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ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

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Research Article

Infestation of Rice by Gall Midge Influences Density and Diversity of Pseudomonas and Wolbachia in the Host Plant Microbiome

Author(s): Deepak K. Sinha, Ayushi Gupta, Ayyagari P. Padmakumari, Jagadish S. Bentur and Suresh Nair*

Volume 23, Issue 2, 2022

Published on: 14 April, 2022

Page: [126 - 136] Pages: 11

DOI: 10.2174/1389202923666220401101604

Price: $65

Abstract

Background: The virulence of phytophagous insects is predominantly determined by their ability to evade or suppress host defense for their survival. The rice gall midge (GM, Orseolia oryzae), a monophagous pest of rice, elicits a host defense similar to the one elicited upon pathogen attack. This could be due to the GM feeding behaviour, wherein the GM endosymbionts are transferred to the host plant via oral secretions, and as a result, the host mounts an appropriate defense response(s) (i.e., up-regulation of the salicylic acid pathway) against these endosymbionts.

Methods: The current study aimed to analyze the microbiome present at the feeding site of GM maggots to determine the exchange of bacterial species between GM and its host and to elucidate their role in rice-GM interaction using a next-generation sequencing approach.

Results: Our results revealed differential representation of the phylum Proteobacteria in the GMinfested and -uninfested rice tissues. Furthermore, analysis of the species diversity of Pseudomonas and Wolbachia supergroups at the feeding sites indicated the exchange of bacterial species between GM and its host upon infestation.

Conclusion: As rice-GM microbial associations remain relatively unstudied, these findings not only add to our current understanding of microbe-assisted insect-plant interactions but also provide valuable insights into how these bacteria drive insect-plant coevolution. Moreover, to the best of our knowledge, this is the first report analyzing the microbiome of a host plant (rice) at the feeding site of its insect pest (GM).

Keywords: Orseolia oryzae, plant-insect interaction, rice microbiome, insect microbiome, Proteobacteria, 16S rRNA, ftsZ.

