Toluene degradation via a unique metabolic route in indigenous bacterial species

Muccee, Fatima; Ejaz, Samina; Riaz, Naheed

doi:10.1007/s00203-019-01705-0

Original Paper
Published: 22 July 2019

Toluene degradation via a unique metabolic route in indigenous bacterial species

Archives of Microbiology volume 201, pages 1369–1383 (2019)Cite this article

746 Accesses
12 Citations
Metrics details

Abstract

Tanneries are the primary source of toluene pollution in the environment and toluene due to its hazardous effects has been categorized as persistent organic pollutant. Present study was initiated to trace out metabolic fingerprints of three toluene-degrading bacteria isolated from tannery effluents of Southern Punjab. Using selective enrichment and serial dilution methods followed by biochemical, molecular and antibiotic resistance analysis, isolated bacteria were subjected to metabolomics analysis. GC–MS/LC–MS analysis of bacterial metabolites helped to identify toluene transformation products and underlying pathways. Three toluene-metabolizing bacteria identified as Bacillus paralicheniformis strain KJ-16 (IUBT4 and IUBT24) and Brevibacillus agri strain NBRC 15538 (IUBT19) were found tolerant to toluene and capable of degrading toluene. Toluene-degrading potential of these isolates was detected to be IUBT4 (10.35 ± 0.084 mg/h), IUBT19 (14.07 ± 3.14 mg/h) and IUBT24 (11.1 ± 0.282 mg/h). Results of GC–MS analysis revealed that biotransformation of toluene is accomplished not only through known metabolic routes such as toluene 3-monooxygenase (T3MO), toluene 2-monooxygenase (T2MO), toluene 4-monooxygenase (T4MO), toluene methyl monooxygenase (TOL), toluene dioxygenase (Tod), meta- and ortho-ring fission pathways. But additionally, confirmed existence of a unique metabolic pathway that involved conversion of toluene into intermediates such as cyclohexene, cyclohexane, cyclohexanone and cyclohexanol. LC–MS analysis indicated the presence of fatty acid amides, stigmine, emmotin A and 2, 2-dinitropropanol in supernatants of bacterial cultures. As the isolated bacteria transformed toluene into relatively less toxic molecules and thus can be preferably exploited for the eco-friendly remediation of toluene.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Data access statement

These sequence data have been submitted to the GenBank database under accession numbers IUBT1 (MH014864), IUBT4 (MH014871), IUBT19 (MH014861) and IUBT24 (MG190870). Details of data submission can be found at: https://www.ncbi.nlm.nih.gov.

Abbreviations

VOC:: Volatile organic compound
EPA:: Environmental Protection Agency
PEL:: Permissible exposure limit
Tod:: Dioxygenase-mediated pathway
TOM:: Toluene-2-monooxygenase pathway
Tbu:: Toluene-3-monooxygenase pathway
TMO:: Toluene-4-monooxygenase pathway
TOL:: Toluene methyl monooxygenase pathway
GC–MS:: Gas chromatography–mass spectrometry
LC–MS:: Liquid chromatography–mass spectrometry
BLAST:: Basic local alignment search tool
AChEIs:: Acetylcholinesterase inhibitor

