Skip to main content

Advertisement

SpringerLink
Log in

Biotechnological potential of Actinobacteria from Canadian and Azorean volcanic caves

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Caves are regarded as extreme habitats with appropriate conditions for the development of Actinobacteria. In comparison with other habitats, caves have not yet been the target of intensive screening for bioactive secondary metabolites produced by actinomycetes. As a primary screening strategy, we conducted a metagenomic analysis of the diversity and richness of a key gene required for non-ribosomal peptide (NRP) biosynthesis, focusing on cave-derived sediments from two Canadian caves (a lava tube and a limestone cave) to help us predict whether different types of caves may harbor drug-producing actinobacteria. Using degenerate PCR primers targeting adenylation domains (AD), a conserved domain in the core gene in NRP biosynthesis, a number of amplicons were obtained that mapped back to biomedically relevant NRP gene cluster families. This result guided our culture-dependent sampling strategy of actinomycete isolation from the volcanic caves of Canada (British Columbia) and Portugal (Azores) and subsequent characterization of their antibacterial and enzymatic activities. Multiple enzymatic and antimicrobial activities were identified from bacterial of the Arthrobacter and Streptomyces genera demonstrating that actinomycetes from volcanic caves are promising sources of antibacterial, antibiofilm compounds and industrially relevant enzymes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adrio JL, Demain AL (2014) Microbial enzymes: tools for biotechnological processes. Biomolecules:117–139

  • Alasil SM, Omar R, Ismail S, Yusof MY (2014) Antibiofilm activity, compound characterization, and acute toxicity of extract from a novel bacterial species of Paenibacillus. Int J Microbiol 2014:e649420

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • ASTM E2799-12 (2012) Standard test method for testing disinfectant efficiacy against Pseudomonas aeruginosa biofilm using the MBEC assay. ASTM International, West Conshohocken

    Google Scholar 

  • Ayuso-Sacido A, Genilloud O (2005) New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb Ecol 49:10–24

    Article  CAS  PubMed  Google Scholar 

  • Babavalian H, Amoozegar MA, Pourbabaee AA, Moghaddam MM, Shakeri F (2013) Isolation and identification of moderately halophilic bacteria producing hydrolytic enzymes from the largest hypersaline playa in Iran. Microbiology 82:466–474

    Article  CAS  Google Scholar 

  • Bauer AW, Kirby WM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493–496

    CAS  PubMed  Google Scholar 

  • Bhat MK (2000) Cellulases and related enzymes in biotechnology. Biotechnol Adv 18:355–383

    Article  CAS  PubMed  Google Scholar 

  • Brady SF (2007) Construction of soil environmental DNA cosmid libraries and screening for clones that produce biologically active small molecules. Nat Protoc 2:1297–1305

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi:10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavicchioli R, Charlton T, Ertan H, Mohd Omar S, Siddiqui KS, Williams T (2011) Biotechnological uses of enzymes from psychrophiles. Microb Biotechnol 4:449–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang FY, Brady SF (2014) Characterization of an environmental DNA-derived gene cluster that encodes the bisindolylmaleimide methylarcyriarubin. Chembiochem 15:815–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chao A (1984) Non-parametric estimation of the number of classes in a population. Scand J Stat 11:265–270

    Google Scholar 

  • Chao A, Shen TJ (2003) Nonparametric estimation of Shannon’s index of diversity when there are unseen species in sample. Environ Ecol Stat 10:429–443

    Article  Google Scholar 

  • Charlop-Powers Z, Owen JG, Reddy BVB, Ternei MA, Brady SF (2014) Chemical-biogeographic survey of secondary metabolism in soil. P Natl Acad Sci 111:3757–3762

    Article  CAS  Google Scholar 

  • Charlop-Powers Z, Owens JG, Reddy BVB, Ternei MA, Guimarães DO, de Frias UA, Pupo MT, Seepe P, Feng Z, Brady SF (2015) Global biogeographic sampling of bacterial secondary metabolism. eLife 4:e05048

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheeptham N, Towers GHN (2002) Light-mediated activities of some Thai medicinal plant teas. Fitoterapia 73:651–662

    Article  CAS  PubMed  Google Scholar 

  • Cheeptham N, Sadoway T, Rule D, Watson K, Moote P, Soliman L, Azad N, Donkor KD, Horne D (2013) Cure from the cave: volcanic cave actinomycetes and their potential in drug discovery. Int J Speleol 42:35–47

