Skip to main content
SpringerLink
Log in

Mechanism study of cyfluthrin biodegradation by Photobacterium ganghwense with comparative metabolomics

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

Abstract

A high-efficiency pyrethroid-degrading bacterium, Photobacterium ganghwense strain 6046 (PGS6046), was first isolated from an offshore seawater environment. Metabolomics method was used to investigate the biotransformation pathway of PGS6046 to cyfluthrin wherein 156 metabolites were identified. The growth rates of the PGS6046 cultivated in nourishing media were much higher than those cultivated in seawater, regardless of the presence of cyfluthrin. Statistical analyses revealed that the metabolic profile of PGS6046 was associated with the culture medium, the presence of cyfluthrin, and culture time. The PGS6046 cultivated in a nourishing medium was characterized by higher levels of amino acids, a lower abundance of intermediates in the tricarboxylic acid cycle, and the presence of some fatty acids than those cultivated in seawater. The effects of cyfluthrin on PGS6046 metabolism varied based on the culture medium, whereas the cyanoalanine levels increased under both culture conditions. Culture time significantly affected the metabolism of amino acids and carbohydrates in PGS6046. The present study revealed the metabolic characteristics of PGS6046 under different culture conditions and will further facilitate the exploration of the fundamental questions regarding PGS6046 and its potential applications in environmental bioremediation.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Almakkawy HK, Madbouly MD (1999) Persistence and accumulation of some organic insecticides in Nile water and fish. Resour Conserv Recycl 27(1–2):105–115

    Article  Google Scholar 

  • Antwi FB, Reddy GV (2015) Toxicological effects of pyrethroids on non-target aquatic insects. Environ Toxicol Pharmacol 40(3):915–923

    Article  CAS  Google Scholar 

  • Bertini I, Hu X, Luchinat C (2014) Global metabolomics characterization of bacteria: pre-analytical treatments and profiling. Metabolomics 10(2):241–249

    Article  CAS  Google Scholar 

  • Brander SM, Gabler MK, Fowler NL, Connon RE, Schlenk D (2016) Pyrethroid pesticides as endocrine disruptors: molecular mechanisms in vertebrates with a focus on fishes. Environ Sci Technol 50(17):8977–8992

    Article  CAS  Google Scholar 

  • Bringaud F, Biran M, Millerioux Y, Wargnies M, Allmann S, Mazet M (2015) Combining reverse genetics and nuclear magnetic resonance-based metabolomics unravels trypanosome-specific metabolic pathways. Mol Microbiol 96(5):917–926

    Article  CAS  Google Scholar 

  • Ccanccapa-Cartagena A, Masiá A, Picó Y (2017) Simultaneous determination of pyrethroids and pyrethrins by dispersive liquid-liquid microextraction and liquid chromatography triple quadrupole mass spectrometry in environmental samples. Anal Bioanal Chem 409(20):4787–4799

    Article  CAS  Google Scholar 

  • Chen SH, Dong YH, Chang CQ, Deng YY, Zhang XF, Zhong GH, Song HW, Hu MY, Zhang LH (2013) Characterization of a novel cyfluthrin-degrading bacterial strain Brevibacterium aureum and its biochemical degradation pathway. Bioresour Technol 132(3):16–23

    Article  CAS  Google Scholar 

  • Clarke JD, Alexander DC, Ward DP, Ryals JA, Mitchell MW, Wulff JE, Guo LN (2013) Assessment of genetically modified soybean in relation to natural variation in the soybean seed metabolome. Sci Rep-UK 3(3082):3082

    Article  Google Scholar 

  • Demoute JP (1989) A brief review of the environmental fate and metabolism of pyrethroids. Pest Manag Sci 27(4):375–385

    Article  CAS  Google Scholar 

  • Den BG, Van EK, Groen AK, Venema K, Reijngoud DJ, Bakker BM (2013) The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res 54(9):2325–2340

    Article  Google Scholar 

  • Dubey SK, Holmes DS (1995) Biological cyanide destruction mediated by microorganisms. World J Microbiol Biotechnol 11(3):257–265

