Advertisement

Current Microbiology

, Volume 70, Issue 3, pp 307–314 | Cite as

Drotaverine Hydrochloride Degradation Using Cyst-like Dormant Cells of Rhodococcus ruber

  • Irena B. Ivshina
  • Anna N. Mukhutdinova
  • Helena A. Tyumina
  • Helena V. Vikhareva
  • Nataliya E. Suzina
  • Galina I. El’-Registan
  • Andrey L. Mulyukin
Article

Abstract

This work has a focus on adaptive capabilities of the actinobacterium Rhodococcus ruber IEGM 326 to cope with drotaverine hydrochloride (DH), a known pharmaceutical pollutant. Cultivation of R. ruber in a nitrogen-limited medium with incubation at the ambient temperature resulted in the formation of cyst-like dormant cells (CLDCs). They maintained viability for 2–7 months, possessed the undetectable respiratory activity and elevated resistance to heating, and had a specific morphology. CLDCs are regarded to ensure long-term survival in various habitats and may be used as storage formulations. R. ruber IEGM 326 was tolerant to DH (MIC, 200 mg/l) and displayed different abilities to degrade this compound, depending on inoculum, temperature, and the presence of glucose as co-oxidized substrate. Thus, the loss of DH (20 mg/l) over 48 h at the optimal temperature (27 ± 2 °C) was 5–8 % in the absence of glucose after inoculating with vegetative cells. The addition of glucose (5 g/l) increased DH degradation up to 46 %. Noteworthy, CLDCs as inoculum were advantageous over vegetative cells to degrade DH at the non-optimal temperature (35 ± 2 °C) at reduced bulk respiratory activity. The obtained results are promising to improve the biodegrading capabilities of other Rhodococcus strains.

Keywords

Vegetative Cell Rhodococcus Respiratory Activity Mycobacterium Smegmatis Dormant Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The research was partially supported by the Grant of the Russian Academy of Sciences Presidium Program “Leaving Nature: Current State and Development Problems” (01201256869) and the Russian Scientific Foundation Grant (14-14-00643).

Supplementary material

284_2014_718_MOESM1_ESM.pdf (373 kb)
Online Resource 1 Morphology of Rhodococcus ruber IEGM 326. Vegetative cells and CLDCs in a phase contrast microscope (a) and TEM images of CLDCs (c, d) (SR1 medium, N-limited, 4-month-old cultures). Designations: CW, cell wall; CL, capsular layer; I, electron-transparent inclusions. Scale bars: 1 μm for micrographs of cell sections and 2 μm for light microscopy images
284_2014_718_MOESM2_ESM.pdf (30 kb)
Online Resource 2 Thermal resistance (% of the control) of R. ruber IEGM 326: vegetative cells (1) and CLDCs at different ages: 2 months (2) and 7 months (3) to heating at 55–90 °C for 10 min
284_2014_718_MOESM3_ESM.pdf (41 kb)
Online Resource 3 Respiration rate (a) and CO2 release dynamics (b) during DH biodegradation as the sole carbon and energy source in the medium inoculated with vegetative cell (3) and CLDC (2) suspensions of R. ruber IEGM 326. Cultures were incubated at 35 °C. Un-inoculated (abiotic) controls (1)
284_2014_718_MOESM4_ESM.pdf (37 kb)
Online Resource 4 Respiration rate (a) and CO2 release dynamics (b) during DH biodegradation in glucose-supplemented medium following inoculations with vegetative cell (3) and CLDC (2) suspensions of R. ruber IEGM 326. Un-inoculated (abiotic) controls (1). Cultures were incubated at 27 °C
284_2014_718_MOESM5_ESM.pdf (45 kb)
Online Resource 5 Chromatographic separation of DH metabolites produced by R. ruber IEGM 326 vegetative cells. Mass spectra of DH (m/z = 411.2) as well as of protocatechuic acid derivates (m/z = 137.0; 193.0; 109.0; 239.84) accumulated in the RS medium. The same product was identified when CLDCs were used as inocula (spectra are not shown here)

