Abstract
The presence of herbicides residues in soil represents a serious problem for agriculture. Quinclorac is a common herbicide applied in rice field, but its residue can cause abnormal growth in successive crop of tobacco in Southern China. Remediation by microorganisms is considered to be an environmentally friendly method to remove such pollutants injury. The aims of this study were to obtain quinclorac remediation isolates and to investigate the possible mechanism(s) of remediation. Six bacterial isolates were obtained from rhizosphere of rice-tobacco rotation fields, and were found to be capable of degrading quinclorac on a mineral salt medium (MSM), with degradation efficiency ranging from 2.1 to 23.7%. Among these isolates, J5 had the highest degradation efficiency, and was identified as Klebsiella variicola based on phylogenetic analyses and a metabolic profile generating by Biolog GEN III system. Bioremediation of quinclorac injury was confirmed using pot assays with tobacco, in which J5 reversed the detrimental effect of quinclorac on leaf area, leaf number, and plant height. The J5 isolate also seemed to promote plant growth, in terms of tobacco seedling growth and seed germination, which were 2.2 times and 1.6 times higher compared to untreated control, respectively. The mechanisms of plant growth promoting (PGP) traits were found to involve nitrogen-fixing, indole-3-acetic acid (IAA) production, and phosphate solubilization ability. In addition, proteomic analysis and relative quantitative PCR revealed an elevated level of 4-hydroxyphenylacetate 3-monooxygenase (HPMO) in quinclorac-treated J5, suggesting that this enzyme may play an important role in quinclorac remediation. This study showed that the J5 isolate could be exploited to not only assist in soil remediation due to quinclorac residue issues but also promote tobacco growth.
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Data availability
DNA sequences of J5 isolates were deposited in NCBI GenBank (https://www.ncbi.nlm.nih.gov/genbank/). Further procured and analyzed datasets are available from the corresponding author on reasonable request.
References
Afzal AM, Rasool MH, Waseem M, Aslam B (2017) Assessment of heavy metal tolerance and biosorptive potential of Klebsiella variicola isolated from industrial effluents. AMB Express 7:184. https://doi.org/10.1186/s13568-017-0482-2
Ahmad F, Iqbal S, Anwar S, Afzal M, Islam E, Mustafa T, Khan QM (2012) Enhanced remediation of chlorpyrifos from soil using ryegrass (Lollium multiflorum) and chlorpyrifos-degrading bacterium Bacillus pumilus C2A1. J Hazard Mater 237:110–115. https://doi.org/10.1016/j.jhazmat.2012.08.006
Chen Z, Wang J, Wan S, Li H, Chen J, He D, Li X, Deng J, Zhan S, Wang W (2004) Analysis and control of the abnormal growth of tobacco in areas in Guangdong (in Chinese). Acta Tabacaria Sinica 10:34–37
Cookson WR, Beare MH, Wilson PE (1998) Effects of prior crop residue management on microbial properties and crop residue decomposition. Appl Soil Ecol 7:179–188. https://doi.org/10.1016/S0929-1393(97)00032-2
Cycon M, Mrozik A, Piotrowska-Seget Z (2017) Bioaugmentation as a strategy for the remediation of pesticide-polluted soil: a review. Chemosphere 172:52–71. https://doi.org/10.1016/j.chemosphere.2016.12.129
de Souza R, Ambrosini A, Passaglia LMP (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38:401–419. https://doi.org/10.1590/s1415-475738420150053
Defez R, Andreozzi A, Bianco C (2017) The overproduction of indole-3-acetic acid (IAA) in endophytes upregulates nitrogen fixation in both bacterial cultures and inoculated rice plants. Microb Ecol 74:441–452. https://doi.org/10.1007/s00248-017-0948-4
Deletoile A, Decre D, Courant S, Passet V, Audo J, Grimont P, Arlet G, Brisse S (2009) Phylogeny and identification of Pantoea species and typing of Pantoea agglomerans strains by multilocus gene sequencing. J Clin Microbiol 47:300–310. https://doi.org/10.1128/jcm.01916-08
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Feng Y, Feng J, Shu QL (2018) Isolation and characterization of heterotrophic nitrifying and aerobic denitrifying Klebsiella pneumoniae and Klebsiella variicola strains from various environments. J Appl Microbiol 124:1195–1211. https://doi.org/10.1111/jam.13703