References

Afrouzossadat HA, Emtiazi G, Ghasemi SM, Roghanian R (2013) Isolation and characterization of a novel toluene-degrading bacterium exhibiting potential application in bioremediation. Jundishapur J Microb. https://doi.org/10.5812/jjm.5142
Article Google Scholar
Ali J, Ali N, Wang L, Waseem H, Pan G (2019) Revisiting the mechanistic pathways for bacterial mediated synthesis of noble metal nanoparticles. J. Microbiol Methods 159:18–25. https://doi.org/10.1016/j.mimet.2019.02.010
CAS Article PubMed Google Scholar
Anantha PS, Deventhiran M, Saravanan P, Anand D, Rajarajan S (2016) A comparative GC–MS analysis of bacterial secondary metabolites of Pseudomonas species. J Pharm Innov 5:84. https://www.thepharmajournal.com/archives/2016/vol5issue4/PartB/5-3-26.pdf
Anderson RC, Rasmussen MA, Allison MJ (1996) Enrichment and isolation of a nitropropanol-metabolizing bacterium from the rumen. Appl Environ Microbiol 62:3885–3886. https://www.ncbi.nlm.nih.gov/pubmed/8837447
Anderson RC, Rasmussen MA, Jensen NS, Allison MJ (2000) Denitrobacterium detoxificans gen. nov., sp. nov., a ruminal bacterium that respires on nitrocompounds. Int J Syst Evol Microbiol 50:633–638. https://doi.org/10.1099/00207713-50-2-633
CAS Article PubMed Google Scholar
Appelbaum PC, Jacobs MR, Palko WM, Frauenhoffer EE, Duffett A (1986) Accuracy and reproducibility of the IDS rapID STR system for species identification of streptococci. J Clin Microbiol 23:843–846. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC268734
Assinder SJ, Williams PA (1990) The TOL plasmids: determinants of the catabolism of toluene and the xylenes. Adv Microb Physiol 31:1–69. https://www.ncbi.nlm.nih.gov/pubmed/2264522
Atashgahi S, Sanchez-Andrea I, Heipieper HJ, Van der Meer JR, Stams AJM, Smidt H (2018) Prospects for harnessing biocide resistance for bioremediation and detoxification. Science 360:743–746. https://doi.org/10.1126/science.aar3778
CAS Article PubMed Google Scholar
Balster RL, Cruz SL, Howard MO, Dell CA, Cottler LB (2009) Classification of abused inhalants. Addiction 104:878–882
Article Google Scholar
Bauer AW, Kirby WM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493. https://www.ncbi.nlm.nih.gov/pubmed/5325707
CAS Article Google Scholar
Bose U, Hewavitharana AK, Ng YK, Shaw PN, Fuerst JA, Hodson MP (2015) LC–MS-based metabolomics study of marine bacterial secondary metabolite and antibiotic production in Salinispora arenicola. Mar Drugs 13:249–266. https://doi.org/10.3390/md13010249
CAS Article PubMed PubMed Central Google Scholar
Chakrabarty AM (1996) Microbial degradation of toxic environmental pollutants: ecological and evolutionary considerations. Int Biodeterior Biodegrad 3:252. https://doi.org/10.1016/0964-8305(95)90033-0
Article Google Scholar
Cheng Q, Thomas SM, Kostichka K, Valentine JR, Nagarajan V (2000) Genetic analysis of a gene cluster for cyclohexanol oxidation in Acinetobacter sp. strain SE19 by in vitro transposition. J Bacteriol 182:4744–4751
CAS Article Google Scholar
Crawford RL (1976) Pathways of 4-hydroxybenzoate degradation among species of Bacillus. J Bacteriol 127:204–210. https://jb.asm.org/content/127/1/204
Ding N, Jiang Y, Liu J, Li Q, Wang X, Mu Y, Han L, Huang X (2016) Structure determination of two new sesquiterpenoids from Streptomyces sanglieri. Magn Reson Chem 54:930–932. https://doi.org/10.1002/mrc.4473
CAS Article PubMed Google Scholar
Dobslaw D, Engesser KH (2015) Degradation of toluene by ortho cleavage enzymes in Burkholderia fungorum FLU100. Microb Biotechnol 8:143–154. https://doi.org/10.1111/1751-7915.12147
CAS Article PubMed Google Scholar
