnellii sp. nov., a proteolytic streptomycete isolated from soil under cerrado (savanna) vegetation cover. Int J Syst Evol Microbiol 67:5211–5215CrossRefGoogle Scholar
  24. Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131CrossRefGoogle Scholar
  25. Rong X, Huang Y (2012) Taxonomic evaluation of the Streptomyces hygroscopicus clade using multilocus sequence analysis and DNA-DNA hybridization, validating the MLSA scheme for systematics of the whole genus. Syst Appl Microbiol 35:7–18CrossRefGoogle Scholar
  26. Rüegg UT, Gillian B (1989) Staurosporine, K-252 and UCN-01: potent but nonspecific inhibitors of protein kinases. Trends Pharmacol Sci 10:218–220CrossRefGoogle Scholar
  27. Shirling EB, Gottlieb DA (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340CrossRefGoogle Scholar
  28. Smith CG (1956) Fermentation studies with Streptomyces niveus. Appl Microbiol 4:232–236Google Scholar
  29. Smith CG, Dietz A, Sokolski WT, Savage GM (1956) Streptonivicin, a new antibiotic. I. Discovery and biologic studies. Antibiot Chemother (Northfield) 6:135–142Google Scholar
  30. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Truper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464CrossRefGoogle Scholar
  31. Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek, Int J Gen Mol Microbiol 110:1281–1286CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2019

Authors and Affiliations

  • Paris S. Hamm
    • 1
    • 2
    Email author
  • Nicole A. Caimi
    • 2
  • Diana E. Northup
    • 2
  • Ernest W. Valdez
    • 3
  • Debbie C. Buecher
    • 4
  • Christopher A. Dunlap
    • 5
  • David P. Labeda
    • 5
  • Andrea Porras-Alfaro
    • 1
    • 2
  1. 1.Department of Biological SciencesWestern Illinois UniversityMacombUSA
  2. 2.Department of BiologyUniversity of New MexicoAlbuquerqueUSA
  3. 3.U. S. Geological Survey, Fort Collins Science CenterFort CollinsUSA
  4. 4.Buecher Biological ConsultingTucsonUSA
  5. 5.Agriculture Research Service, US Department of AgriculturePeoriaUSA

Personalised recommendations