Advertisement

Applied Microbiology and Biotechnology

, Volume 97, Issue 20, pp 8923–8930 | Cite as

Application of micro-segmented flow for two-dimensional characterization of the combinatorial effect of zinc and copper ions on metal-tolerant Streptomyces strains

  • Jialan Cao
  • Dana Kürsten
  • Katrin Krause
  • Erika Kothe
  • Karin Martin
  • Martin Roth
  • J. Michael Köhler
Biotechnological products and process engineering

Abstract

The cultivation and growth behavior of metal-tolerant strains of Streptomyce acidiscabies E13 and Streptomyces sp. F4 were studied under droplet-based microfluidics conditions. It was shown that the technique of micro segmented flow is well suited for the investigation of dependence of bacterial growth on different concentrations of either single metal ions or combinations of them. This study confirms higher tolerance to Zn than to Cu by our test organism. The highly resolved dose–response curves reflect two transitions between the different growth behaviors, separating initial responses to Cu concentration ranges into those with (a) intense growth, (b) moderate growth, and (c) growth inhibition. For Streptomyces sp. F4, an initial stimulation was shown in the sublethal range of zinc sulfate. Two-dimensional screenings using computer-controlled fluid actuation and in situ micro flow-through fluorimetry reflected a strong growth stimulation of strain F4 by zinc sulfate in the presence of sublethal Cu concentrations. This stimulatory effect on binary mixtures may be useful in providing optimal growth conditions in bioremediation procedures.

Keywords

Droplet-based microfluidics Segmented flow Streptomyces Heavy metal resistance Combinatorial effects Bioremediation 

Notes

Acknowledgments

The financial support of the German Federal Ministry of Education and Research (BMBF) in the frame of the project “BactoCat” (Kz: 031A161A) is gratefully acknowledged. J. Cao is financially supported by the German Federal Environmental Foundation.

