Applied Microbiology and Biotechnology

, Volume 101, Issue 16, pp 6563–6572 | Cite as

Carbon and hydrogen isotope fractionation during aerobic biodegradation of quinoline and 3-methylquinoline

  • Mingchao CuiEmail author
  • Wenbing ZhangEmail author
  • Jun Fang
  • Qianqiong Liang
  • Dongxuan Liu
Environmental biotechnology


Compound-specific isotope analysis has been used extensively to investigate the biodegradation of various organic pollutants. To date, little isotope fractionation information is available for the biodegradation of quinolinic compounds. In this study, we report on the carbon and hydrogen isotope fractionation during quinoline and 3-methylquinoline aerobic microbial degradation by a Comamonas sp. strain Q10. Degradation of quinoline and 3-methylquinoline was accompanied by isotope fractionation. Large hydrogen and small carbon isotope fractionation was observed for quinoline while minor carbon and hydrogen isotope fractionation effects occurred for 3-methylquinoline. Bulk carbon and hydrogen enrichment factors (ε bulk) for quinoline biodegradation were −1.2 ± 0.1 and −38 ± 1‰, respectively, while −0.7 ± 0.1 and −5 ± 1‰ for 3-methylquinoline, respectively. This reveals a potential advantage for employing quinoline as the model compound and hydrogen isotope analysis for assessing aerobic biodegradation of quinolinic compounds. The apparent kinetic isotope effects (AKIEC) values of carbon were 1.008 ± 0.0005 for quinoline and 1.0048 ± 0.0005 for 3-methylquinoline while AKIEH values of hydrogen of 1.264 ± 0.011 for quinoline and 1.0356 ± 0.0103 for 3-methylquinoline were obtained. The combined evaluation of carbon and hydrogen isotope fractionation yields Λ values (Λ = Δδ2H/Δδ13C ≈ εHbulk/εCbulk) of 29 ± 2 for quinoline and 8 ± 2 for 3-methylquinoline. The results indicate that the substrate specificity may have a significant influence on the isotope fractionation for the biodegradation of quinolinic compounds. The substrate-specific isotope enrichment factors would be important for assessing the behavior and fate of quinolinic compounds in the environment.


Quinoline 3-Methylquinoline Aerobic biodegradation Isotope fractionation Compound-specific isotope analysis 



This work was financially supported by National Natural Science Foundation of China (NSFC- 41271460 and 40901250).

