Abstract
Lindane contamination in different environmental compartments is still posing a serious threat to our environment and effective measures need to be taken for the detoxification of lindane. Soil bacteria isolated from agricultural fields are known to possess certain plant growth promoting traits like the production of phytohormones, production of ammonia, nitrogen fixation and solubilization of phosphorus, etc. In the present study, an indigenous bacterial strain Paracoccus sp. NITDBR1 have been isolated from an agricultural field in Manipur, India which could grow on 100 mg L−1 lindane as the sole source of carbon and could degrade up to 90% of lindane in mineral salt media under liquid culture conditions in 8 days. The strain NITDBR1 was able to form biofilm in lindane media and the addition of substrate like glucose and sucrose enhanced the biofilm formation by 1.3 and 1.17-fold respectively in 3 days. The strain NITDBR1 could produce glycolipid and glycoprotein based biosurfactants. It was also found to possess plant growth promoting traits like nitrogen fixation and indole-3-acetic acid production to assist crop production. The phytotoxicity studies carried out on mustard seeds revealed that the degradation products formed after treatment with NITDBR1 could lower the toxicity of lindane for root elongation by 1.3-fold. Therefore, strain NITDBR1 could be useful for the bioremediation of soil contaminated with lindane with lesser damage to the environment, biofilm forming ability may help the bacteria survive under stressed environmental conditions, and biosurfactant production will help in increasing the bioavailability of contaminants. The plant growth promoting traits can be beneficial for agriculture. With such soil friendly activities coupled with pesticide degradation, this strain can be used for environmental as well as agricultural applications.
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Abdul Salam J, Lakshmi V, Das D, Das N (2013) Biodegradation of lindane using a novel yeast strain, Rhodotorula sp. VITJzN03 isolated from agricultural soil. World J Microbiol Biotechnol Abdul Sala. https://doi.org/10.1007/s11274-012-1201-4
Abhilash PC, Srivastava S, Singh N (2011) Comparative bioremediation potential of four rhizospheric microbial species against lindane. Chemosphere 82:56–63. https://doi.org/10.1016/j.chemosphere.2010.10.009
Akbar S, Sultan S (2016) Soil bacteria showing a potential of chlorpyrifos degradation and plant growth enhancement. Braz J Microbiol 47:563–570. https://doi.org/10.1016/j.bjm.2016.04.009
An X, Cheng Y, Huang M et al (2018) Treating organic cyanide-containing groundwater by immobilization of a nitrile-degrading bacterium with a biofilm-forming bacterium using fluidized bed reactors. Environ Pollut 237:908–916. https://doi.org/10.1016/j.envpol.2018.01.087
Anupama KS, Paul S (2010) Ex situ and in situ biodegradation of lindane by Azotobacter chroococcum. J Environ Sci Heal - Part B Pestic Food Contam Agric Wastes. https://doi.org/10.1080/03601230903404465
ATSDR, Agency for toxic substances and disease registry, US Department of Health and Human Services (1999) Toxicological profile for alpha-, beta-, gamma-, and delta-hexachlorocyclohexane. Clement and Associates, Tauranga
Bajaj S, Sagar S, Khare S, Singh DK (2017) Biodegradation of γ-hexachlorocyclohexane (lindane) by halophilic bacterium Chromohalobacter sp. LD2 isolated from HCH dumpsite. Int Biodeterior Biodegrad 122:23–28. https://doi.org/10.1016/j.ibiod.2017.04.014
Bakkiyaraj D, Pandian STK (2010) In vitro and in vivo antibiofilm activity of a coral associated actinomycete against drug resistant Staphylococcus aureus biofilms. Biofouling 26:711–717. https://doi.org/10.1080/08927014.2010.511200
Benimeli CS, Castro GR, Chaile AP, Amoroso MJ (2007) Lindane uptake and degradation by aquatic Streptomyces sp. strain M7. Int Biodeterior Biodegrad. https://doi.org/10.1016/j.ibiod.2006.07.014
Beyer A, Matthies M (2001) Long-range transport potential of semivolatile organic chemicals in coupled air-water systems. Environ Sci Pollut Res 8:173–179. https://doi.org/10.1007/BF02987382
Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538
Cappuccino JC, Sherman N (1992) In: Microbiology: A Laboratory Manual, New York, pp 125–179