Duldhardt I, Gaebel J, Chrzanowski L, Nijenhuis I, Härtig C, Schauer F, Heipieper HJ (2010) Adaptation of anaerobically grown Thauera aromatica, Geobacter sulfurreducens and Desulfococcus multivorans to organic solvents on the level of membrane fatty acid composition. Microb Biotechnol 3:201–209. https://doi.org/10.1111/j.1751-7915.2009.00124.x
CAS Article PubMed PubMed Central Google Scholar
Fernie AR, Trethewey RN, Krotzky AJ, Willmitzer L (2004) Metabolite profiling: from diagnostics to systems biology. Nat Rev Mol Cell Biol 5:763. https://www.nature.com/articles/nrm1451
CAS Article Google Scholar
Field JA, Sierra AR (2008) Microbial transformation of chlorinated benzoates. Rev Environ Sci Bio Technol 7:191–210. https://link.springer.com/article/10.1007/s11157-008-9133-z
CAS Article Google Scholar
Gopinath M, Dhanasekar R (2012) Microbial degradation of toluene. Afr J Biotechnol 11:16210–16219
CAS Article Google Scholar
Harwood CS, Parales RE (1996) The β-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol 50:553–590. https://doi.org/10.1146/annurev.micro.50.1.553
CAS Article PubMed Google Scholar
Guo X, Peng Z, Huang D, Xu P, Zeng G, Zhou S, Gong X, Cheng M, Deng R, Yi H (2018) Biotransformation of cadmium-sulfamethazine combined pollutant in aqueous environments: Phanerochaete chrysosporium bring cautious optimism. Chem Eng J 347:74–83. https://doi.org/10.1016/j.cej.2018.04.089
CAS Article Google Scholar
Heydarnezhad F, Hoodaji M, Shahriarinour M, Tahmourespour A, Shariati S (2018) Optimizing toluene degradation by bacterial strain isolated from oil-polluted soils. Polish J Environ Stud 27. https://www.pjoes.com/abstracts/2018/Vol27/No02/20.html
Huang WH, Dong CD, Chen CW, Surampalli RY, Kao CM (2017) Application of sulfate reduction mechanisms for the simultaneous bioremediation of toluene and copper contaminated groundwater. Int Biodeterior Biodegrad 124:215–222. https://doi.org/10.1016/j.ibiod.2017.03.017
CAS Article Google Scholar
Hu C, Huang D, Zeng G, Cheng M, Gong X, Wang R, Xue W, Hu Z, Liu Y (2018) The combination of Fenton process and Phanerochaete chrysosporium for the removal of bisphenol A in river sediments: mechanism related to extracellular enzyme, organic acid and iron. Chem Eng J 338:432–439. https://doi.org/10.1016/j.cej.2018.01.068
CAS Article Google Scholar
Idle JR, Gonzalez FJ (2007) Metabolomics. Cell Metab 6:348–351. https://doi.org/10.1016/j.cmet.2007.10.005
CAS Article PubMed PubMed Central Google Scholar
Janben HJ, Steinbuchel A (2014) Fatty acid synthesis in Escherichia coli and its applications towards the production of fatty acid based biofuels. Biotechnol Biofuels 7:7. https://doi.org/10.1186/1754-6834-7-7
CAS Article Google Scholar
Jehmlich N, Kleinsteuber S, Vogt C, Benndorf D, Harms H, Schmidt F, Bergen VM, Seifert J (2010) Phylogenetic and proteomic analysis of an anaerobic toluene-degrading community. J Appl Microbiol 109:1937–1945. https://doi.org/10.1111/j.1365-2672.2010.04823.x
CAS Article PubMed Google Scholar
Johnson GR, Olsen RH (1997) Multiple pathways for toluene degradation in Burkholderia sp. strain JS150. Appl Environ Microbiol 63:4047–4052. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC168715
Kim JM, Jeon CO (2009) Isolation and characterization of a new benzene, toluene, and ethylbenzene degrading bacterium, Acinetobacter sp. B113. Curr Microbiol 58:70–75. https://doi.org/10.1007/s00284-008-9268-8
CAS Article PubMed Google Scholar
Koek MM, Muilwijk B, Van der Werf MJ, Hankemeier T (2006) Microbial metabolomics with gas chromatography/mass spectrometry. Anal Chem 8:1272–1281. https://doi.org/10.1021/ac051683
Article Google Scholar
Kongpol A, Pongtharangkul T, Kato J, Honda K, Ohtake H, Vangnai AS (2009) Characterization of an organic-solvent-tolerant Brevibacillus agri strain 13 able to stabilize solvent/water emulsion. FEMS Microbiol Lett 297:225–233. https://doi.org/10.1111/j.1574-6968.2009.01684.x