Compliance with ethical standards

Studies with human participants or animals

This article does not contain any studies with human participants or animals performed by any of the authors. Informed consent was obtained from all individual participants included in the study.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Bai Y, Sun Q, Xing R, Wen D, Tang X (2011) Analysis of denitrifier community in a bioaugmented sequencing batch reactor for the treatment of coking wastewater containing pyridine and quinoline. Appl Microbiol Biotechnol 90:1485–1492CrossRefPubMedGoogle Scholar
  2. Bauder R, Tshisuaka B, Lingens F (1990) Microbial metabolism of quinoline and related-compounds. 7. Quinoline oxidoreductase from Pseudomonas putida—a molybdenum-containing enzyme. Biol Chem Hoppe Seyler 371:1137–1144CrossRefPubMedGoogle Scholar
  3. Bergmann FD, Abu Laban NM, Meyer AH, Elsner M, Meckenstock RU (2011) Dual (C, H) isotope fractionation in anaerobic low molecular weight (poly)aromatic hydrocarbon (PAH) degradation: potential for field studies and mechanistic implications. Environ Sci Technol 45:6947–6953CrossRefPubMedGoogle Scholar
  4. Blaschke M, Kretzer A, Schäfer C, Nagel M, Andreesen JR (1991) Molybdenum-dependent degradation of quinoline by Pseudomonas putida Chin IK and other aerobic bacteria. Arch Microbiol 155:164–169CrossRefPubMedGoogle Scholar
  5. Chartrand MMG, Morrill PL, Lacrampe-Couloume G, Lollar BS (2005) Stable isotope evidence for biodegradation of chlorinated ethenes at a fractured bedrock site. Environ Sci Technol 39:4848–4856CrossRefPubMedGoogle Scholar
  6. Coplen TB (2011) Guidelines and recommended terms for expression of stable isotope-ratio and gas-ratio measurement results. Rapid Commun Mass Spectrom 25:2538–2560CrossRefPubMedGoogle Scholar
  7. Cui MC, Chen FZ, Fu JM, Sheng GY, Sun GP (2003) Cometabolic biodegradation of quinoline’s derivatives by a quinoline-degrading bacteria: Comamonas sp strain Q(10). J Gen Appl Microbiol 49:351–355CrossRefPubMedGoogle Scholar
  8. Cui MC, Chen FZ, Fu JM, Sheng GY, Sun GP (2004) Microbial metabolism of quinoline by Comamonas sp. World J Microbiol Biotechnol 20:539–543CrossRefGoogle Scholar
  9. Elsner M, Zwank L, Hunkeler D, Schwarzenbach RP (2005) A new concept linking observable stable isotope fractionation to transformation pathways of organic pollutants. Environ Sci Technol 39:6896–6916CrossRefPubMedGoogle Scholar
  10. Elsner M (2010) Stable isotope fractionation to investigate natural transformation mechanisms of organic contaminants: principles, prospects and limitations. J Environ Monit 12:2005–2031CrossRefPubMedGoogle Scholar
  11. Fetzner S, Tshisuaka B, Lingens F, Kappl R, Huttermann J (1998) Bacterial degradation of quinoline and derivatives—pathways and their biocatalysts. Angew Chemie-International Ed 37(5):577–597CrossRefGoogle Scholar
  12. Fetzner S (1998) Bacterial degradation of pyridine, indole, quinoline, and their derivatives under different redox conditions. Appl Microbiol Biotechnol 49:237–250CrossRefGoogle Scholar
  13. Fischer A, Gehre M, Breitfeld J, Richnow H-H, Vogt C (2009) Carbon and hydrogen isotope fractionation of benzene during biodegradation under sulfate-reducing conditions: a laboratory to field site approach. Rapid Commun Mass Spectrom 23:2439–2447CrossRefPubMedGoogle Scholar
  14. Fischer A, Herklotz I, Herrmann S, Thullner M, Weelink SAB, Stams AJ, Schlömann M, Richnow HH, Vogt C (2008) Combined carbon and hydrogen isotope fractionation investigations for elucidating benzene biodegradation pathways. Environ Sci Technol 42:4356–4363CrossRefPubMedGoogle Scholar
  15. Fischer A, Weber S, Reineke A-K, Hollender J, Richnow HH (2010) Carbon and hydrogen isotope fractionation during anaerobic quinoline degradation. Chemosphere 81:400–407CrossRefPubMedGoogle Scholar
  16. Hille R, Hall J, Basu P (2014) The mononuclear molybdenum enzymes. Chem Rev 114(7):3963–4038CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hirschorn SK, Dinglasan MJ, Elsner M, Mancini SA, Lacrampe-Couloume G, Edwards EA, Lollar BS (2004) Pathway dependent isotopic fractionation during aerobic biodegradation of 1,2-dichloroethane. Environ Sci Technol 38:4775–4781CrossRefPubMedGoogle Scholar
  18. Hunkeler D, Aravena R, Berry-Spark K, Cox E (2005) Assessment of degradation pathways in an aquifer with mixed chlorinated hydrocarbon contamination using stable isotope analysis. Environ Sci Technol 39:5975–5981CrossRefPubMedGoogle Scholar
  19. Johansen SS, Hansen AB, Mosbaek H, Arvin E (1997) Identification of heteroaromatic and other organic compounds in ground water at creosote contaminated sites in Denmark. Ground Water Monit R 17:106–115CrossRefGoogle Scholar
  20. Liang X, Howlett MR, Nelson JL, Grant G, Dworatzek S, Lacrampe-Couloume G, Zinder SH, Edwards EA, Sherwood Lollar B (2011) Pathway-dependent isotope fractionation during aerobic and anaerobic degradation of monochlorobenzene and 1,2,4-trichlorobenzene. Environ Sci Technol 45:8321–8327Google Scholar
