Skip to main content

Advertisement

Log in

Bioremediation of the tobacco waste-contaminated soil by Pseudomonas sp. HF-1: nicotine degradation and microbial community analysis

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

Abstract

The highly effective nicotine-degrading bacterium Pseudomonas sp. HF-1 was augmented into the tobacco waste-contaminated soil to degrade nicotine and evaluate the effect of the bioremediation. Comparing with non-adding (NA) systems, the treatments with addition of strain HF-1 (TA) exhibited considerably stronger pollution disposal abilities and higher stability of pH value and moisture content, especially in groups containing a large quantity of tobacco waste. The denaturing gradient gel electrophoresis (DGGE) profiles showed that the Shannon–Wiener index decreased with increasing wastes in the NA treatments, while a gradual increase was found in the TA groups. A comparison of sequences from DGGE bands demonstrated that there were differences in the dominant microbial species between the two treatments, suggesting that strain HF-1 could persist in the soil and enhance the efficiency of tobacco waste disposal. The results of real-time fluorescence quantitative PCR (RT-qPCR) also indicated that strain HF-1 existed in the TA systems and grew with relative high quantities. In conclusion, the nicotine-degrading strain HF-1 played a leading role in the bioremediation of the tobacco waste-contaminated soil and influenced the dynamics and structure of the microbial community.

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

Access this article

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

Similar content being viewed by others

References

  • Almeida A, Pozio E, Caccio SM (2010) Genotyping of Giardia duodenalis cysts by new real-time PCR assays for detection of mixed infections in human samples. Appl Environ Microb 6976:1895–1901

    Article  Google Scholar 

  • Benowitz NJ (1992) Cigarette smoking and nicotine addiction. Med Clin N Am 76:415–437

    CAS  Google Scholar 

  • Beškoski VP, Gojgić-Cvijović G, Milić J, Ilić M, Miletić S, Solević T, Vrvić MM (2011) Ex situ bioremediation of a soil contaminated by mazut (heavy residual fuel oil)—a field experiment. Chemosphere 83:34–40

    Article  Google Scholar 

  • Brenner K, You L, Arnold FH (2008) Engineering microbial consortia: a new frontier in synthetic biology. Trends Biotechnol 26:483–489

    Article  CAS  Google Scholar 

  • Briški F, Horgas N, Vuković M, Gomzi Z (2003) Aerobic composting of tobacco industry solid waste-simulation of the process. Clean Techn Environ Policy 5:295–301

    Article  Google Scholar 

  • Brunneman KD, Prokopczyk B, Djordjevic MV, Hoffman D (1996) Formation and analysis of tobacco specific N-nitrosamines. Crit Rev Toxicol 26:121–137

    Article  Google Scholar 

  • Campain JA (2004) Nicotine: potentially a multifunctional carcinogen. Toxicol Sci 79:1–3

    Article  CAS  Google Scholar 

  • Civilini M, Domenis C, Sebastianutto N, Bertoldi M (1997) Nicotine decontamination of tobacco agro-industrial waste and its degradation by microorganisms. Waste Manage Res 15:349–358

    CAS  Google Scholar 

  • Couling NR, Towell MG, Semple KT (2010) Biodegradation of PAHs in soil: influence of chemical structure, concentration and multiple ammendment. Environ Pollut 158:3411–3420

    Article  CAS  Google Scholar 

  • Cunliffe M, Kawasaki A, Fellows E, Kertesz MA (2006) Effect of inoculums pretreatment on survival, activity and catabolic gene expression of Sphingobium yanoikuyae B1 in an aged polycyclic aromatic hydrocarbon-contaminated soil. FEMS Microbiol Ecol 58:364–372

    Article  CAS  Google Scholar 

  • Davies H, Bignell GR, Cox C, Stephens P, Edkins S (2002) Mutation of the BRAF gene in human cancer. Nature 417:949–954

    Article  CAS  Google Scholar 

  • De Neve S, Hofman G (2000) Influence of soil compaction on carbon and nitrogen mineralization of soil organic matter and crop residues. Biol Fert Soils 30:544–549

    Article  Google Scholar 

  • Devinny JS, Chang SH (2000) Bioaugmentation for soil bioremediation. In: Wise DL, Trantolo DJ, Cichon EJ, Inyang HI, Stottmeister U (eds) Bioremediation of contaminated Soils, 2nd edn. Marcel Dekker, New York, pp 465–488