    Article  Google Scholar 

  • Cheng XC, Kihara T, Kusakabe H, Magae J, Kobayashi Y, Fang RP, Ni ZF, Shen YC, Ko K, Yamaguchi I, Isono K (1987) A new antibiotic, tautomycin. J Antibiot 40:907–909

    Article  CAS  PubMed  Google Scholar 

  • Chi Z, Chi Z, Zhang T, Liu G, Yue L (2009) Inulinase-expressing microorganisms and applications of inulinases. Appl Microbiol Biot 82:211–220

    Article  CAS  Google Scholar 

  • Cimermancic P, Medema MH, Claesen J, Kurita K, Wieland Brown LC, Mavrommatis K, Pati A, Godfrey PA, Koehrsen M, Clardy J, Birren BW, Takano E, Sali A, Linington RG, Fischbach MA (2014) Insights into secondary metabolism from a global analysis of prokaryotic biosynthetic gene clusters. Cell 158:412–421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies J (2006) Are antibiotics naturally antibiotics? J Ind Microbiol Biot 33:496–499

    Article  CAS  Google Scholar 

  • Donadio S, Maffioli S, Monciardini P, Sosio M, Jabes D (2010) Antibiotic discovery in the twenty-first century: current trends and future perspectives. J Antibiot 63:423–430

    Article  CAS  PubMed  Google Scholar 

  • Duangmal K, Mingma R, Phatom-aree W, Niyomvong N, Inahashi Y, Matsumoto A, Thamchaipenet A, Takahashi Y (2012) Microbispora thailandensis sp. nov., an actinomycete isolated from cave soil. J Antibiot 65:491–494

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  • Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, Ravel J (2014) An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2:6

    Article  PubMed  PubMed Central  Google Scholar 

  • Farmer JT, Shimkevitch AV, Reilly PS, Mlynek KD, Jensen KS, Callahan MT, Bushaw-Newton KL, Kaplan JB (2014) Environmental bacteria produce abundant and diverse antibiofilm compounds. J Appl Microbiol 117:1663–1673

    Article  CAS  PubMed  Google Scholar 

  • Fischbach MA, Walsh CT, Clardy J (2008) The evolution of gene collectives: how natural selection drives chemical innovation. Proc Natl Acad Sci 105:4601–4608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu H, Wei Y, Zou Y, Li M, Wang F, Chen J, Zhang L, Liu Z, Ding L (2014) Research progress on the actinomycete Arthrobacter. Adv Microbiol 4:747–753

    Article  CAS  Google Scholar 

  • Gaddy JA, Actis LA (2009) Regulation of Acinetobacter baumannii biofilm formation. Future Microbiol 4:273–278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golapkhan HBZ, Rodrigues T, Avanessian A, Alnadhi R, Vieira N, Cheeptham N (2013) Isolation of and Screening for potential antibiotic producing actinomycetes from Tupper Cave System, British Columbia. In: The 4th British Columbia Protected Areas Research Forum Conference (BCPARF). TRU campus, Kamloops

  • Goodfellow M, Fiedler HP (2010) A guide to successful bioprospecting: informed by actinobacterial systematic. Anton Leeuw 98:119–142

    Article  Google Scholar 

  • Guo XH, Kim JM, Nam HM, Park SY, Kim JM (2010) Screening lactic acid bacteria from swine origins for multistrain probiotics based on in vitro functional properties. Anaerobe 16:321–326

    Article  PubMed  Google Scholar 

  • Guo X, Liu N, Li X, Ding Y, Shang F, Gao Y, Ruan J, Huang Y (2015) Red soils harbor diverse culturable actinomycetes that are promising sources of novel secondary metabolites. Appl Environ Microbiol 81:3086–3103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108

    Article  CAS  PubMed  Google Scholar 

  • Harris AD, Ramalingam C (2010) Xylanases and its application in food industry: a review. Journal of Experimental Sciences 1:1–11

    Article  Google Scholar 

  • Hathaway JJM, Garcia MG, Moya M, Spilde MN, Stone FD, Dapkevicius MDLNE, Amorim IR, Gabriel R, Borges PAV, Northup DE (2014) Comparison of bacterial diversity in Azorean and Hawaiian lava cave microbial mats. Geomicrobiol J 31:205–220