Feng Y, Huang Y, Zhan H, Bhatt P, Chen S (2020) An overview of strobilurin fungicide degradation:current status and future perspective. Front Microbiol. https://doi.org/10.3389/fmicb.2020.00389
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:1–15. https://doi.org/10.6064/2012/963401
Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796. https://doi.org/10.1128/aem.61.2.793-796.1995
Govindarajan M, Kwon S-W, Weon H-Y (2007) Isolation, molecular characterization and growth-promoting activities of endophytic sugarcane diazotroph Klebsiella sp GR9. World J Microbiol Biotechnol 23:997–1006. https://doi.org/10.1007/s11274-006-9326-y
Grossman K (1998) Quinclorac belongs to a new class of highly selective auxin herbicides. Weed Sci 46:707–716
Grossmann K (2010) Auxin herbicides: current status of mechanism and mode of action. Pest Manag Sci 66:113–120. https://doi.org/10.1002/ps.1860
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. https://doi.org/10.1093/sysbio/syq010
He H, Ye Z, Yang D, Yan J, Xiao L, Zhong T, Yuan M, Cai X, Fang Z, Jing Y (2013) Characterization of endophytic Rahnella sp JN6 from Polygonum pubescens and its potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Chemosphere 90:1960–1965. https://doi.org/10.1016/j.chemosphere.2012.10.057
Hu Y, Xi J, Qian Z, Zhang Y, Zhou T, Gu G, Zhan J, Chen F (2017) Comparison of four methods for quinclorac extraction from soil. Plant Prot (in Chinese) 43:125–128
Huang X, He J, Sun J, Pan J, Sun X, Li S (2007) Isolation and characterization of a metsulfuron-methyl degrading bacterium Methylopila sp S113. Int Biodeter Biodegr 60:152–158. https://doi.org/10.1016/j.ibiod.2007.02.005
Huang X, Shi J, Cui C, Yin H, Zhang R, Ma X, Zhang X (2016) Biodegradation of phenanthrene by Rhizobium petrolearium SL-1. J Appl Microbiol 121:1616–1626. https://doi.org/10.1111/jam.13292
James RM, Rudy E, Boswall AL (1999) Effects of quinclorac on following rotational crops. Weed Technol 13:548–553
Jiao S, Li Q, Zai X, Gao X, Wei G, Chen W (2019) Complexity of bacterial communities within the rhizospheres of legumes drives phenanthrene degradation. Geoderma 353:1–10. https://doi.org/10.1016/j.geoderma.2019.06.019
Kalyaanamoorthy S, Bui Quang M, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285
Karthik C, Elangovan N, Kumar TS, Govindharaju S, Barathi S, Oves M, Arulselvi PI (2017) Characterization of multifarious plant growth promoting traits of rhizobacterial strain AR6 under Chromium (VI) stress. Microbiol Res 204:65–71. https://doi.org/10.1016/j.micres.2017.07.008
Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19. https://doi.org/10.1007/s10311-008-0155-0
Kyung KS, Suh YT, Lee JK (1997) Behaviour of the herbicide quinclorae in a riceplant-grow lysimeter. Int J Environ Anal Chem 68:187–198. https://doi.org/10.1080/03067319708030490
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 371–375
Lang Z, Qi D, Dong J, Ren L, Zhu Q, Huang W, Liu Y, Lu D (2018) Isolation and characterization of a quinclorac-degrading Actinobacteria Streptomyces sp. strain AH-B and its implication on microecology in contaminated soil. Chemosphere 199:210–217. https://doi.org/10.1016/j.chemosphere.2018.01.133
Li Y, Chen W, Wang Y, Luo K, Li Y, Bai L, Luo F (2017) Identifying and sequencing a Mycobacterium sp. strain F4 as a potential bioremediation agent for quinclorac. PLoS ONE. https://doi.org/10.1371/journal.pone.0185721
Liang B, Lin Y, Zhu Q, Lin Z, Lin W (2001) Association of soil nutrients and pH in tobacco field in Fujian. Chin Tobacco Sci 22:25–27
Liu T, Liao Q, Yu F, Zi S, Tian S, Fan L (2022) Plant growth-promoting activities of bacterial endophytes isolated from the medicinal plant Pairs polyphylla var. yunnanensis. World J Microbiol Biotechnol. https://doi.org/10.1007/s11274-021-03194-0
Liu W, Hou J, Wang Q, Ding L, Luo Y (2014) Isolation and characterization of plant growth-promoting rhizobacteria and their effects on phytoremediation of petroleum-contaminated saline-alkali soil. Chemosphere 117:303–308. https://doi.org/10.1016/j.chemosphere.2014.07.026
Luis Perez-Rodriguez J, Rodriguez Escriba RC, Lorente Gonzalez GY, Gonzalez Olmedo JL, Martinez-Montero ME (2017) Effect of desiccation on physiological and biochemical indicators associated with the germination and vigor of cryopreserved seeds of Nicotiana tabacum L. cv. Sancti Spiritus 96. In Vitro Cell Dev Biol Plant 53:440–448. https://doi.org/10.1007/s11627-017-9857-y