CAS Article PubMed Google Scholar
Kurokawa T, Suzuki K, Hayaoka T, Nakagawa T, Izawa T, Kobayashi M, Harada N (1993) Cyclophostin, acetylcholinesterase inhibitor from Streptomyces lavendulae. J Antibiot 46:1315–1318. https://doi.org/10.7164/antibiotics.46.1315
CAS Article PubMed Google Scholar
Lau PCK, Wang Y, Patel A, Labbé D, Bergeron H, Brousseau R, Konishi Y, Rawlings M (1997) A bacterial basic region leucine zipper histidine kinase regulating toluene degradation. Proc Natl Acad Sci 94:1453–1458. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC19812
CAS Article Google Scholar
Lee Y, Jeon CO (2019) Biodegradation of naphthalene, BTEX, and aliphatic hydrocarbons by Paraburkholderia aromaticivorans BN5 isolated from petroleum-contaminated soil. Sci Rep. https://www.nature.com/articles/s41598-018-36165-x
Lee, Kim H, Yu MJ, Ko CH, Jeon JK, Jae J, Park SH, Jung SC, Park YK (2016) Catalytic hydrodeoxygenation of bio-oil model compounds over Pt/HY catalyst. Sci Rep 6:28765. https://pdfs.semanticscholar.org/5c9b/beab6ab7245cede5f8df6aab5a8a8c72a1cc.pdf
Liebeke M, Dörries K, Meyer H, Lalk M (2012) Metabolome analysis of gram-positive bacteria such as Staphylococcus aureus by GC–MS and LC–MS. Functional genomics. Springer, pp 377–398. https://doi.org/10.1007/978-1-61779-424-7_28
Google Scholar
Liew SM, Tay ST, Wongratanacheewin S, Puthucheary SD (2012) Enzymatic profiling of clinical and environmental isolates of Burkholderia pseudomallei. Trop Biomed. https://www.ncbi.nlm.nih.gov/pubmed/22543616
Martinez LPM, Muller C, Nijenhuis I, Kappelmeyer U, Buffing M, McPherson K, Heipieper HJ (2010) High stability and fast recovery of expression of the TOL plasmid-carried toluene catabolism genes of Pseudomonas putida mt-2 under conditions of oxygen limitation and oscillation. Appl Environ Microbiol 76:6715–6723. https://doi.org/10.1128/AEM.01039-10
CAS Article Google Scholar
Megharaj M, Ramakrishnan B, Venkateswarlu K, Sethunathan N, Naidu R (2011) Bioremediation approaches for organic pollutants: a critical perspective. Environ Int 37:1362–1375. https://doi.org/10.1016/j.envint.2011.06.003
CAS Article PubMed Google Scholar
Meyer, CI, Martinez L, Marin CV, Böhnke S, Harms H, Müller JA, Heipieper HJ (2017) Isolation and characterization of Magnetospirillum sp. strain 15-1 as a representative anaerobic toluene-degrader from a constructed wetland model. PLoS One 12:1–16. https://www.ncbi.nlm.nih.gov/pubmed/28369150
Murao S, Hayashi H (1986) Physostigmine and N8-norphysostigmine, insecticidal compounds, from Streptomyces sp. Agric Biol Chem 50:523–524. https://doi.org/10.1080/00021369.1986.10867419
CAS Article Google Scholar
Nahar N (1994) Characterization of activated sludge bacteria capable of growth on toluene and other aromatic compounds. https://doras.dcu.ie/19130/1
Neumann R, Peter HH (1987) Insecticidal organophosphates: nature made them first. Experientia 43:1235–1237. https://link.springer.com/article/10.1007/BF01945541
CAS Article Google Scholar
Newman LM, Wackett LP (1995) Purification and characterization of toluene 2-monooxygenase from Burkholderia cepacia G4. Biochemistry 34:14066–14076. https://pubs.acs.org
CAS Article Google Scholar
Olsen Kukor JJ, Kaphammer B (1994) A novel toluene-3-monooxygenase pathway cloned from Pseudomonas pickettii PKO1. J Bacteriol 176:3749–3756. https://doi.org/10.1128/jb.176.12
CAS Article PubMed PubMed Central Google Scholar
Otoguro K, Kuno F, Omura S (1997) Arisugacins, selective acetylcholinesterase inhibitors of microbial origin. Pharmacol Ther 76:45–54. https://doi.org/10.1016/S0163-7258(97)00093-4