References

  1. 1.
    Adam W, Luckacs Z, Kahle C, Saha-Möller CR, Schreier P (2001) Biocatalytic asymmetric hydroxylation of hydrocarbons by free and immobilized Bacillus megaterium cells. J Mol Catal B Enzym 11:377–385. doi: 10.1016/S1381-1177(00)00028-X CrossRefGoogle Scholar
  2. 2.
    Alvarez HM, Silva RA, Cesari AC, Zamit AL, Peressutti SR, Reichelt R, Keller U, Malkus U, Rasch C, Maskow T, Mayer F, Steinbüchel A (2004) Physiological and morphological responses of the soil bacterium Rhodococcus opacus strain PD630 to water stress. FEMS Microbiol Ecol 50(2):75–86. doi: 10.1016/j.femsec.2004.06.002 PubMedCrossRefGoogle Scholar
  3. 3.
    Anuchin AM, Mulyukin AL, Suzina NE, Duda VI, El’-Registan GI, Kaprelyants AS (2009) Dormant forms of Mycobacterium smegmatis with distinct morphology. Microbiology 155:1071–1079. doi: 10.1099/mic.0.023028-0 PubMedCrossRefGoogle Scholar
  4. 4.
    Bell KS, Kuyukina MS, Heidbrink S, Philp JC, Aw DWJ, Ivshina IB, Christofi N (1999) Identification and environmental detection of Rhodococcus species by 16S rDNA-targeted PCR. J Appl Microbiol 87:472–480. doi: 10.1046/j.1365-2672.1999.00824.x PubMedCrossRefGoogle Scholar
  5. 5.
    Bessems JG, Vermeulen NP (2001) Paracetamol (acetaminophen)-induced toxicity: molecular and biochemical mechanisms, analogues and protective approaches. Crit Rev Toxicol 31(1):55–138PubMedCrossRefGoogle Scholar
  6. 6.
    Celiz MD, Tso J, Aga DS (2009) Pharmaceutical metabolites in the environment: analytical challenges and ecological risks. Environ Toxicol Chem 28(12):2473–2484. doi: 10.1897/09-173.1 PubMedCrossRefGoogle Scholar
  7. 7.
    de Carvalho CCCR, Costa SC, Fernandes P, Couto I, Viveiros M (2014) Membrane transport systems and the biodegradation potential and pathogenicity of genus Rhodococcus. Front Physiol 5:133. doi: 10.3389/fphys.2014.00133 PubMedCentralPubMedGoogle Scholar
  8. 8.
    de Carvalho CCCR, da Fonseca MMR (2005) The remarkable Rhodococcus erythropolis. Appl Microbiol Biotechnol 67:715–726. doi: 10.1007/s00253-005-1932-3 PubMedCrossRefGoogle Scholar
  9. 9.
    Duca G, Boldescu V (2009) Pharmaceuticals and personal care products in the environment. In: Bahadir AM, Duca G (eds) The role of ecological chemistry in pollution research and sustainable development. Springer, Dordrecht, pp 27–35. doi: 10.1007/978-90-481-2903-4_3 CrossRefGoogle Scholar
  10. 10.
    El’-Registan GI, Mulyukin AL, Nikolaev YuA, Suzina NE, Gal’chenko VF, Duda VI (2006) Adaptogenic functions of extracellular autoregulators of microorganisms. Microbiology 75(4):380–389. doi: 10.1134/S0026261706040035 CrossRefGoogle Scholar
  11. 11.
    Endreffy E, Boda D (1983) Effect of drugs used in obstetrics on the constriction by oxygen of the ductus arteriosus of the rabbit fetus. Acta Paediatr Hung 24(3):281–285PubMedGoogle Scholar
  12. 12.
    Gauthier H, Yargeau V, Cooper DG (2010) Biodegradation of pharmaceuticals by Rhodococcus rhodochrous and Aspergillus niger by co-metabolism. Sci Total Environ 408:1701–1706. doi: 10.1016/j.scitotenv.2009.12.012 PubMedCrossRefGoogle Scholar
  13. 13.
    Ivshina IB (2012) Current situation and challenges of specialized microbial resource centres in Russia. Microbiology 81(5):509–516. doi: 10.1134/S0026261712050098 CrossRefGoogle Scholar
  14. 14.
    Ivshina IB, Kuyukina MS, Krivoruchko AV, Plekhov OA, Naimark OB, Podorozhko EA, Lozinsky VI (2013) Biosurfactant-enhanced immobilization of hydrocarbon-oxidizing Rhodococcus ruber on sawdust. Appl Microbiol Biotechnol 97(12):5315–5327. doi: 10.1007/s00253-013-4869-y PubMedCrossRefGoogle Scholar
  15. 15.
    Ivshina IB, Kuyukina MS, Philp JC, Christofi N (1998) Oil desorption from mineral and organic materials using biosurfactant complexes produced by Rhodococcus species. World J Microbiol Biotechnol 14:711–717CrossRefGoogle Scholar
  16. 16.