    Google Scholar 

  • Du H, Jiao N, Hu Y, Zeng Y (2006) Real-time PCR for quantification of aerobic anoxygenic phototrophic bacteria based on pufM gene in marine environment. J Exp Mar Biol Ecol 329:113–121

    Article  CAS  Google Scholar 

  • Edenborn SL, Sexstone AJ (2007) DGGE fingerprinting of culturable soil bacterial communities complements culture-independent analyses. Soil Biol Biochem 39:1570–1579

    Article  CAS  Google Scholar 

  • Fetzner S (1998) Bacterial degradation of pyridine, indole, quinoline and their derivatives under different redox conditions. Appl Microbiol Biot 49:237–250

    Article  CAS  Google Scholar 

  • Freudenberg W, Koenig K, Andreesen JR (1988) Nicotine dehydrogenase from Arthrobacter oxidans: a molybdenum-containing hydroxylase. FEMS Microbiol Lett 52:13–18

    Article  CAS  Google Scholar 

  • Garneau M, Schnetzer A, Countway PD, Jones AC, Seubert EL, Caron DA (2011) Examination of the seasonal dynamics of the toxic dinoflagellate Alexandrium catenella at Redondo Beach, California, by quantitative PCR. Appl Environ Microb 77:7669–7680

    Article  CAS  Google Scholar 

  • Gies G (1995) Composting residential and commercial streams. Biocycle 36:78–79

    Google Scholar 

  • Gravely LE, Geiss VL, Newton RP (1977) Process for maximizing the growth and nicotine degrading activity of microorganisms. United States Patent, No, 4011141

    Google Scholar 

  • Gravely LE, Geiss VL, Gregory CF (1985) Process for reduction of nitrate and nicotine content of tobacco by microbial treatment. United States Patent, No, 4557280

    Google Scholar 

  • Haug RT (1993) The practical handbook of compost engineering. Lewis Publishers, Boca Raton, USA

    Google Scholar 

  • Heisheman SC, Taylor RC, Henningfield JE (1994) Nicotine and smoking: a review of effects on human performance. Exp Clin Pharmcol 2:345–395

    Google Scholar 

  • Heuer H, Krsek M, Baker P (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microb 63:3233–3241

    CAS  Google Scholar 

  • Hylin JW (1958) Microbial degradation of nicotine. I. morphology and physiology of Achromobacter nicotinophagum n. sp. J Bacteriol 76:36–40

    CAS  Google Scholar 

  • Kayhanian M, Tchobanoglous G (1993) Innovative two-stage process for the recovery of energy and compost from the organic fraction of municipal solid waste (MSW). Water Sci Technol 27:133–143

    CAS  Google Scholar 

  • König S, Wubet T, Dormann CF, Hempel S, Renker C, Buscot F (2010) TaqMan Real-Time PCR assays to assess Arbuscular mycorrhizal responses to field manipulation of grassland biodiversity: effects of soil characteristics, plant species richness, and functional traits. Appl Environ Microb 76:3765–3775

    Article  Google Scholar 

  • Langer U, Bӧhme L, Bӧhme F (2004) Classification of soil microorganisms based on growth properties: a critical view of some commonly used terms. J Plant Nutr Soil Sci 167:267–269

    Article  CAS  Google Scholar 

  • Li H, Li X, Duan Y, Zhang KQ, Yang JK (2010) Biotransformation of nicotine by microorganism: the case of Pseudomonas sp. Appl Microbiol Biot 86:11–17

    Article  CAS  Google Scholar 

  • Liu HY (2004) Improvement of the determination method for organic matter content of organic and inorganic fertilizer material. Fine Chem Intermed 34:70–71

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the \( {2^{{ - \varDelta \varDelta {{\mathrm{C}}_{\mathrm{T}}}}}} \) method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Madejón E, López R, Murillo JM, Cabrera F (2001) Agricultural use of three (sugar-beet) vinasse composts: effect on crops and chemical properties of a Cambisol soil in the Guadalquivir river valley (SW Spain). Agr Ecosyst Environ 84:53–65

    Article  Google Scholar 

  • Margesin R, Schinner F (2001) Biodegradation and bioremediation of hydrocarbons in extreme environments. Appl Microbiol Biot 56:650–663

    Article  CAS  Google Scholar 

  • Meher KK, Panchwagh AM, Rangrass S, Gollakota KG (1995) Biomethanation of tobacco waste. Environ Pollut 90:199–202