CAS Article PubMed Google Scholar
Oyetibo GO, Miyauchi K, Huang Y, Chien MF, Ilori MO, Amund OO, Endo G (2017) Biotechnological remedies for the estuarine environment polluted with heavy metals and persistent organic pollutants. Int. Biodeterior Biodegrad 119:614–625. https://doi.org/10.1016/j.ibiod.2016.10.005
CAS Article Google Scholar
Pandey S, Sree A, Sethi DP, Kumar CG, Kakollu S, Chowdhury L, Dash SS (2014) A marine sponge associated strain of Bacillus subtilis and other marine bacteria can produce anticholinesterase compounds. Microb Cell Fact 13:24. https://doi.org/10.1186/1475-2859-13-24
CAS Article PubMed PubMed Central Google Scholar
Parales RE, Harwood CS (1992) Characterization of the genes encoding beta-ketoadipate: succinyl-coenzyme A transferase in Pseudomonas putida. J Bacteriol 174:4657–4666. https://doi.org/10.1128/jb.174.14.4657-4666
CAS Article PubMed PubMed Central Google Scholar
Pepi M, Heipieper H J, Fischer J, Ruta M, Volterrani M, Focardi SE (2008) Membrane fatty acids adaptive profile in the simultaneous presence of arsenic and toluene in Bacillus sp. ORAs2 and Pseudomonas sp. ORAs5 strains. Extremophiles 12:343–349. https://link.springer.com/article/10.1007/s00792-008-0147-9
CAS Article Google Scholar
Perez S, Rosa M, Abalos RA, Gomez Montes de Oca JM, Cantero MD (2006) Biodegradation of crude oil by Pseudomonas aeruginosa AT18 strain. Tecnologia Quimica 26. https://www.redalyc.org/html/4455/445543749010
Pinu F, Villas BS (2017) Extracellular microbial metabolomics: the state of the art. Metabolites. 7:43. https://doi.org/10.3390/metabo7030043
CAS Article PubMed Central Google Scholar
Radulovic NS, Blagojevic PD, Skropeta D (2010) Average mass scan of the total ion chromatogram versus percentage chemical composition in multivariate statistical comparison of complex volatile mixtures. J Braz Chem Soc 21:2319–2326. https://doi.org/10.1590/S0103-50532010001200020
CAS Article Google Scholar
Rajamanickam R, Kaliyamoorthi K, Ramachandran N, Baskaran D, Krishnan J (2017) Batch biodegradation of toluene by mixed microbial consortia and its kinetics. Int Biodeterior Biodegrad 119:282–288. https://doi.org/10.1016/j.ibiod.2016.11.014
CAS Article Google Scholar
Rizwan M, Singh M, Mitra CK, Morve RK (2014) Ecofriendly application of nanomaterials: nanobioremediation. J Nanopart. https://doi.org/10.1155/2014/431787
Article Google Scholar
Santos IC, Chaumette A, Smuts J, Hildenbrand ZL, Schug KA (2019) Analysis of bacteria stress responses to contaminants derived from shale energy extraction. Environ Sci Process Impacts
Sapcariu SC, Kanashova T, Weindl D, Ghelfi J, Dittmar G, Hiller K (2014) Simultaneous extraction of proteins and metabolites from cells in culture. MethodsX 1:74–80. https://www.sciencedirect.com/science/article/pii/S2215016114200586
Article Google Scholar
Sayqal A, Xu Y, Trivedi DK, AlMasoud N, Ellis DI, Muhamadali H, Rattray NJW, Webb C, Goodacre R (2016) Metabolic analysis of the response of Pseudomonas putida DOT-T1E strains to toluene using Fourier transform infrared spectroscopy and gas chromatography mass spectrometry. Metabolomics 12:112. https://link.springer.com/article/10.1007/s11306-016-1054-1
Sayyed RZ, Patel PR (2011) Soil microorganisms and environmental health. Int J Biotechnol Biosci 1:41–66. https://www.researchgate.net/publication/277254300
Shinoda Y, Sakai Y, Uenishi H, Uchihashi Y, Hiraishi A, Yukawa H, Yurimoto H, Kato N (2004) Aerobic and anaerobic toluene degradation by a newly isolated denitrifying bacterium, Thauera sp. strain DNT-1. Appl Environ Microbiol 70:1385–1392. https://aem.asm.org/content/70/3/1385.short
CAS Article Google Scholar