References

  1. Admiraal W, Blanck H, Buckert-De Jong M, Guasch H, Ivorra N, Lehmann V, Nystrom BAH, Paulsson M, Sabater S (1999) Short-term toxicity of zinc to microbenthic algae and bacteria in a metal polluted stream. Water Res 33:1989–1996CrossRefGoogle Scholar
  2. Amoroso MJ, Schubert D, Mitscherlich P, Schumann P, Kothe E (2000) Evidence for high affinity nickel transporter genes in heavy metal resistant Streptomyces spec. J Basic Microb 40:295–301CrossRefGoogle Scholar
  3. Barbulovic-Nad I, Yang H, Park PS, Wheeler AR (2008) Digital microfluidics for cell-based assays. Lab Chip 8:519–526CrossRefPubMedGoogle Scholar
  4. Blinova I, Ivask A, Heinlaan M, Mortimer M, Kahru A (2010) Ecotoxicity of nanoparticles of CuO and ZnO in natural water. Environ Pollut 158:41–47CrossRefPubMedGoogle Scholar
  5. Cao JL, Kursten D, Schneider S, Knauer A, Gunther PM, Kohler JM (2012) Uncovering toxicological complexity by multi-dimensional screenings in microsegmented flow: modulation of antibiotic interference by nanoparticles. Lab Chip 12:474–484CrossRefPubMedGoogle Scholar
  6. Churski K, Kaminski TS, Jakiela S, Kamysz W, Baranska-Rybak W, Weibel DB, Garstecki P (2012) Rapid screening of antibiotic toxicity in an automated microdroplet system. Lab Chip 12:1629–1637CrossRefPubMedGoogle Scholar
  7. Clausell-Tormos J, Merten CA (2012) Micro segmented-flow in biochemical and cell-based assays. Front Biosci 4:1768–1779 (Elite Ed)Google Scholar
  8. Costa JSD, Kothe E, Abate CM, Amoroso MJ (2012) Unraveling the Amycolatopsis tucumanensis copper-resistome. Biometals 25:905–917CrossRefGoogle Scholar
  9. Franklin NM, Stauber JL, Lim RP, Petocz P (2002) Toxicity of metal mixtures to a tropical freshwater alga (Chlorella sp.): The effect of interactions between copper, cadmium, and zinc on metal cell binding and uptake. Environ Toxicol Chem 21:2412–2422PubMedGoogle Scholar
  10. Funfak A, Brosing A, Brand M, Kohler JM (2007) Micro fluid segment technique for screening and development studies on Danio rerio embryos. Lab Chip 7:1132–1138CrossRefPubMedGoogle Scholar
  11. Funfak A, Hartung R, Cao JL, Martin K, Wiesmuller KH, Wolfbeis OS, Kohler JM (2009) Highly resolved dose–response functions for drug-modulated bacteria cultivation obtained by fluorometric and photometric flow-through sensing in microsegmented flow. Sensor Actuat B-Chem 142:66–72CrossRefGoogle Scholar
  12. Funfak A, Cao JL, Knauer A, Martin K, Kohler JM (2011) Synergistic effects of metal nanoparticles and a phenolic uncoupler using microdroplet-based two-dimensional approach. J Environ Monitor 13:410–415CrossRefGoogle Scholar
  13. Gherbal R, Hamed H, Foth H (2011) The effect of zinc ions on expression of metallothionein and poly (ADP-ribose) polymerase-1 in human lung cells. Toxicol Lett 205:S160CrossRefGoogle Scholar
  14. Gunther PM, Schneider S, Groß GA, Kohler JM (2011) Addressing of multidimensional concentration spaces by micro segmented flow technique. Proc Mikrosyst Technol CongrDarmst 10:945–947Google Scholar
  15. Haferburg G, Kothe E (2010) Metallomics: lessons for metalliferous soil remediation. Appl Microbiol Biot 87:1271–1280CrossRefGoogle Scholar
  16. Ince NH, Dirilgen N, Apikyan IG, Tezcanli G, Ustun B (1999) Assessment of toxic interactions of heavy metals in binary mixtures: a statistical approach. Arch Environ Con Tox 36:365–372CrossRefGoogle Scholar
  17. Kalantari N, Ghaffari S (2008) Evaluation of toxicity of heavy metals for Escherichia coli growth. Iran J Environ Health 5:173–178Google Scholar
  18. Kohler JM, Henkel T, Grodrian A, Kirner T, Roth M, Martin K, Metze J (2004) Digital reaction technology by micro segmented flow—components, concepts and applications. Chem Eng J 101:201–216CrossRefGoogle Scholar
  19. Kuersten D, Cao J, Funfak A, Mueller P, Köhler JM (2011) Cultivation of Chlorella vulgaris in microfluid segments and microtoxicological determination of their sensitivity against CuCl2 in the nanoliter range. Eng Life Sci 11:1–8CrossRefGoogle Scholar
  20. Le TTY, Vijver MG, Hendriks AJ, Peijnenburg WJGM (2013) Modeling toxicity of binary metal mixtures (Cu2+–Ag+, Cu2+–Zn2+) to lettuce, Lactuca sativa, with the biotic ligand model. Environ Toxicol Chem 32:137–143CrossRefGoogle Scholar
  21. Malik A (2004) Metal bioremediation through growing cells. Environ Int 30:261–278CrossRefPubMedGoogle Scholar
  22. Martin K, Henkel T, Baier V, Grodrian A, Schon T, Roth M, Kohler JM, Metze J (2003) Generation of larger numbers of separated microbial populations by cultivation in segmented-flow microdevices. Lab Chip 3:202–207CrossRefPubMedGoogle Scholar
  23. Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ, Quigg A, Santschi PH, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17:372–386CrossRefPubMedGoogle Scholar
  24. Nies AT, Damme K, Schaeffeler E, Schwab M (2012) Multidrug and toxin extrusion proteins as transporters of antimicrobial drugs. Expert Opin Drug Met 8:1565–1577CrossRefGoogle Scholar
  25. Rademacher C, Masepohl B (2012) Copper-responsive gene regulation in bacteria. Microbiol-Uk 158:2451–2464CrossRefGoogle Scholar
  26. Sani RK, Peyton BM, Brown LT (2001) Copper-induced inhibition of growth of Desulfovibrio desulfuricans G20: assessment of its toxicity and correlation with those of zinc and lead. Appl Environ Microb 67:4765–4772CrossRefGoogle Scholar
  27. Schmidt A, Haferburg G, Sineriz M, Merten D, Buchel G, Kothe E (2005) Heavy metal resistance mechanisms in actinobacteria for survival in AMD contaminated soils. Chem Erde-Geochem 65:131–144CrossRefGoogle Scholar
  28. Schmidt A, Schmidt A, Haferburg G, Kothe E (2007) Superoxide dismutases of heavy metal resistant streptomycetes. J Basic Microb 47:56–62CrossRefGoogle Scholar
  29. Schmidt A, Haferburg G, Schmidt A, Lischke U, Merten D, Ghergel F, Buchel G, Kothe E (2009) Heavy metal resistance to the extreme: Streptomyces strains from a former uranium mining area. Chem Erde-Geochem 69:35–44CrossRefGoogle Scholar
  30. Schmidt A, Rzanny M, Schmidt A, Hagen M, Schutze E, Kothe E (2012) GC content-independent amino acid patterns in Bacteria and Archaea. J Basic Microb 52:195–205CrossRefGoogle Scholar
  31. Theberge AB, Courtois F, Schaerli Y, Fischlechner M, Abell C, Hollfelder F, Huck WTS (2010) Microdroplets in microfluidics: an evolving platform for discoveries in chemistry and biology. Angew Chem Int Edit 49:5846–5868CrossRefGoogle Scholar
  32. Utgikar VP, Tabak HH, Haines JR, Govind R (2003) Quantification of toxic and inhibitory impact of copper and zinc on mixed cultures of sulfate-reducing bacteria. Biotechnol Bioeng 82:306–312CrossRefPubMedGoogle Scholar
  33. Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208CrossRefPubMedGoogle Scholar
  34. Zheng B, Tice JD, Ismagilov RF (2004) Formation of droplets of alternating composition in microfluidic channels and applications to indexing of concentrations in droplet-based assays. Anal Chem 76:4977–4982CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Jialan Cao
    • 1
  • Dana Kürsten
    • 1
  • Katrin Krause
    • 2
  • Erika Kothe
    • 2
  • Karin Martin
    • 3
  • Martin Roth
    • 3
  • J. Michael Köhler
    • 1
  1. 1.Institute of Micro- and Nanotechnologies/Institute for Chemistry and Biotechnology, Dept. of Phys. Chem. and Microreaction TechnologyIlmenau University of TechnologyIlmenauGermany
  2. 2.Institute of Microbiology, Microbial CommunicationFriedrich-Schiller-UniversityJenaGermany
  3. 3.Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute, Bio Pilot PlantJenaGermany

Personalised recommendations