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[1]
Bentur, J.S.; Rawat, N.; Divya, D.; Sinha, D.K.; Agarrwal, R.; Atray, I.; Nair, S. Rice-gall midge interactions: Battle for survival. J. Insect Physiol., 2016, 84, 40-49.
[http://dx.doi.org/10.1016/j.jinsphys.2015.09.008] [PMID: 26455891]
[2]
Sardesai, N.; Rajyashri, K.R.; Behura, S.K.; Nair, S.; Mohan, M. Genetic, physiological and molecular interactions of rice and its major dipteran pest, gall midge. Plant Cell Tissue Organ Cult., 2001, 64(2/3), 115-131.
[http://dx.doi.org/10.1023/A:1010727607866]
[3]
Sinha, D.K.; Bentur, J.S.; Nair, S. Compatible interaction with its rice host leads to enhanced expression of the gamma subunit of oligosaccharyl transferase in the Asian rice gall midge, Orseolia oryzae. Insect Mol. Biol., 2011, 20(5), 567-575.
[http://dx.doi.org/10.1111/j.1365-2583.2011.01085.x] [PMID: 21668550]
[4]
Sinha, D.K.; Atray, I.; Bentur, J.S.; Nair, S. Expression of Orseolia oryzae nucleoside diphosphate kinase (OoNDPK) is enhanced in rice gall midge feeding on susceptible rice hosts and its over-expression leads to salt tolerance in Escherichia coli. Insect Mol. Biol., 2012, 21(6), 593-603.
[http://dx.doi.org/10.1111/j.1365-2583.2012.01163.x] [PMID: 23126268]
[5]
Sinha, D.K.; Nagaraju, J.; Tomar, A.; Bentur, J.S.; Nair, S. Pyrosequencing-based transcriptome analysis of the asian rice gall midge reveals differential response during compatible and incompatible interaction. Int. J. Mol. Sci., 2012, 13(10), 13079-13103.
[http://dx.doi.org/10.3390/ijms131013079] [PMID: 23202939]
[6]
Sinha, D.K.; Atray, I.; Agarrwal, R.; Bentur, J.S.; Nair, S. Genomics of the Asian rice gall midge and its interactions with rice. Curr. Opin. Insect Sci., 2017, 19, 76-81.
[http://dx.doi.org/10.1016/j.cois.2017.03.004] [PMID: 28521946]
[7]
Abramovitch, R.B.; Anderson, J.C.; Martin, G.B. Bacterial elicitation and evasion of plant innate immunity. Nat. Rev. Mol. Cell Biol., 2006, 7(8), 601-611.
[http://dx.doi.org/10.1038/nrm1984] [PMID: 16936700]
[8]
Agarrwal, R.; Bentur, J.S.; Nair, S. Gas chromatography mass spectrometry based metabolic profiling reveals biomarkers involved in rice-gall midge interactions. J. Integr. Plant Biol., 2014, 56(9), 837-848.
[http://dx.doi.org/10.1111/jipb.12244] [PMID: 25059749]
[9]
Divya, D.; Madhavi, K.R.; Dass, M.A.; Maku, R.V.; Mallikarjuna, G.; Sundaram, R.M.; Laha, G.S.; Padmakumari, A.P.; Patel, H.K.; Prasad, M.S.; Sonti, R.V.; Bentur, J.S. Expression profile of defence genes in rice lines pyramided with resistance genes against bacterial blight, fungal blast and insect gall midge. Rice (N. Y.), 2018, 11(1), 40.
[http://dx.doi.org/10.1186/s12284-018-0231-4] [PMID: 30006850]
[10]
Divya, D.; Sahu, N.; Nair, S.; Bentur, J.S. Map-based cloning and validation of a gall midge resistance gene, Gm8, encoding a proline-rich protein in the rice variety Aganni. Mol. Biol. Rep., 2018, 45(6), 2075-2086.
[http://dx.doi.org/10.1007/s11033-018-4364-8] [PMID: 30209741]
[11]
Kumar, V.A.; Balachiranjeevi, C.H.; Naik, S.; Rekha, G.; Rambabu, R.; Harika, G.; Pranathi, K.; Hajira, S.K.; Anila, M.; Kousik, M.; Kale, R.; Dilip Kumar, T.; Prasad, M.S.; Hari Prasad, A.S.; Padmakumari, A.P.; Laha, G.S.; Balachandran, S.M.; Madhav, M.S.; Senguttuvel, P.; Kemparajau, K.B.; Fiyaz, A.R.; Bentur, J.S.; Viraktamath, B.C.; Ravindra Babu, V.; Sundaram, R.M. Marker-assisted pyramiding of bacterial blight and gall midge resistance genes into RPHR-1005, the restorer line of the popular rice hybrid DRRH-3. Mol. Breed., 2017, 37(7), 86.