Sievers F, Higgins DG (2014) Clustal Omega, accurate alignment of very large numbers of sequences. Multiple sequence alignment methods. Springer, Berlin, pp 105–116. https://link.springer.com/protocol/10.1007/978-1-62703-646-7_6
Google Scholar
Sinensky M (1974) Homeoviscous adaptation—a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc Natl Acad Sci 71:522–525. https://doi.org/10.1073/pnas.71.2.522
CAS Article PubMed Google Scholar
Song JM, Sung JHY (2002) Roles of the meta- and the ortho-cleavage pathways for the efficient utilization of aromatic hydrocarbons by Sphingomonas yanoikuyae B1. J Microbiol
Sun MW, Zhang XM, Bi HL, Li WJ, Lu CH (2017) Two new sesquiterpenoids produced by halophilic Nocardiopsis chromatogenes YIM 90109. Nat Prod Res 31:77–83. https://doi.org/10.1080/14786419.2016.1214831
CAS Article PubMed Google Scholar
Surendra SV, Mahalingam BL, Velan M (2017) Degradation of monoaromatics by Bacillus pumilus MVSV3. Braz Arch Biol Technol. https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1516-89132017000100408
Tao Y, Fishman A, Bentley WE, Wood TK (2004) Oxidation of benzene to phenol, catechol, and 1, 2, 3-trihydroxybenzene by toluene 4-monooxygenase of Pseudomonas mendocina KR1 and toluene 3-monooxygenase of Ralstonia pickettii PKO1. Appl Environ Microbiol 70:3814–3820. https://aem.asm.org/content/70/7/3814.short
CAS Article Google Scholar
Varshini DV, Sumathy VJH (2017) Isolation of toluene degrading bacteria from polluted environment. Eur J Pharm Med Res 4:341–346. https://www.ejpmr.com/admin/assets/article_issue/1504176511.pdf
Wang L, Shao Z (2006) Isolation and characterization of 4 benzene/toluene-degrading bacterial strains and detection of related degradation genes. Acta Microbiol Sin 46:753–757. https://www.ncbi.nlm.nih.gov/pubmed/17172023
Weber FJ, Isken S, De Bont JAM (1994) Cis/trans isomerization of fatty acids as a defence mechanism of Pseudomonas putida strains to toxic concentrations of toluene. Microbiology 140:2013–2017. https://edepot.wur.nl/210152#page=81
CAS Article Google Scholar
Whited GM, Gibson DT (1991a) Separation and partial characterization of the enzymes of the toluene-4-monooxygenase catabolic pathway in Pseudomonas mendocina KR1. J Bacteriol 173:3017–3020. https://jb.asm.org/content/173/9/3017.short
CAS Article Google Scholar
Whited GM, Gibson DT (1991b) Toluene-4-monooxygenase, a three-component enzyme system that catalyzes the oxidation of toluene to p-cresol in Pseudomonas mendocina KR1. J Bacteriol 173:3010–3016. https://jb.asm.org/content/173/9/3010.short
CAS Article Google Scholar
Worsey MJ, Williams, PA (1975) Metabolism of toluene and xylenes by Pseudomonas (putida (arvilla) mt-2: evidence for a new function of the TOL plasmid. J Bacteriol 124:7–13
Yavas A, Icgen B (2018) Aerobic bacterial degraders with their relative pathways for efficient removal of individual BTEX compounds. Clean Soil Air Water. https://doi.org/10.1002/clen.201800068
Article Google Scholar
Yin M, Li G, Jiang Y, Han L, Huang X, Lu T, Jiang C (2017) The complete genome sequence of Streptomyces albolongus YIM 101047, the producer of novel bafilomycins and odoriferous sesquiterpenoids. J Biotechnol 262:89–93. https://doi.org/10.1016/j.jbiotec.2017.09.018
CAS Article PubMed Google Scholar
You J, Du M, Chen H, Zhang X, Zhang S, Chen J, Cheng Z, Chen D, Ye J (2018) BTEX degradation by a newly isolated bacterium: performance, kinetics, and mechanism. Int Biodeterior Biodegrad 129:202–208. https://doi.org/10.1016/j.ibiod.2018.02.012
CAS Article Google Scholar
Zylstra GJ, McCombie WR, Gibson DT, Finette BA (1988) Toluene degradation by Pseudomonas putida F1: genetic organization of the tod operon. Appl Environ Microbiol 54:1498–1503. https://aem.asm.org/content/54/6/1498.short