    Article  Google Scholar 

  • Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8:15–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hosaka T, Ohnishi-Kameyama M, Muramatsu H, Murakami K, Tsurumi Y, Kodani S, Yoshida M, Fujie A, Ochi K (2009) Antibacterial discovery in actinomycetes strains with mutations in RNA polymerase or ribosomal protein S12. Nat Biotechnol 27:462–464

    Article  CAS  PubMed  Google Scholar 

  • Kango N, Jain SC (2011) Production and properties of microbial inulinases: recent advances. Food Biotechnol 25:165–212

    Article  CAS  Google Scholar 

  • Katz M, Hover BM, Brady SF (2015) Culture-independent discovery of natural products from soil metagenomes. J Ind Microbiol Biot 43:129–141

    Article  Google Scholar 

  • Kirst HA (2013) Developing new antibacterials through natural product research. Expert Opinion Drug Dis 8:479–493

    Article  CAS  Google Scholar 

  • Lam KS (2006) Discovery of novel metabolites from marine actinomycetes. Curr Opin Microbiol 9:245–251

    Article  CAS  PubMed  Google Scholar 

  • Lazarkevich I, Tomova A, Kambourova M, Vasileva-Tonkova E (2013) Diversity and biosynthetic potential of culturable aerobic heterotrophic bacteria isolated from Magura cave, Bulgaria. Int J Speleol 42:65–76

    Article  Google Scholar 

  • Li Q, Chen X, Jiang Y, Jiang C (2016) Morphological Identification of Actinobacteria. In: Dhanasekaran D, Jiang Y (eds) Actinobacteria - Basics and Biotechnological Applications. InTech, Rijeka, pp. 59–86

    Google Scholar 

  • Mah TFC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39

    Article  CAS  PubMed  Google Scholar 

  • Manivasagan P, Venkatesan J, Sivakumar K, Kim S-K (2014) Pharmaceutically active secondary metabolites of marine actinobacteria. Microbiol Res 169:262–278

    Article  CAS  PubMed  Google Scholar 

  • Mason C (2015) Screening of cave bacteria for antimicrobial activity against Pseudomonas aeruginosa biofilms. Undergraduate Honours thesis. Thompson Rivers University, Kamloops

    Google Scholar 

  • Mazotto AM, Melo ACN, Macrae A, Rosado AS, Peixoto R, Cedrola SML, Fábio de Lima M, Couri S, Paraguai de Souza E, Vermelho AB (2011) Biodegradation of feather waste by extracelular keratinases and gelatinases from Bacillus spp. World J Microbiol Biotechnol 27:1355–1365

    Article  CAS  PubMed  Google Scholar 

  • McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8 e61217

  • Miao V, Davies J (2010) Actinobacteria: the good, the bad, and the ugly. Anton Leeuw 98:143–150

    Article  Google Scholar 

  • Milshteyn A, Schneider JS, Brady SF (2014) Mining the Metabiome: identifying novel natural products from microbial communities. Chem Biol 21:1211–1223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montano ET, Henderson LO (2013) Studies of antibiotic production by cave bacteria. In: Cheeptham N (ed) Cave microbiomes: a novel resource for drug discovery. Springer-Verlag, New York, pp. 109–130

    Chapter  Google Scholar 

  • Nakaew N, Pathom-aree W, Lumyong S (2009) Generic diversity of rare actinomycetes from Thai cave soils and their possible use as new bioactive compounds. Actinomycetologica 23:21–26

    Article  CAS  Google Scholar 

  • Narayana KJP, Vijayalakshmi M (2009) Chitinase production by Streptomyces sp. ANU 6277. Braz J Microbiol 40:725–733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman DJ, Cragg GM (2012) Natural products as sources of new drugs over the 30 years from 1981 to 2010. J Nat Prod 75:311–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nithya C, Aravindraja C, Pandian SK (2010) Bacillus pumilus of Palk Bay origin inhibits quorum-sensing-mediated virulence factors in gram-negative bacteria. Res Microbiol 161:293–304

    Article  CAS  PubMed  Google Scholar 

  • Nogawa T, Okano A, Takahashi S, Uramoto N, Konno H, Saito T, Osada H (2010) Verticilactam, a new Macrolactam isolated from a microbial metabolite fraction library. Org Lett 12:4564–4567

    Article  CAS  PubMed  Google Scholar 

  • Northup DE, Melim LA, Spilde MN, Hathaway JJM, Garcia MG, Moya M, Stone FD, Boston PJ, Dapkevicius ML, Riquelme C (2011) Lava cave microbial communities within mats and secondary mineral deposits: implications for life detection on other planets. Astrobiology 11:1–18