Lϋ Z-M, Li Z-M, Sang L-Y, Min H (2008) Characterization of a strain capable of degrading a herbicide mixture of quinclorac and bensulfuronmethyl. Pedosphere 18:554–563. https://doi.org/10.1016/s1002-0160(08)60049-1
Lϋ ZM, Min H, Wu SW, Ruan AD (2003) Phylogenetic and degradation characterization of Burkholderia cepacia WZ1 degrading herbicide quinclorac. J Environ Sci Health B 38:771–782. https://doi.org/10.1081/pfc-120025560
Mattice JD, Skulman BW, Norman RJ, Gbur EE Jr (2010) Analysis of river water for rice pesticides in eastern Arkansas from 2002 to 2008. J Soil Water Conserv 65:130–140. https://doi.org/10.2489/jswc.65.2.130
McGuinness M, Dowling D (2009) Plant-associated bacterial degradation of toxic organic compounds in soil. Int J Environ Res Public Health 6:2226–2247. https://doi.org/10.3390/ijerph6082226
Minh BQ, Nguyen MA, von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30:1188–1195. https://doi.org/10.1093/molbev/mst024
Mir ZA, Ali S, Tyagi A, Ali A, Bhat JA, Jaiswal P, Qari HA, Oves M (2017) Degradation and conversion of endosulfanby newly isolated Pseudom meonasndocina ZAM1 strain. 3 Biotech. https://doi.org/10.1007/s13205-017-0823-5
Mutiat F-BY, Gbolahan B, Olu O (2018) A comparative study of the wild and mutated heavy metal resistant Klebsiella variicola generated for cadmium bioremedation. Bioremediat J 22:28–42
Pretto A, Loro VL, Menezes C, Silveira Moraes B, Boschmann Reimche G, Zanella R, de Ávila LA (2011) Commercial formulation containing quinclorac and metsulfuron-methyl herbicides inhibit acetylcholinesterase and induce biochemical alterations in tissues of Leporinus obtusidens. Ecotoxicol Environ Saf 74:336–341. https://doi.org/10.1016/j.ecoenv.2010.10.003
Resgalla C Jr, Noldin JA, Tamanaha MS, Deschamps FC, Eberhardt DS, Rorig LR (2007) Risk analysis of herbicide quinclorac residues in irrigated rice areas, Santa Catarina, Brazil. Ecotoxicology 16:565–571. https://doi.org/10.1007/s10646-007-0165-x
Saravanan A, Jeevanantham S, Narayanan VA, Kumar PS, Yaashikaa PR, Muthu CMM (2020) Rhizoremediation—a promising tool for the removal of soil contaminants: a review. J Environ Chem Eng 8:103543. https://doi.org/10.1016/j.jece.2019.103543
Silambarasan S, Vangnai AS (2016) Biodegradation of 4-nitroaniline by plant-growth promoting Acinetobacter sp. AVLB2 and toxicological analysis of its biodegradation metabolites. J Hazard Mater 302:426–436. https://doi.org/10.1016/j.jhazmat.2015.10.010
Singh B, Singh K (2016) Microbial degradation of herbicides. Crit Rev Microbiol 42:245–261. https://doi.org/10.3109/1040841x.2014.929564
Smith K, Evans DA, El-Hiti GA (2008) Role of modern chemistry in sustainable arable crop protection. Philos T R Soc B 363:623–637. https://doi.org/10.1098/rstb.2007.2174
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Trombin-Souza M, Grzybowski CRD, de Oliveira-Cauduro Y, Vieira ESN, Panobianco M (2017) Osmotic stress on genetically transformed tobacco plant seeds. J Seed Sci 39:426–432. https://doi.org/10.1590/2317-1545v39n4181134
Ueji M, Inao K (2001) Rice paddy field herbicides and their effects on the environment and ecosystems. Weed Biol Manag 1:71–79. https://doi.org/10.1046/j.1445-6664.2001.00002.x
Wang X, Tang D, Wang W (2020a) Adaptation strategies of Pseudomonas protegens SN15-2 to hyperosmotic growth environment. J Appl Microbiol 128:1720–1734. https://doi.org/10.1111/jam.14582
Wang Y-Y, Li P-S, Zhang B-X, Wang Y-P, Meng J, Gao Y-F, He X-M, Hu X-M (2020b) Identification of phosphate-solubilizing microorganisms and determination of their phosphate-solubilizing activity and growth-promoting capability. BioResources 15:2560–2578. https://doi.org/10.15376/biores.15.2.2560-2578
Wei C-Y, Lin L, Luo L-J, Xing Y-X, Hu C-J, Yang L-T, Li Y-R, An Q (2014) Endophytic nitrogen-fixing Klebsiella variicola strain DX120E promotes sugarcane growth. Biol Fertil Soils 50:657–666. https://doi.org/10.1007/s00374-013-0878-3
Wisniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6:359-U360. https://doi.org/10.1038/nmeth.1322
Xia X (2017) DAMBE6: New tools for microbial genomics, phylogenetics, and molecular evolution. J Hered 108:431–437. https://doi.org/10.1093/jhered/esx033