[http://dx.doi.org/10.1007/s11032-017-0687-8]
[12]
Rawat, N.; Chiruvuri Naga, N.; Raman Meenakshi, S.; Nair, S.; Bentur, J.S. A novel mechanism of gall midge resistance in the rice variety Kavya revealed by microarray analysis. Funct. Integr. Genomics, 2012, 12(2), 249-264.
[http://dx.doi.org/10.1007/s10142-012-0275-2] [PMID: 22447493]
[13]
Lakshmi, P.V.; Amudhan, S.; Bindu, K.H.; Cheralu, C.; Bentur, J.S. A new biotype of the Asian rice gall midge Orseolia oryzae (Diptera: Cecidomyiidae) characterized from the Warangal population in Andhra Pradesh, India. Int. J. Trop. Insect Sci., 2006, 26, 207-211.
[14]
Gatehouse, J.A. Plant resistance towards insect herbivores: a dynamic interaction. New Phytol., 2002, 156(2), 145-169.
[http://dx.doi.org/10.1046/j.1469-8137.2002.00519.x] [PMID: 33873279]
[15]
Rawat, N.; Himabindu, K.; Neeraja, C.N.; Nair, S.; Bentur, J.S. Suppressive subtraction hybridization reveals that rice gall midge attack elicits plant-pathogen-like responses in rice. Plant Physiol. Biochem., 2013, 63, 122-130.
[http://dx.doi.org/10.1016/j.plaphy.2012.11.021] [PMID: 23257077]
[16]
Rawat, N.; Sinha, D.K.; Rajendrakumar, P.; Shrivastava, P.; Neeraja, C.N.; Sundaram, R.M.; Nair, S.; Bentur, J.S. Role of pathogenesis-related genes in rice–gall midge interactions. Curr. Sci., 2010, 99(10), 1361-1368.
[17]
Gupta, A.; Nair, S. Dynamics of insect–microbiome interaction influence host and microbial symbiont. Front. Microbiol., 2020, 11, 1357.
[http://dx.doi.org/10.3389/fmicb.2020.01357] [PMID: 32676060]
[18]
Chrostek, E.; Pelz-Stelinski, K.; Hurst, G.D.D.; Hughes, G.L. Horizontal transmission of intracellular insect symbionts via plants. Front. Microbiol., 2017, 8, 2237.
[http://dx.doi.org/10.3389/fmicb.2017.02237] [PMID: 29234308]
[19]
Erb, M.; Meldau, S.; Howe, G.A. Role of phytohormones in insect-specific plant reactions. Trends Plant Sci., 2012, 17(5), 250-259.
[http://dx.doi.org/10.1016/j.tplants.2012.01.003] [PMID: 22305233]
[20]
Pieterse, C.M.J.; Van der Does, D.; Zamioudis, C.; Leon-Reyes, A.; Van Wees, S.C.M. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol., 2012, 28(1), 489-521.
[http://dx.doi.org/10.1146/annurev-cellbio-092910-154055] [PMID: 22559264]
[21]
Howe, G.A.; Jander, G. Plant immunity to insect herbivores. Annu. Rev. Plant Biol., 2008, 59(1), 41-66.
[http://dx.doi.org/10.1146/annurev.arplant.59.032607.092825] [PMID: 18031220]
[22]
Durrant, W.E.; Dong, X. Systemic acquired resistance. Annu. Rev. Phytopathol., 2004, 42(1), 185-209.
[http://dx.doi.org/10.1146/annurev.phyto.42.040803.140421] [PMID: 15283665]
[23]
Chung, S.H.; Rosa, C.; Scully, E.D.; Peiffer, M.; Tooker, J.F.; Hoover, K.; Luthe, D.S.; Felton, G.W. Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc. Natl. Acad. Sci. USA, 2013, 110(39), 15728-15733.
[http://dx.doi.org/10.1073/pnas.1308867110] [PMID: 24019469]
[24]
Felton, G.W.; Chung, S.H.; Hernandez, M.G.E.; Louis, J.; Peiffer, M.; Tian, D. Herbivore oral secretions are the first line of protection against plant-induced defences.Annual Plant Reviews; John Wiley & Sons, Ltd: Chichester, UK, 2018, pp. 37-76.