Download references

Acknowledgements

We are thankful to Dr. Asma Shaukat, Department of Pathology, Quaid-e-Azam Medical College, Bahawalpur, for providing us the antibiotic sensitivity discs.

Funding

This research did not receive any grant from funding agencies in the public, commercial or not-for-profit sectors.

Author information

Affiliations

Department of Biochemistry and Biotechnology, The Islamia University of Bahawalpur, Bahawalpur, Pakistan
Fatima Muccee & Samina Ejaz
Department of Chemistry, The Islamia University of Bahawalpur, Bahawalpur, Pakistan
Naheed Riaz

Authors

Fatima Muccee
View author publications
You can also search for this author in PubMed Google Scholar
Samina Ejaz
View author publications
You can also search for this author in PubMed Google Scholar
Naheed Riaz
View author publications
You can also search for this author in PubMed Google Scholar

Contributions

SE conceived the idea and designed study. FM performed all bench top work and wrote first draft of manuscript. NR interpreted the results of GC–MS analysis. All the authors contributed to finalize the manuscript.

Corresponding author

Correspondence to Samina Ejaz.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Human and animal rights statement

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

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Erko Stackebrandt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 687 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Muccee, F., Ejaz, S. & Riaz, N. Toluene degradation via a unique metabolic route in indigenous bacterial species. Arch Microbiol 201, 1369–1383 (2019). https://doi.org/10.1007/s00203-019-01705-0

Download citation

Received: 03 June 2019
Revised: 27 June 2019
Accepted: 10 July 2019
Published: 22 July 2019
Issue Date: December 2019
DOI: https://doi.org/10.1007/s00203-019-01705-0

Keywords

Toluene-degrading bacteria
Bioremediation
Consortium
Brevibacillus agri
Bacillus paralicheniformis
Burkholderia lata