Carrillo PG, Mardaraz C, Pitta-Alvarez SI, Giulietti AM (1996) Isolation and selection of biosurfactant-producing bacteria. World J Microbiol Biotechnol 12:82–84. https://doi.org/10.1007/BF00327807
Christensen GD, Simpson WA, Bisno AL, Beachey EH (1982) Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infect Immun 37:318–326
Cooper DG, Goldenberg BG (1987) Surface-active agents from two Bacillus species. Appl Environ Microbiol 53:224–229 0099-2240/87/020224
Deo PG, Karanth NG, Gopalakrishna N, Karanth K (1994) Biodegradation of hexachlorocyclohexane isomers in soil and food environment. Crit Rev Microbiol 20:57–78. https://doi.org/10.3109/10408419409113546
Dubey RC, Maheshwari DK (2002) Practical microbiology. S.Chand & company Ltd., New Delhi, pp 172–174
Etesami H, Alikhani HA (2016) Rhizosphere and endorhiza of oilseed rape (Brassica napus L.) plant harbor bacteria with multifaceted beneficial effects. Biol Control 94:11–24. https://doi.org/10.1016/j.biocontrol.2015.12.003
Garcia MT, Campos E, Dalmau M et al (2006) Inhibition of biogas production by alkyl benzene sulfonates (LAS) in a screening test for anaerobic biodegradability. Biodegradation 17:39–46. https://doi.org/10.1007/s10792-005-0078-8
Gordon SA, Weber RP (1951) Colorimetric Estimation of Inodoleacetic Acid. Plant Physiol 26:192–195. https://doi.org/10.1016/0003-2697(76)90514-5
Guillén-Jiménez FDM, Cristiani-Urbina E, Cancino-Díaz JC et al (2012) Lindane biodegradation by the Fusarium verticillioides AT-100 strain, isolated from Agave tequilana leaves: Kinetic study and identification of metabolites. Int Biodeterior Biodegrad 74:36–47. https://doi.org/10.1016/j.ibiod.2012.04.020
Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133:71–84. https://doi.org/10.1016/j.envpol.2004.04.015
Kumar D, Kumar A, Sharma J (2016) Degradation study of lindane by novel strains Kocuria sp. DAB-1Y and Staphylococcus sp. DAB-1W. Bioresour Bioprocess 3:53. https://doi.org/10.1186/s40643-016-0130-8
Lal R, Pandey G, Sharma P et al (2010) Biochemistry of Microbial Degradation of Hexachlorocyclohexane and Prospects for Bioremediation. Microbiol Mol Biol Rev 74:58–80. https://doi.org/10.1128/MMBR.00029-09
Lima TMS, Procópio LC, Brandão FD et al (2011) Biodegradability of bacterial surfactants. Biodegradation 22:585–592. https://doi.org/10.1007/s10532-010-9431-3
Manickam N, Mau M, Schlömann M (2006) Characterization of the novel HCH-degrading strain, Microbacterium sp. ITRC1. Appl Microbiol Biotechnol 69:580–588. https://doi.org/10.1007/s00253-005-0162-z
Manickam N, Bajaj A, Saini HS, Shanker R (2012) Surfactant mediated enhanced biodegradation of hexachlorocyclohexane (HCH) isomers by Sphingomonas sp. NM05. Biodegradation 23:673–682. https://doi.org/10.1007/s10532-012-9543-z
Mathurasa L, Tongcumpou C, Sabatini DA, Luepromchai E (2012) Anionic surfactant enhanced bacterial degradation of tributyltin in soil. Int Biodeterior Biodegrad 75:7–14. https://doi.org/10.1016/j.ibiod.2012.06.027
Mohan PK, Nakhla G, Yanful EK (2006) Biokinetics of biodegradation of surfactants under aerobic, anoxic and anaerobic conditions. Water Res 40:533–540. https://doi.org/10.1016/j.watres.2005.11.030
Mulvaney RL, Khan SA, Ellsworth TR (2009) Synthetic Nitrogen Fertilizers Deplete Soil Nitrogen: A Global Dilemma for Sustainable Cereal Production. J Environ Qual. 38(6):2295–2314. https://doi.org/10.2134/jeq2008.0527
Nagasawa S, Kikuchi R, Nagata Y et al (1993) Aerobic mineralization of γ-HCH by Pseudomonas paucimobilis UT26. Chemosphere 26:1719–1728. https://doi.org/10.1016/0045-6535(93)90115-L
Nisha KN, Devi V, Varalakshmi P, Ashokkumar B (2015) Biodegradation and utilization of dimethylformamide by biofilm forming Paracoccus sp. strains MKU1 and MKU2. Bioresour Technol 188:9–13. https://doi.org/10.1016/j.biortech.2015.02.042
Ohisa N, Yamaguchi M, Kurihara N (1980) Lindane degradation by cell-free extracts of Clostridium rectum. Arch Microbiol 125:221–225. https://doi.org/10.1007/BF00446880
Okeke BC, Siddique T, Arbestain MC, Frankenberger WT (2002) Biodegradation of gamma-hexachlorocyclohexane (lindane) and alpha-hexachlorocyclohexane in water and a soil slurry by a Pandoraea species. J Agric Food Chem 50:2548–2555. https://doi.org/10.1007/BF00510822