    Article  CAS  Google Scholar 

  • Ebrahimi P, Larsen FH, Jensen HM, Vogensen FK, Engelsen SB (2016) Real-time metabolomic analysis of lactic acid bacteria as monitored by in vitro NMR and chemometrics. Metabolomics 12(4):1–17

    Article  CAS  Google Scholar 

  • Escribano R, González-Arenzana L, Garijo P, Berlanas C, López-Alfaro I, López R, Gutiérrez AR, Santamaría P (2017) Screening of enzymatic activities within different enological non-Saccharomyces yeasts. J Food Sci Technol 54(6):1555–1564

    Article  CAS  Google Scholar 

  • Evans AM, DeHaven CD, Barrett T, Mitchell M, Milgram E (2009) Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small-molecule complement of biological systems. Anal Chem 81(16):6656–6667

    Article  CAS  Google Scholar 

  • Fuentes S, Méndez V, Aguila P, Seeger M (2014) Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications. Appl Microbiol Biotechnol 98(11):4781–4794

    Article  CAS  Google Scholar 

  • Giri S, Sharma GD (2002) Fenvalerate-induced chromosome aberrations and sister chromatid exchanges in the bone marrow cells of mice in vivo. Mutat Res 520(1–2):125–132

    Article  CAS  Google Scholar 

  • Hu GP, Zhao Y, Song FQ, Liu B, Vasseur L, Douglas C, You MS (2014) Isolation, identification and cyfluthrin-degrading potential of a novel Lysinibacillus sphaericus strain, FLQ-11-1. Res Microbiol 165(2):110–118

    Article  CAS  Google Scholar 

  • Husain A, Sato D, Jeelani G, Mi-ichi F, Ali V, Suematsu M, Soga T, Nozaki T (2010) Metabolome analysis revealed increase in S-methylcysteine and phosphatidylisopropanolamine synthesis upon L-cysteine deprivation in the anaerobic protozoan parasite Entamoeba histolytica. J Biol Chem 285(50):39160–39170

    Article  CAS  Google Scholar 

  • Ila HB, Topaktas M, Rencuzogullari E, Kayraldiz A, Donbak L, Daglioglu YK (2008) Genotoxic potential of cyfluthrin. Mutat Res 656(1–2):49–54

    Article  CAS  Google Scholar 

  • Keum YS, Seo JS, Li QX, Kim JH (2008) Comparative metabolomic analysis of Sinorhizobium sp. C4 during the degradation of phenanthrene. Appl Microbiol Biotechnol 80(5):863–872

    Article  CAS  Google Scholar 

  • Laskowski DA (2002) Physical and chemical properties of pyrethroids. Rev Environ Contam Toxicol 174:49–170

    Article  CAS  Google Scholar 

  • Miao JY, Wang DZ, Yan J, Wang Y, Teng MM, Zhou ZQ, Zhu WT (2017) Comparison of subacute effects of two types of pyrethroid insecticides using metabolomics methods. Pestic Biochem Physiol 143:161–167

    Article  CAS  Google Scholar 

  • Mokarizadeh A, Faryabi MR, Rezvanfar MA, Abdollahi M (2015) A comprehensive review of pesticides and the immune dysregulation: mechanisms, evidence and consequences. Toxicol Mech Methods 25(4):258–278

    Article  CAS  Google Scholar 

  • Ohta T, Masutomi N, Tsutsui N, Sakairi T, Mitchell M, Milburn MV, Ryals JA, Beebe KD, Guo LN (2009) Untargeted metabolomic profiling as an evaluative tool of fenofibrate-induced toxicology in Fischer 344 male rats. Toxicol Pathol 37(4):521–535

    Article  CAS  Google Scholar 

  • Qi Q, Steinbüchel A, Rehm BH (1998) Metabolic routing towards polyhydroxyalkanoic acid synthesis in recombinant Escherichia coli (fadR): inhibition of fatty acid β-oxidation by acrylic acid. FEMS Microbiol Lett 167(1):89–94

    CAS  PubMed  Google Scholar 

  • Ratledge C (2004) Fatty acid biosynthesis in microorganisms being used for single cell oil production. Biochimie 86(11):807–815