    Ivshina IB, Peshkur TA, Korobov VP (2002) Efficient uptake of cesium ions by Rhodococcus cells. Mikrobiologiia 71(3):357–361. doi: 10.1023/a:1015875216095 Google Scholar
  17. 17.
    Ivshina IB, Vikhareva EV, Richkova MI, Mukhutdinova AN, Karpenko JuN (2012) Biodegradation of drotaverine hydrochloride by free and immobilized cells of Rhodococcus rhodochrous IEGM 608. World J Microbiol Biotechnol 28:2997–3006. doi: 10.1007/s11274-012-1110-6 PubMedCrossRefGoogle Scholar
  18. 18.
    Iwabuchi N, Sunairi M, Anzai H, Nakajima M, Harayama S (2000) Relationships between colony morphotypes and oil tolerance in Rhodococcus rhodochrous. Appl Environ Microbiol 66(11):5073–5077. doi: 10.1128/AEM.66.11.5073-5077.2000 PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Kim Y-U, Han J, Lee SS, Shimizu K, Tsutsumi Y, Kondo R (2007) Steroid 9α-hydroxylation during testosterone degradation by resting Rhodococcus equi cells. Arch Pharm Chem Life Sci 340:209–214. doi: 10.1002/ardp.200600175 CrossRefGoogle Scholar
  20. 20.
    Kolomytseva MP, Solyanikova IP, Golovlev EL, Golovleva LA (2005) Heterogeneity of Rhodococcus opacus 1CP as a response to stress induced by chlorophenols. Appl Biochim Microbiol 41(5):474–479. doi: 10.1007/s10438-005-0085-6 CrossRefGoogle Scholar
  21. 21.
    Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999–2000: a national reconnaissance. Environ Sci Technol 36:1202–1211. doi: 10.1021/es011055j PubMedCrossRefGoogle Scholar
  22. 22.
    Kuyukina MS, Ivshina IB (2010) Rhodococcus biosurfactants: biosynthesis, properties, and potential application. In: Alvarez HM (ed) Biology of Rhodococcus, microbiology monographs, vol 16. Springer, Berlin, pp 291–313. doi: 10.1007/978-3-642-12937-7_11 Google Scholar
  23. 23.
    Lalumera GM, Calamari D, Galli P, Castiglioni S, Crosa G, Fanelli R (2004) Preliminary investigation on the environmental occurrence and effects of antibiotics used in aquaculture in Italy. Chemosphere 54:661–668. doi: 10.1016/j.chemosphere.2003.08.001 PubMedCrossRefGoogle Scholar
  24. 24.
    Larkin MJ, Kulakov LA, Allen CCR (2005) Biodegradation and Rhodococcus: masters of catabolic versatility. Curr Opin Biotechnol 16:282–290PubMedCrossRefGoogle Scholar
  25. 25.
    Larkin MJ, Kulakov LA, Allen CCR (2006) Biodegradation by members of the genus Rhodococcus: biochemistry, physiology, and genetic adaptation. Adv Appl Microbiol 59:1–29. doi: 10.1016/S0065-2164(06)59001-X PubMedCrossRefGoogle Scholar
  26. 26.
    Leilei Z, Mingxin H, Suiyi Z (2012) Biodegradation of p-nitrophenol by immobilized Rhodococcus sp. strain Y-1. Chem Biochem Eng Q 26(2):137–144Google Scholar
  27. 27.
    Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130PubMedCrossRefGoogle Scholar
  28. 28.
    Marchand P, Rosenfeld E, Erable B, Maugard T, Lamare S, Goubet I (2008) Coupled oxidation–reduction of butanol–hexanal by resting Rhodococcus erythropolis NCIMB 13064 cells in liquid and gas phases. Enzyme Microb Technol 43(6):423–430. doi: 10.1016/j.enzmictec.2008.07.004 CrossRefGoogle Scholar
  29. 29.
    Martínková L, Uhnáková B, Pátek M, Nešvera J, Křen V (2009) Biodegradation potential of the genus Rhodococcus. Environ Int 35:162–177. doi: 10.1006/j.envint.2008.07.018 PubMedCrossRefGoogle Scholar
  30. 30.
    Morita R (1982) Starvation-survival of heterotrophs in the marine environment. Adv Microb Ecol 6:171–178CrossRefGoogle Scholar
  31. 31.
    Mulyukin AL, Kozlova AN, El’-Registan GI (2008) Properties of the phenotypic variants of Pseudomonas aurantiaca and P. fluorescens. Microbiology 77(6):681–690. doi: 10.11134/S0026261708060052 CrossRefGoogle Scholar
  32. 32.
    Mulyukin AL, Kudykina YUK, Shleeva MO, Anuchin AM, Suzina NE, Danilevich VN, Duda VI, Kaprelyants AS, El’-Registan GI (2010) Intraspecies diversity of dormant forms of Mycobacterium smegmatis. Microbiology 79(4):461–471. doi: 10.1134/S0026261710040089 CrossRefGoogle Scholar
  33. 33.