    Google Scholar 

  • Newton RP, Geiss VL, Jewell JN, Gravely LE (1977) Process for reduction of nicotine content of tobacco by microbial treatment. United States Patent, No, 4037609

    Google Scholar 

  • Novotny TE, Zhao F (1999) Consumption and production waste: another externality of tobacco use. Tob Control 8:75–80

    Article  CAS  Google Scholar 

  • Peng JJ, Cai C, Qiao M, Li H, Zhu YG (2010) Dynamic changes in functional gene copy numbers and microbial communities during degradation of pyrene in soils. Environ Pollut 158:2872–2879

    Article  CAS  Google Scholar 

  • Qiu J, Ma Y, Chen L, Wu L, Wen Y, Liu W (2011) A sirA-like gene, sirA2, is essential for 3-succinoyl-pyridine metabolism in the newly isolated nicotine-degrading Pseudomonas sp. HZN6 strain. Appl Microbiol Biot 92:1023–1032

    Article  CAS  Google Scholar 

  • Riley IT, Wiebkin S, Hartley D, McKay AC (2010) Quantification of roots and seeds in soil with real-time PCR. Plant Soil 331:151–163

    Article  CAS  Google Scholar 

  • Ruan AD, Min H, Peng XH, Huang Z (2005) Isolation and characterization of Pseudomonas sp. strain HF-1, capable of degrading nicotine. Res Microbiol 156:700–706

    Article  CAS  Google Scholar 

  • Saito A, Minamisawa K (2006) Evaluation of the nitrogen fixing ability of endophytic Clostridia based on acetylene reduction and reverse transcription-PCR targeting the nifH transcript and ribosomal RNA. Microbes Environ 21:23–35

    Article  Google Scholar 

  • Schenk S, Hoelz A, Krass B, Decker K (1998) Gene structures and properties of enzymes of the plasmid-encoded nicotine catabolism of Arthrobacter nicotinovorans. J Mol Biol 284:1323–1329

    Article  CAS  Google Scholar 

  • Wada E, Yamasaki K (1953) Mechanism of microbial degradation of nicotine. Science 117:152–153

    Article  CAS  Google Scholar 

  • Wang J, Lu D, Liang Y, Zhao H, Luo M, Ling X, Ouyang P (2012) Isolation of mono-caffeoylquinic acids from tobacco waste using continuous resin-based pre-separation and preparative HPLC. J Sep Sci 35:1379–1387

    Article  CAS  Google Scholar 

  • Wang MZ, Yang GQ, Min H, Lv ZM (2009a) A novel nicotine catabolic plasmid pMH1 in Pseudomonas sp. strain HF-1. Can J Microbiol 55:228–233

    Article  CAS  Google Scholar 

  • Wang MZ, Yang GQ, Min H, Lv ZM, Jia XY (2009b) Bioaugmentation with the nicotine-degrading bacterium Pseudomonas sp. HF-1 in a sequencing batch reactor treating tobacco wastewater: degradation study and analysis of its mechanisms. Water Res 43:4187–4196

    Article  CAS  Google Scholar 

  • Wang SN, Liu Z, Tang HZ, Meng J, Xu P (2007) Characterization of environmentally friendly nicotine degradation by Pseudomonas putida biotype A strain S16. Microbiology 153:1556–1565

    Article  CAS  Google Scholar 

  • Yang CH, Crowley DE (2000) Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl Environ Microb 66:345–351

    Article  CAS  Google Scholar 

  • Yildiz D (2004) Nicotine, its metabolism and an overview of its biological effects. Toxicon 43:619–632

    Article  CAS  Google Scholar 

  • Ying YL, Lv ZM, Min H, Cheng J (2008) Dynamic changes of microbial community diversity in a photohydrogen producing reactor monitored by PCR-DGGE. J Environ Sci-China 20:1118–1125

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (no. 31170115, 31100032) and the Major Science and Technology Program for Water Pollution Control and Treatment (no. 2012ZX07101-012). We are sincerely grateful to Mr. Philip Alexzander Lorhrmann for greatly improving the use of English.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhenmei Lu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 544 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, X., Tang, L., Yao, Y. et al. Bioremediation of the tobacco waste-contaminated soil by Pseudomonas sp. HF-1: nicotine degradation and microbial community analysis. Appl Microbiol Biotechnol 97, 6077–6088 (2013). https://doi.org/10.1007/s00253-012-4433-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-012-4433-1

Keywords

Navigation