Pacwa-Płociniczak M, Płociniczak T et al (2016) Isolation of hydrocarbon-degrading and biosurfactant-producing bacteria and assessment their plant growth-promoting traits. J Environ Manage 168:175–184. https://doi.org/10.1016/j.jenvman.2015.11.058
Pannu R, Kumar D (2017) Process optimization of γ- Hexachlorocyclohexane degradation using three novel Bacillus sp. strains. Biocatal Agric Biotechnol 11:97–107
Passari AK, Mishra VK et al (2016) Phytohormone production endowed with antagonistic potential and plant growth promoting abilities of culturable endophytic bacteria isolated from Clerodendrum colebrookianum Walp. Microbiol Res 193:57–73. https://doi.org/10.1016/j.micres.2016.09.006
Pokhrel LR, Dubey B (2013) Evaluation of developmental responses of two crop plants exposed to silver and zinc oxide nanoparticles. Sci Total Environ 452–453:321–332. https://doi.org/10.1016/j.scitotenv.2013.02.059
Qu J, Xu Y, Ai GM et al (2015) Novel Chryseobacterium sp. PYR2 degrades various organochlorine pesticides (OCPs) and achieves enhancing removal and complete degradation of DDT in highly contaminated soil. J Environ Manage 161:350–357. https://doi.org/10.1016/j.jenvman.2015.07.025
Salam JA, Das N (2014) Lindane degradation by Candida VITJzN04, a newly isolated yeast strain from contaminated soil: Kinetic study, enzyme analysis and biodegradation pathway. World J Microbiol Biotechnol 30:1301–1313. https://doi.org/10.1007/s11274-013-1551-6
Sangwan N, Lata P, Dwivedi V et al (2012) Comparative Metagenomic Analysis of Soil Microbial Communities Across Three Hexachlorocyclohexane Contamination Levels. PLoS One 7:1–12. https://doi.org/10.1371/journal.pone.0046219
Sasser M (2001) Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids. Tech Note 101:1–6
Sharma AD, Singh J (2005) A nonenzymatic method to isolate genomic DNA from bacteria and actinomycete. Anal Biochem 337:354–356. https://doi.org/10.1016/j.ab.2004.11.029
Siegmund I, Wagner F (1991) New method for detecting rhamnolipids excreted by Pseudomonas species during growth on mineral agar. Biotechnol Tech 5:265–268. https://doi.org/10.1007/BF02438660
Thompson JD, Gibson TJ, Plewniak F et al (1997) The CLUSTAL X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876
Vaux D, Cottingham M (2001) Method and apparatus for measuring surface configuration. patent number WO 2007/039729 A1
Vega FA, Covelo EF, Andrade ML (2007) Accidental Organochlorine Pesticide Contamination of Soil in Porriño, Spain. J Environ Qual 36:272. https://doi.org/10.2134/jeq2006.0053
Wagner SC (2011) Biological Nitrogen Fixation. Nature Education Knowledge 3(10):15. http://www.nature.com/scitable/knowledge/library/biological-nitrogen-fixation-23570419
Welp G, Brümmer GW (1999) Effects of organic pollutants on soil microbial activity: influence of sorption, solubility, and speciation. Ecotoxicol Env Saf 43:83–90. https://doi.org/10.1006/eesa.1999.1770
Weselowski B, Nathoo N, Eastman AW et al (2016) Isolation, identification and characterization of Paenibacillus polymyxa CR1 with potentials for biopesticide, biofertilization, biomass degradation and biofuel production. BMC Microbiol 16:1–10. https://doi.org/10.1186/s12866-016-0860-y
Yang L, Watts DJ (2005) Particle surface characteristics may play an important role in phytotoxicity of alumina nanoparticles. Toxicol Lett 158:122–132. https://doi.org/10.1016/j.toxlet.2005.03.003
Zhang Y, Wang F, Zhu X et al (2015) Extracellular polymeric substances govern the development of biofilm and mass transfer of polycyclic aromatic hydrocarbons for improved biodegradation. Bioresour Technol 193:274–280. https://doi.org/10.1016/j.biortech.2015.06.110
Acknowledgments
We thank Centre of Excellence, National Institute of Technology Durgapur, West Bengal for FESEM analysis, Bose Institute, Kolkata for FTIR analysis, Royal Life Sciences Pvt. Ltd., Secunderabad for GC-FAME and PathCare Labs Pvt Ltd, Hyderabad for microbial identification.
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Sahoo, B., Ningthoujam, R. & Chaudhuri, S. Isolation and characterization of a lindane degrading bacteria Paracoccus sp. NITDBR1 and evaluation of its plant growth promoting traits. Int Microbiol 22, 155–167 (2019). https://doi.org/10.1007/s10123-018-00037-1
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DOI: https://doi.org/10.1007/s10123-018-00037-1