    Article  Google Scholar 

  • Oksanen JF, Blanchet G, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. (2015) vegan: Community Ecology Package. R package version 2.3–0. URL http://CRAN.R-project.org/package=vegan

  • Owen JG, Charlop-Powers Z, Smith AG, Ternei MA, Calle PY, Reddy BV, Montiel D, Brady SF (2015) Multiplexed metagenome mining using short DNA sequence tags facilitates targeted discovery of epoxyketone proteasome inhibitors. Proc Natl Acad Sci 112:4221–4226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedrolli DB, Monteiro AC, Gomes E, Carmona EC (2009) Pectin and pectinases: production, characterization and industrial application of microbial pectinolytic enzymes. Open Biotechnol J 3:9–18

    Article  CAS  Google Scholar 

  • Prakash D, Nawani N, Prakash M, Bodas M, Mandal A, Khetmalas M (2013) Actinomycetes: a repertory of green catalysts with a potential revenue resource. BioMed Res Int 2013:264020

    Article  PubMed  PubMed Central  Google Scholar 

  • Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quan C, Zhang L, Wang Y, Ohta Y (2001) Production of phytase in a low-phosphate medium by a novel yeast Candida crusei. J Biosci Bioeng 92:154–160

    Article  CAS  PubMed  Google Scholar 

  • Reddy BV, Milshteyn A, Charlop-Powers Z, Brady SF (2014) eSNaPD: a versatile, web-based bioinformatics platform for surveying and mining natural product biosynthetic diversity from metagenomes. Chem Biol 21:1023–1033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riquelme C, Hathaway JJM, Dapkevicius MDLE, Miller AZ, Kooser A, Northup DE, Jurado V, Fernandez O, Saiz-Jimenez C, Cheeptham N (2015a) Actinobacterial diversity in volcanic caves and associated geomicrobiological interactions. Front Microbiol 6:1342

    Article  PubMed  PubMed Central  Google Scholar 

  • Riquelme C, Rigal F, Hathaway JJ, Northup DE, Spilde MN, Borges PA, Gabriel R, Amorim IR, Dapkevicius Mde L. (2015b) Cave microbial community composition in oceanic islands: disentangling the effect of different colored mats in diversity patterns of Azorean lava caves. FEMS Microbiol Ecol 91:fiv141

  • Rule D, Cheeptham N (2013) Effects of UV light on antimicrobial activity of cave actinomycete metabolites. Int J Speleol 42:147–153

    Article  Google Scholar 

  • Sanchez S, Demain AL (2011) Enzymes and bioconversions of industrial, pharmaceutical, and biotechnological significance. Org Process Res Dev 15:224–230

    Article  CAS  Google Scholar 

  • Sánchez-Porro C, Martín S, Mellado E, Ventosa A (2003) Diversity of moderately halophilic bacteria producing extracellular hydrolytic enzymes. J Appl Microbiol 94:295–300

    Article  PubMed  Google Scholar 

  • Shannon CE (1948) A mathematical theory of communication. Bell Sys Tech J 27:379–423 and 623–656

    Article  Google Scholar 

  • Silver LL (2015) Natural products as a source of drug leads to overcome drug resistance. Future Microbiol 10:1711–1718

    Article  CAS  PubMed  Google Scholar 

  • Simpson EH (1949) Measurement of diversity. Nature 163:688

    Article  Google Scholar 

  • Swartjes JJTM, Theerthankar D, Sharifi S, Subbiadoss G, Sharma PK, Krom BP, Busscher HJ, van der Mei HC (2013) A functional DNase I coating to prevent adhesion of bacteria and the formation of biofilm. Adv Funct Mater 23:2843–2849

    Article  CAS  Google Scholar 

  • Terzic-Vidojevic A, Veljovic K, Tolinacki M, Nikolic M, Ostojic M, Topisirovic L (2009) Characterization of lactic acid bacteria isolated from artisanal Zlatar cheeses produced at two different geographical location. Genetika 41:117–136

    Article  Google Scholar 

  • Thenmozhi R, Nithyanand P, Rathna J, Karutha Pandian S (2009) Antibiofilm activity of coral-associated bacteria against different clinical M serotypes of Streptococcus pyogenes. FEMS Immunol Med Microbiol 57:284–294