[http://dx.doi.org/10.1002/9781119312994.apr0506]
[25]
Ojha, A.; Sinha, D.K.; Padmakumari, A.P.; Bentur, J.S.; Nair, S. Bacterial community structure in the Asian rice gall midge reveals a varied microbiome rich in Proteobacteria. Sci. Rep., 2017, 7(1), 9424.
[http://dx.doi.org/10.1038/s41598-017-09791-0] [PMID: 28842593]
[26]
Werren, J.H.; Baldo, L.; Clark, M.E. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol., 2008, 6(10), 741-751.
[http://dx.doi.org/10.1038/nrmicro1969] [PMID: 18794912]
[27]
Werren, J.H. Biology of Wolbachia. Annu. Rev. Entomol., 1997, 42(1), 587-609.
[http://dx.doi.org/10.1146/annurev.ento.42.1.587] [PMID: 15012323]
[28]
Behura, S.K.; Sahu, S.C.; Mohan, M.; Nair, S. Wolbachia in the Asian rice gall midge, Orseolia oryzae (Wood-Mason): correlation between host mitotypes and infection status. Insect Mol. Biol., 2001, 10(2), 163-171.
[http://dx.doi.org/10.1046/j.1365-2583.2001.00251.x] [PMID: 11422512]
[29]
Silby, M.W.; Winstanley, C.; Godfrey, S.A.; Levy, S.B.; Jackson, R.W. Pseudomonas genomes: diverse and adaptable. FEMS Microbiol. Rev., 2011, 35(4), 652-680.
[http://dx.doi.org/10.1111/j.1574-6976.2011.00269.x] [PMID: 21361996]
[30]
Loper, J.E.; Hassan, K.A.; Mavrodi, D.V.; Davis, E.W., II; Lim, C.K.; Shaffer, B.T.; Elbourne, L.D.; Stockwell, V.O.; Hartney, S.L.; Breakwell, K.; Henkels, M.D.; Tetu, S.G.; Rangel, L.I.; Kidarsa, T.A.; Wilson, N.L.; van de Mortel, J.E.; Song, C.; Blumhagen, R.; Radune, D.; Hostetler, J.B.; Brinkac, L.M.; Durkin, A.S.; Kluepfel, D.A.; Wechter, W.P.; Anderson, A.J.; Kim, Y.C.; Pierson, L.S., III; Pierson, E.A.; Lindow, S.E.; Kobayashi, D.Y.; Raaijmakers, J.M.; Weller, D.M.; Thomashow, L.S.; Allen, A.E.; Paulsen, I.T. Comparative genomics of plant-associated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet., 2012, 8(7), e1002784.
[http://dx.doi.org/10.1371/journal.pgen.1002784] [PMID: 22792073]
[31]
Saati-Santamaría, Z.; Rivas, R. Kolařik, M.; García-Fraile, P. A new perspective of Pseudomonas—host interactions: Distribution and potential ecological functions of the genus Pseudomonas within the bark beetle holobiont. Biology (Basel), 2021, 10(2), 164.
[http://dx.doi.org/10.3390/biology10020164] [PMID: 33669823]
[32]
Maniatis, T.; Fritsch, E.F.; Sambrook, J. Molecular Cloning – A Laboratory Manual, 7th ed; Cold Spring Harbor Laboratory: New York, 1982.
[33]
Klindworth, A.; Pruesse, E.; Schweer, T.; Peplies, J.; Quast, C.; Horn, M.; Glöckner, F.O. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res., 2013, 41(1), e1.
[http://dx.doi.org/10.1093/nar/gks808] [PMID: 22933715]
[34]
Magoč T.; Salzberg, S.L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 2011, 27(21), 2957-2963.
[http://dx.doi.org/10.1093/bioinformatics/btr507] [PMID: 21903629]
[35]
Li, W.; Fu, L.; Niu, B.; Wu, S.; Wooley, J. Ultrafast clustering algorithms for metagenomic sequence analysis. Brief. Bioinform., 2012, 13(6), 656-668.
[http://dx.doi.org/10.1093/bib/bbs035] [PMID: 22772836]
[36]
Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Peña, A.G.; Goodrich, J.K.; Gordon, J.I.; Huttley, G.A.; Kelley, S.T.; Knights, D.; Koenig, J.E.; Ley, R.E.; Lozupone, C.A.; McDonald, D.; Muegge, B.D.; Pirrung, M.; Reeder, J.; Sevinsky, J.R.; Turnbaugh, P.J.; Walters, W.A.; Widmann, J.; Yatsunenko, T.; Zaneveld, J.; Knight, R. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods, 2010, 7(5), 335-336.