    Mulyukin AL, Suzina NE, Pogorelova AYu, Antonyuk LP, Duda VI, El’-Registan GI (2009) Diverse morphological types of dormant cells and conditions for their formation in Azospirillum brasilense. Microbiology 78(1):33–41. doi: 10.1134/S0026261709010056 CrossRefGoogle Scholar
  34. 34.
    Nallapan Maniyam M, Sjahrir F, Ibrahim AL (2011) Bioremediation of cyanide by optimized resting cells of Rhodococcus strains isolated from Peninsular Malaysia. Int J Biosci Biochem Bioinform 1(2):98–101. doi: 10.7763/IJBBB.2011.V1.18 Google Scholar
  35. 35.
    Nallapan Maniyam M, Sjahrir F, Ibrahim AL, Cass AEG (2013) Biodegradation of cyanide by Rhodococcus UKMP-5M. Biologia 68(2):177–185. doi: 10.2478/s11756-013-0158-6 CrossRefGoogle Scholar
  36. 36.
    Narvaez JFV, Jimenez CC (2012) Pharmaceutical products in the environment: sources, effects and risks. Vitae 19(1):93–108Google Scholar
  37. 37.
    Nikolaou A (2013) Pharmaceuticals and related compounds as emerging pollutants in water: analytical aspects. Global NEST J 15(1):1–12Google Scholar
  38. 38.
    Reynolds E (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–212. doi: 10.1083/jcb.17.1.208 PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Soina VS, Mulyukin AL, Demkina EV, Vorobyova EA, El-Registan GI (2004) The structure of resting microbial populations in soil and subsoil permafrost. Astrobiology 4(3):348–358. doi: 10.1089/ast.2004.4.345 CrossRefGoogle Scholar
  40. 40.
    Solyanikova IP, Mulyukin AL, Suzina NE, El’-Registan GI, Golovleva LA (2011) Improved xenobiotic-degrading activity of Rhodococcus opacus strain 1cp after dormancy. J Environ Sci Health B 46(7):638–647. doi: 10.1080/03601234.2011.594380 PubMedCrossRefGoogle Scholar
  41. 41.
    Sudo SZ, Dworkin M (1973) Comparative biology of procaryotic resting cells. Adv Microbiol Physiol 9:153–224. doi: 10.1016/S0065-2911(08)60378-1 CrossRefGoogle Scholar
  42. 42.
    Suzina NE, Muliukin AL, Kozlova AN, Shorokhova AP, Dmitriev VV, Barinova ES, Mokhova ON, El’-Registan GI, Duda VI (2004) Ultrastructure of resting cells of some non-spore-forming bacteria. Mikrobiologiia 73(4):35–447. doi: 10.1023/B:MICI.0000036990.94039.af Google Scholar
  43. 43.
    Suttinun O, Müller R, Luepromchai E (2010) Cometabolic degradation of trichloroethene by Rhodococcus sp. strain L4 immobilized on plant materials rich in essential oils. Appl Environ Microbiol 76(14):4684–4690. doi: 10.1128/AEM.03036-09 PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Ternes TA (1998) Occurrence of drugs in German sewage treatment plants and rivers. Water Res 32:3245–3260. doi: 10.1016/S0043-1354(98)00099-2 CrossRefGoogle Scholar
  45. 45.
    Veeranagouda Y, Lim EJ, Kim DW, Kim JK, Cho K, Heipieper HJ, Lee K (2009) Formation of specialized aerial architectures by Rhodococcus during utilization of vaporized p-cresol. Microbiology 155:3788–3796. doi: 10.1099/mic.0.029926-0 PubMedCrossRefGoogle Scholar
  46. 46.
    Yoshimoto T, Nagai F, Fujimoto J, Watanabe K, Mizukoshi H, Makino T, Kimura K, Saino H, Sawada H, Omura H (2004) Degradation of estrogens by Rhodococcus zopfii and Rhodococcus equi isolates from activated sludge in wastewater treatment plants. Appl Environ Microbiol 70(9):5283–5289. doi: 10.1128/AEM.70.9.5283-5289.2004 PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Irena B. Ivshina
    • 1
    • 2
  • Anna N. Mukhutdinova
    • 1
  • Helena A. Tyumina
    • 2
  • Helena V. Vikhareva
    • 3
  • Nataliya E. Suzina
    • 4
  • Galina I. El’-Registan
    • 5
  • Andrey L. Mulyukin
    • 5
  1. 1.Institute of Ecology and Genetics of MicroorganismsRussian Academy of SciencesPermRussia
  2. 2.Microbiology and Immunology DepartmentPerm State National Research UniversityPermRussia
  3. 3.Perm State Pharmaceutical AcademyPermRussia
  4. 4.Skryabin Institute of Biochemistry and Physiology of MicroorganismsRussian Academy of SciencesMoscowRussia
  5. 5.Winogradsky Institute of MicrobiologyRussian Academy of SciencesMoscowRussia

Personalised recommendations