Xia XH, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7. https://doi.org/10.1016/s1055-7903(02)00326-3
Yang Y, Singh RP, Song D, Chen Q, Zheng X, Zhang C, Zhang M, Li Y (2020) Synergistic effect of Pseudomonas putida II-2 and Achromobacter sp. QC36 for the effective biodegradation of the herbicide quinclorac. Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2019.109826
Yu C, Yao J, Cai M, Wang F, Masakorala K, Liu H, Blake RE, Doni S, Ceccanti B (2013) Functional gene expression of oil-degrading bacteria resistant to hexadecane toxicity. Chemosphere 93:1424–1429. https://doi.org/10.1016/j.chemosphere.2013.07.035
Yu Q, Bin B, Zeng Y (2014) Quinclorac injury occurred causes and preventive measures on tobacco. J Antibiot 70:147–151. https://doi.org/10.1038/ja.2016.125 ((In Chinese))
Zhang B-H, Salam N, Cheng J, Li H-Q, Yang J-Y, Zha D-M, Guo Q-G, Li W-J (2017) Microbacterium lacusdiani sp nov., a phosphate-solubilizing novel actinobacterium isolated from mucilaginous sheath of Microcystis. J Antibiotics 70:147–151. https://doi.org/10.1038/ja.2016.125
Zhang D, Gao F, Jakovlic I, Zou H, Zhang J, Li WX, Wang GT (2020a) PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecol Res 20:348–355. https://doi.org/10.1111/1755-0998.13096
Zhang H, Mu W, Hou Z, Wu X, Zhao W, Zhang X, Pan H, Zhang S (2012a) Biodegradation of nicosulfuron by the bacterium Serratia marcescens N80. J Environ Sci Health B 47:153–160. https://doi.org/10.1080/03601234.2012.632249
Zhang Q, Wang B, Cao Z, Yu Y (2012b) Plasmid-mediated bioaugmentation for the degradation of chlorpyrifos in soil. J Hazard Mater 221:178–184. https://doi.org/10.1016/j.jhazmat.2012.04.024
Zhang W, Lin Z, Pang S, Bhatt P, Chen S (2020b) Insights into the biodegradation of lindane (γ-hexachlorocyclohexane) using a microbial system. Front Microbiol 11:522. https://doi.org/10.3389/fmicb.2020.00522
Zhong Q, Wan S, Shen C, Liu Y (2018) Decay of quinclorac in acidic paddy soil and risk evaluation to the subsequent crop, tobacco (Nicotiana tabacum L.). Bull Environ Contam Toxicol 101:284–287. https://doi.org/10.1007/s00128-018-2372-y
Zhou G-C, Wang Y, Ma Y, Zhai S, Zhou L-Y, Dai Y-J, Yuan S (2014) The metabolism of neonicotinoid insecticide thiamethoxam by soil enrichment cultures, and the bacterial diversity and plant growth-promoting properties of the cultured isolates. J Environ Sci Health B 49:381–390. https://doi.org/10.1080/03601234.2014.894761
Funding
This work was supported by the Science Foundation from the Fujian Branch of National Tobacco Corporation [Grant Numbers (2014)181], Natural Science Foundation of Fujian province (2020J01596) and the Innovative Science Foundation from Fujian Agriculture and Forestry University (CXZX2020022A and CXZX2020020A).
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by LL, ZT, ZL and ZQ. The first draft of the manuscript was written by LL and ZT. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Below is the link to the electronic supplementary material. Table S1 Primers and amplicon size of 16S rDNA, gyrB, and leuS used for phylogenetic tree analyses. Table S2 Parameters used in protein identification. Table S3 Saturation statistics of nucleotide substitution for all sites in 16S rDNA, gyrB, and leuS sequences. Fig. S1 Schematic procedure for isolating degrading culture from the rhizosphere soil of rice-tobacco rotation fields. The soil sample was added to the mineral salt medium amended with quinclorac. After one week of incubation, 1 ml of the resulting suspension was transferred to fresh mineral salt medium amended with quinclorac. The growing cultures were confirmed by inoculation on the Luria-Bertani broth (LB) plate. The cultures were enriched in a total of ten transfers. Fig. S2 The response of tobacco seedling to quinclorac. Fig. S3 The morphology of the J5 isolate colony on the Luria-Bertani broth (LB) medium.
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Li, L., Zhou, T., Zhong, L. et al. Bioremediation of quinclorac injury on tobacco by a rhizosphere bacterium. World J Microbiol Biotechnol 38, 147 (2022). https://doi.org/10.1007/s11274-022-03329-x
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DOI: https://doi.org/10.1007/s11274-022-03329-x