[http://dx.doi.org/10.1038/nmeth.f.303] [PMID: 20383131]
[37]
Chao, A. Nonparametric estimation of the number of classes in a population. Scand. J. Stat., 1984, 11(4), 265-270.
[38]
O’Neill, S.L.; Giordano, R.; Colbert, A.M.E.; Karr, T.L.; Robertson, H.M. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl. Acad. Sci. USA, 1992, 89(7), 2699-2702.
[http://dx.doi.org/10.1073/pnas.89.7.2699] [PMID: 1557375]
[39]
Spilker, T.; Coenye, T.; Vandamme, P. LiPuma, J.J. PCR-based assay for differentiation of Pseudomonas aeruginosa from other Pseudomonas species recovered from cystic fibrosis patients. J. Clin. Microbiol., 2004, 42(5), 2074-2079.
[http://dx.doi.org/10.1128/JCM.42.5.2074-2079.2004] [PMID: 15131172]
[40]
Lo, N.; Casiraghi, M.; Salati, E.; Bazzocchi, C.; Bandi, C. How many Wolbachia supergroups exist? Mol. Biol. Evol., 2002, 19(3), 341-346.
[http://dx.doi.org/10.1093/oxfordjournals.molbev.a004087] [PMID: 11861893]
[41]
Shannon, C.E.; Weaver, W. The Mathematical Theory of Communication; University of Illinois Press: Chicago, 1949.
[42]
Simpson, E.H. Measurement of diversity. Nature, 1949, 688(4148), 688.
[http://dx.doi.org/10.1038/163688a0]
[43]
Faddeeva-Vakhrusheva, A.; Kraaijeveld, K.; Derks, M.F.L.; Anvar, S.Y.; Agamennone, V.; Suring, W.; Kampfraath, A.A.; Ellers, J.; Le Ngoc, G.; van Gestel, C.A.M.; Mariën, J.; Smit, S.; van Straalen, N.M.; Roelofs, D. Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida. BMC Genomics, 2017, 18(1), 493.
[http://dx.doi.org/10.1186/s12864-017-3852-x] [PMID: 28659179]
[44]
West, S.A.; Cook, J.M.; Werren, J.H.; Godfray, H.C.J. Wolbachia in two insect host-parasitoid communities. Mol. Ecol., 1998, 7(11), 1457-1465.
[http://dx.doi.org/10.1046/j.1365-294x.1998.00467.x] [PMID: 9819901]
[45]
Purcell, A.H.; Suslow, K.G.; Klein, M. Transmission via plants of an insect pathogenic bacterium that does not multiply or move in plants. Microb. Ecol., 1994, 27(1), 19-26.
[http://dx.doi.org/10.1007/BF00170111] [PMID: 24190165]
[46]
Caspi-Fluger, A.; Inbar, M.; Mozes-Daube, N.; Katzir, N.; Portnoy, V.; Belausov, E.; Hunter, M.S.; Zchori-Fein, E. Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc. Biol. Sci., 2012, 279(17341), 1791-1796.
[http://dx.doi.org/10.1098/rspb.2011.2095] [PMID: 22113034]
[47]
Gonella, E.; Pajoro, M.; Marzorati, M.; Crotti, E.; Mandrioli, M.; Pontini, M.; Bulgari, D.; Negri, I.; Sacchi, L.; Chouaia, B.; Daffonchio, D.; Alma, A. Plant-mediated interspecific horizontal transmission of an intracellular symbiont in insects. Sci. Rep., 2015, 5(1), 15811.
[http://dx.doi.org/10.1038/srep15811] [PMID: 26563507]
[48]
Li, S.J.; Ahmed, M.Z.; Lv, N.; Shi, P.Q.; Wang, X.M.; Huang, J.L.; Qiu, B.L. Plantmediated horizontal transmission of Wolbachia between whiteflies. ISME J., 2017, 11(4), 1019-1028.
[http://dx.doi.org/10.1038/ismej.2016.164] [PMID: 27935594]
[49]
Engel, P.; Moran, N.A. The gut microbiota of insects - diversity in structure and function. FEMS Microbiol. Rev., 2013, 37(5), 699-735.
[http://dx.doi.org/10.1111/1574-6976.12025] [PMID: 23692388]
[50]
Hammer, T.J.; Moran, N.A. Links between metamorphosis and symbiosis in holometabolous insects. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2019, 374(1783), 20190068.