    Article  CAS  PubMed  Google Scholar 

  • Tiwari K, Gupta RK (2013) Diversity and isolation of rare actinomycetes: an overview. Crit Rev Microbiol 39:257–294

    Article  Google Scholar 

  • Tomova I, Lazarkevich I, Tomova A, Kambourova M, Vasileva-Tonkova E (2013) Diversity and biosynthetic potential of culturable aerobic heterotrophic bacteria isolated from Magura cave, Bulgaria. Int J Speleol 42:65–67

    Article  Google Scholar 

  • Upadhyay RK, Dwivedi P, Ahmad S (2010) Antimicrobial activity of photo-activated cow urine against certain pathogenic bacterial strains. Afr J Biotechnol 9:518–522

    Google Scholar 

  • Walsh CT (2004) Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303:1805–1810

    Article  CAS  PubMed  Google Scholar 

  • Watanabe K (2004) Collagenolytic proteases from bacteria. Appl Microbiol Biot 63:520–526

    Article  CAS  Google Scholar 

  • Wilkins TD, Holdeman LV, Abramson IJ, Moore WEC (1972) Standardized single-disc method for antibiotic susceptibility testing of anaerobic bacteria. Antimicrob Agents Chemother 1:451–459

    Article  CAS  PubMed Central  Google Scholar 

  • Yuan F, Hu C, Hu X, Wei D, Chen Y, Qu J (2011) Photodegradation and toxicity changes of antibiotics in UV and UV/H2O2 process. J Hazard Mater 185:1256–1263

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

C. Riquelme was funded by the Regional Fund for Science and Technology and Pro-Emprego program of the Regional Government of the Azores, Portugal [M3.1.7/F/013/2011, M3.1.7/F/030/2011]. Her work was partly supported by National funds from the Foundation for Science and Technology of the Portuguese Government [Understanding Underground Biodiversity: Studies in Azorean Lava Tubes (reference PTDC/AMB/70801/2006)]. A.Z. Miller acknowledges the support from the Marie Curie Intra-European Fellowship of the European Commission’s 7th Framework Programme (PIEF-GA-2012-328689). The authors would like to thank the TRU Innovation in Research Grant, TRU Undergraduate Research Enhancement (UREAP) Fund, Western Economic Diversification Canada Fund, Kent Watson (assisted with the Helmcken Falls Cave sample collection), Dr. Mario Jacques (U of Montreal for his assistance in biofilm culture), Nicholaus Vieira, Christian Stenner, and the Raspberry Rising Expedition team. We acknowledged the Canadian Ministry of Forests, Lands, and Natural Resource Operations for Park Use Permit#102172. The work done in the Brady lab was funded by NIH grant GM077516. Z. Charlop-Powers was also supported by NIH grant AI110029. The authors also wish to thank Fernando Pereira, Ana Rita Varela, Pedro Correia, Berta Borges, and Guida Pires for help during field and lab work in the Azores. The authors would like to thank Dr. Steven Van Wagoner (TRU) and Drs. Julian Davies and Vivian Miao (UBC) for their invaluable comments in manuscript preparation.

Author information

Authors and Affiliations

  1. Food Science and Health Group (CITA-A), Departamento de Ciências Agrárias, Universidade dos Açores, Angra do Heroísmo, Açores, Portugal

    Cristina Riquelme & Maria de Lurdes Enes Dapkevicius

  2. Instituto de Recursos Naturales y Agrobiología de Sevilla, Consejo Superior de Investigaciones Científicas (IRNAS-CSIC), Sevilla, Spain

    Ana Z. Miller

  3. Laboratory of Genetically Encoded Small Molecules, The Rockefeller University, New York, NY, USA

    Zachary Charlop-Powers & Sean Brady

  4. Department of Biological Sciences, Faculty of Science, Thompson Rivers University, Kamloops, BC, Canada

    Cohord Mason & Naowarat Cheeptham

Authors
  1. Cristina Riquelme
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria de Lurdes Enes Dapkevicius
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana Z. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zachary Charlop-Powers
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sean Brady
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cohord Mason
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Naowarat Cheeptham
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Naowarat Cheeptham.

Ethics declarations

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(PDF 45 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Riquelme, C., Enes Dapkevicius, M.d., Miller, A.Z. et al. Biotechnological potential of Actinobacteria from Canadian and Azorean volcanic caves. Appl Microbiol Biotechnol 101, 843–857 (2017). https://doi.org/10.1007/s00253-016-7932-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-016-7932-7

Keywords

Search

Navigation