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.
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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
Benowitz NJ (1992) Cigarette smoking and nicotine addiction. Med Clin N Am 76:415–437
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
Brenner K, You L, Arnold FH (2008) Engineering microbial consortia: a new frontier in synthetic biology. Trends Biotechnol 26:483–489
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
Brunneman KD, Prokopczyk B, Djordjevic MV, Hoffman D (1996) Formation and analysis of tobacco specific N-nitrosamines. Crit Rev Toxicol 26:121–137
Campain JA (2004) Nicotine: potentially a multifunctional carcinogen. Toxicol Sci 79:1–3
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
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
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
Davies H, Bignell GR, Cox C, Stephens P, Edkins S (2002) Mutation of the BRAF gene in human cancer. Nature 417:949–954
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
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
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
Edenborn SL, Sexstone AJ (2007) DGGE fingerprinting of culturable soil bacterial communities complements culture-independent analyses. Soil Biol Biochem 39:1570–1579
Fetzner S (1998) Bacterial degradation of pyridine, indole, quinoline and their derivatives under different redox conditions. Appl Microbiol Biot 49:237–250
Freudenberg W, Koenig K, Andreesen JR (1988) Nicotine dehydrogenase from Arthrobacter oxidans: a molybdenum-containing hydroxylase. FEMS Microbiol Lett 52:13–18
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
Gies G (1995) Composting residential and commercial streams. Biocycle 36:78–79
Gravely LE, Geiss VL, Newton RP (1977) Process for maximizing the growth and nicotine degrading activity of microorganisms. United States Patent, No, 4011141
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
Haug RT (1993) The practical handbook of compost engineering. Lewis Publishers, Boca Raton, USA
Heisheman SC, Taylor RC, Henningfield JE (1994) Nicotine and smoking: a review of effects on human performance. Exp Clin Pharmcol 2:345–395
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
Hylin JW (1958) Microbial degradation of nicotine. I. morphology and physiology of Achromobacter nicotinophagum n. sp. J Bacteriol 76:36–40
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
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
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
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
Liu HY (2004) Improvement of the determination method for organic matter content of organic and inorganic fertilizer material. Fine Chem Intermed 34:70–71
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
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
Margesin R, Schinner F (2001) Biodegradation and bioremediation of hydrocarbons in extreme environments. Appl Microbiol Biot 56:650–663
Meher KK, Panchwagh AM, Rangrass S, Gollakota KG (1995) Biomethanation of tobacco waste. Environ Pollut 90:199–202
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
Novotny TE, Zhao F (1999) Consumption and production waste: another externality of tobacco use. Tob Control 8:75–80
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
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
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
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
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
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
Wada E, Yamasaki K (1953) Mechanism of microbial degradation of nicotine. Science 117:152–153
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
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
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
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
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
Yildiz D (2004) Nicotine, its metabolism and an overview of its biological effects. Toxicon 43:619–632
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
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.
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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
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DOI: https://doi.org/10.1007/s00253-012-4433-1