  21. Mancini SA, Devine CE, Elsner M, Nandi ME, Ulrich AC, Edwards EA, Lollar BS (2008) Isotopic evidence suggests different initial reaction mechanisms for anaerobic benzene biodegradation. Environ Sci Technol 42:8290–8296CrossRefPubMedGoogle Scholar
  22. Mckelvie JR, Hyman MR, Elsner M, Smith C, Aslett DM, Lacrampe-Couloume G, Lollar BS (2009) Isotopic fractionation of methyl tert-butyl ether suggests different initial reaction mechanisms during aerobic biodegradation. Environ Sci Technol 43:2793–2799CrossRefPubMedGoogle Scholar
  23. Meckenstock RU, Morasch B, Griebler C, Richnow HH (2004) Stable isotope fractionation analysis as a tool to monitor biodegradation in contaminated acquifers. J Contam Hydrol 75:215–255CrossRefPubMedGoogle Scholar
  24. Metz S, Thiel W (2011) Theoretical studies on the reactivity of molybdenum enzymes. Coord Chem Rev 255(9–10):1085–1103CrossRefGoogle Scholar
  25. Morasch B, Richnow HH, Schink B, Vieth A, Meckenstock RU (2002) Carbon and hydrogen stable isotope fractionation during aerobic bacterial degradation of aromatic hydrocarbons. Appl Environ Microbiol 68:5191–5194CrossRefPubMedPubMedCentralGoogle Scholar
  26. Nagao M, Yahagi T, Seino Y, Sugimura T, Ito N (1977) Mutagenicities of quinoline and its derivatives. Mutat Res 42:335–342CrossRefPubMedGoogle Scholar
  27. Nijenhuis I, Richnow HH (2016) Stable isotope fractionation concepts for characterizing biotransformation of organohalides. Curr Opin Biotechnol 41:108–113CrossRefPubMedGoogle Scholar
  28. Northrop DB (1981) The expression of isotope effects on enzyme-catalyzed reactions. Annu Rev Biochem 50:103–131CrossRefPubMedGoogle Scholar
  29. Padoley KV, Mudliar SN, Pandey RA (2008) Heterocyclic nitrogenous pollutants in the environment and their treatment options—an overview. Bioresour Technol 99:4029–4043CrossRefPubMedGoogle Scholar
  30. Palau J, Jamin P, Badin A, Vanhecke N, Haerens B, Brouyère S, Hunkeler D (2016) Use of dual carbon-chlorine isotope analysis to assess the degradation pathways of 1,1,1-trichloroethane in groundwater. Water Res 92:235–243CrossRefPubMedGoogle Scholar
  31. Peschke B, Lingens F (1991) Microbial metabolism of quinoline and related compounds. XII. Isolation and characterization of the quinoline oxidoreductase from Rhodococcus spec. B1 compared with the quinoline oxidoreductase from Pseudomonas putida 86. Biol Chem Hoppe Seyler 372(12):1081–1088CrossRefPubMedGoogle Scholar
  32. Philipp B, Hoff M, Germa F, Schink B, Beimborn D, Mersch-Sundermann V (2007) Biochemical interpretation of quantitative structure-activity relationships (QSAR) for biodegradation of N-heterocycles: a complementary approach to predict biodegradability. Environ Sci Technol 41:1390–1398CrossRefPubMedGoogle Scholar
  33. Reineke A-K, Preiss A, Elend M, Hollender J (2008) Detection of methylquinoline transformation products in microcosm experiments and in tar oil contaminated groundwater using LC-NMR. Chemosphere 70:2118–2126CrossRefPubMedGoogle Scholar
  34. Schach S, Tshisuaka B, Fetzner S, Lingens F (1995) Quinoline 2-oxidoreductase and 2-oxo-1,2-dihydroquinoline 5,6-dioxygenase from Comamonas testosteroni 63. The first two enzymes in quinoline and 3-methylquinoline degradation. Eur J Biochem 232:536–544CrossRefPubMedGoogle Scholar
  35. Schwartz G, Bauder R, Speer M, TO R, Lingens F (1989) Microbial metabolism of quinoline and related compounds. II. Degradation of quinoline by Pseudomonas fluorescens 3, Pseudomonas putida 86 and Rhodococcus spec. B1. Biol Chem Hoppe Seyler 370:1183–1189CrossRefGoogle Scholar
  36. Tobler NB, Hofstetter TB, Schwarzenbach RP (2008) Carbon and hydrogen isotope fractionation during anaerobic toluene oxidation by Geobacter metallireducens with different Fe(III) phases as terminal electron acceptors. Environ Sci Technol 42:7786–7792Google Scholar
  37. Vogt C, Cyrus E, Herklotz I, Schlosser D, Bahr A, Herrmann S, Richnow HH, Fischer A (2008) Evaluation of toluene degradation pathways by two-dimensional stable isotope fractionation. Environ Sci Technol 42:7793–7800CrossRefPubMedGoogle Scholar
  38. Wang L, Li Y, Duan J (2014) Biodegradation of 2-methylquinoline by Klebsiella pneumoniae TJ-A isolated from acclimated activated sludge. J Environ Sci Heal Part A-Toxic/Hazardous Subst Environ Eng 49:27–38CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.School of Environmental Science and EngineeringGuangzhou UniversityGuangzhouChina
  2. 2.Guangdong Provincial Key Laboratory of Radioactive Contamination Control and ResourcesGuangzhou UniversityGuangzhouChina
  3. 3.State Key Laboratory of Organic Geochemistry, Guangzhou Institute of GeochemistryChinese Academy of SciencesGuangzhouChina

Personalised recommendations