    Article  CAS  Google Scholar 

  • Rodríguez JL, Ares I, Castellano V, Martínez M, Martínez-Larrañaga MR, Anadón A, Martinez MA (2016) Effects of exposure to pyrethroid cyfluthrin on serotonin and dopamine levels in brain regions of male rats. Environ Res 146:388–394

    Article  Google Scholar 

  • Saikia N, Das SK, Patel BK, Niwas R, Singh A, Gopal M (2005) Biodegradation of beta-cyfluthrin by Pseudomonas stutzeri strain S1. Biodegradation 16(6):581–589

    Article  CAS  Google Scholar 

  • Sasaki D, Sasaki K, Tsuge Y, Morita M, Kondo A (2014) Comparison of metabolomic profiles of microbial communities between stable and deteriorated methanogenic processes. Bioresour Technol 172:83–90

    Article  CAS  Google Scholar 

  • Seo JS, Keum YS, Li QX (2013) Metabolomic and proteomic insights into carbaryl catabolism by Burkholderia sp. C3 and degradation of ten N-methylcarbamates. Biodegradation 24(6):795–811

    Article  CAS  Google Scholar 

  • Sun AL, Liu J, Shi XZ, Li DX, Chen J, Tang DJ (2014) Marine bacterium strain screening and pyrethroid insecticide-degrading efficiency analysis. Chin J Oceanol Limnol 32(5):1029–1035

    Article  CAS  Google Scholar 

  • Szewczyk R, Soboń A, Dlugoński J (2015) Mechanism study of alachlor biodegradation by Paecilomyces marquandii with proteomic and metabolomic methods. J Hazard Mater 291:52–64

    Article  CAS  Google Scholar 

  • Thomas S, Senthilkumar GP, Sivaraman K, Bobby Z, Paneerselvam S, Harichandrakumar KT (2015) Effect of s-methyl-L-cysteine on oxidative stress, inflammation and insulin resistance in male Wistar rats fed with high fructose diet. Iran J Med Sci 40(1):45–50

    PubMed  PubMed Central  Google Scholar 

  • Yoshikawa K, Kyoko A, Miyuki N (2000) Beta-cyanoalanine production by marine bacteria on cyanide-free medium and its specific inhibitory activity toward cyanobacteria. Appl Environ Microbiol 66(2):718–722

    Article  CAS  Google Scholar 

  • Zuo Z, Gong T, Che Y, Liu R, Xu P, Jiang H, Qiao CL, Song CJ, Yang C (2015) Engineering Pseudomonas putida KT2440 for simultaneous degradation of organophosphates and pyrethroids and its application in bioremediation of soil. Biodegradation 26(3):223–233

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Zhejiang Provincial Natural Science Foundation of China (LR16C190001), the National Natural Science Foundation of China (No. 31772856), the Technology Innovation Team of Ningbo city (2015C110018), and the K.C. Wong Magna Fund in Ningbo University.

Author information

Author notes

  1. Tengzhou Wang and Chaoyang Hu contributed equally to this work.

Authors and Affiliations

  1. School of Marine Sciences, Ningbo University, 818 Fenghua Road, 315211, Ningbo, People’s Republic of China

    Tengzhou Wang, Chaoyang Hu, Rongrong Zhang, Aili Sun, Dexiang Li & Xizhi Shi

Authors
  1. Tengzhou Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chaoyang Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rongrong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aili Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dexiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xizhi Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xizhi Shi.

Ethics declarations

Ethical approval

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

Conflict of interest

Tengzhou Wang declares that he has no conflict of interest. Chaoyang Hu declares that he has no conflict of interest. Rongrong Zhang declares that she has no conflict of interest. Aili Sun declares that she has no conflict of interest. Dexiang Li declares that he has no conflict of interest. Xizhi Shi declares that he has no conflict of interest.

Electronic supplementary material

ESM 1

(PDF 876 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, T., Hu, C., Zhang, R. et al. Mechanism study of cyfluthrin biodegradation by Photobacterium ganghwense with comparative metabolomics. Appl Microbiol Biotechnol 103, 473–488 (2019). https://doi.org/10.1007/s00253-018-9458-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-018-9458-7

Keywords

Search

Navigation