[http://dx.doi.org/10.1098/rstb.2019.0068] [PMID: 31438811]
[51]
Wells, J.; Varel, V. Symbiosis of Plants, Animals and Microbes.Animal Welfare in Animal Agriculture: Husbandry, Stewardship and Sustainability in Animal Production; Pond, W.G.; Bazer, F.W.; Rollin, B.E., Eds.; CRC Press: New York, 2011, pp. 185-203.
[52]
Sang, R.C.; Jura, W.G.; Otieno, L.H.; Mwangi, R.W. The effects of a DNA virus infection on the reproductive potential of female tsetse flies, Glossina morsitans centralis and Glossina morsitans morsitans (Diptera: Glossinidae). Mem. Inst. Oswaldo Cruz, 1998, 93(6), 861-864.
[http://dx.doi.org/10.1590/S0074-02761998000600030] [PMID: 9921317]
[53]
Roy, M.; Chatterjee, S.N.; Roy, P.; Dangar, T.K. Significance of the midgut bacterium Pseudomonas fluorescens on Culex vishnui (Diptera: Culicidae) larval development. Int. J. Trop. Insect Sci., 2010, 30(4), 182-185.
[http://dx.doi.org/10.1017/S1742758410000366]
[54]
Panayidou, S.; Georgiades, K.; Christofi, T.; Tamana, S.; Promponas, V.J.; Apidianakis, Y. Pseudomonas aeruginosa core metabolism exerts a widespread growth-independent control on virulence. Sci. Rep., 2020, 10(1), 9505.
[http://dx.doi.org/10.1038/s41598-020-66194-4] [PMID: 32528034]
[55]
Gunsalus, I.C.; Marshall, V.P.; Ribbons, D.W. Monoterpene dissimilation: chemical and genetic models. CRC Crit. Rev. Microbiol., 1971, 1(2), 291-310.
[http://dx.doi.org/10.3109/10408417109104484]
[56]
Stuart, J.J.; Chen, M.S.; Shukle, R.; Harris, M.O. Gall midges (Hessian flies) as plant pathogens. Annu. Rev. Phytopathol., 2012, 50(1), 339-357.
[http://dx.doi.org/10.1146/annurev-phyto-072910-095255] [PMID: 22656645]
[57]
Kao, C.M.; Liu, J.K.; Chen, Y.L.; Chai, C.T.; Chen, S.C. Factors affecting the biodegradation of PCP by Pseudomonas mendocina NSYSU. J. Hazard. Mater., 2005, 124(1-3), 68-73.
[http://dx.doi.org/10.1016/j.jhazmat.2005.03.051] [PMID: 15979238]
[58]
Romanenko, L.A.; Tanaka, N.; Svetashev, V.I.; Mikhailov, V.V. Pseudomonas glareae sp. nov., a marine sediment-derived bacterium with antagonistic activity. Arch. Microbiol., 2015, 197(5), 693-699.
[http://dx.doi.org/10.1007/s00203-015-1103-6] [PMID: 25787010]
[59]
Simon-Colin, C.; Alain, K.; Colin, S.; Cozien, J.; Costa, B.; Guezennec, J.G.; Raguénès, G.H.C. A novel mcl PHA-producing bacterium, Pseudomonas guezennei sp. nov., isolated from a ‘kopara’ mat located in Rangiroa, an atoll of French Polynesia. J. Appl. Microbiol., 2008, 104(2), 581-586.
[PMID: 17927760]
[60]
Archana, S.; Surendran, A.; Thatheyus, A.J. Biodegradation of methyl parathion using Pseudomonas stutzeri (MTCC 2643). J. Biotechnol. Biomed. Sci., 2020, 2(2), 19-33.
[http://dx.doi.org/10.14302/issn.2576-6694.jbbs-20-3282]
[61]
Tao, Y.; Zhou, Y.; He, X.; Hu, X.; Li, D. Pseudomonas chengduensis sp. nov., isolated from landfill leachate. Int. J. Syst. Evol. Microbiol., 2014, 64(Pt 1), 95-100.
[http://dx.doi.org/10.1099/ijs.0.050294-0] [PMID: 24021726]
[62]
Manickam, N.; Ghosh, A.; Jain, R.K.; Mayilraj, S. Description of a novel indole-oxidizing bacterium Pseudomonas indoloxydans sp. nov., isolated from a pesticide-contaminated site. Syst. Appl. Microbiol., 2008, 31(2), 101-107.
[http://dx.doi.org/10.1016/j.syapm.2008.02.002] [PMID: 18406094]

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