Molecular and Phenotypic Investigation on Antibacterial Activities of Limonene Isomers and Its Oxidation Derivative against Xanthomonas oryzae pv. oryzae
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Xanthomonas oryzae pv. oryzae (Xoo) causes a devastating bacterial leaf blight in rice. Here, the antimicrobial effects of D-limonene, L-limonene, and its oxidative derivative carveol against Xoo were investigated. We revealed that carveol treatment at ≥ 0.1 mM in liquid culture resulted in significant decrease in Xoo growth rate (> 40%) in a concentration-dependent manner, and over 1 mM, no growth was observed. The treatment with D-limonene and L-limonene also inhibited the Xoo growth but to a lesser extent compared to carveol. These results were further elaborated with the assays of motility, biofilm formation and xanthomonadin production. The carveol treatment over 1 mM caused no motilities, basal level of biofilm formation (< 10%), and significantly reduced xanthomonadin production. The biofilm formation after the treatment with two limonene isomers was decreased in a concentration-dependent manner, but the degree of the effect was not comparable to carveol. In addition, there was negligible effect on the xanthomonadin production mediated by the treatment of two limonene isomers. Field emission-scanning electron microscope (FE-SEM) unveiled that all three compounds used in this study cause severe ultrastructural morphological changes in Xoo cells, showing shrinking, shriveling, and holes on their surface. Moreover, quantitative real-time PCR revealed that carveol and D-limonene treatment significantly down-regulated the expression levels of genes involved in virulence and biofilm formation of Xoo, but not with L-limonene. Together, we suggest that limonenes and carveol will be the candidates of interest in the development of biological pesticides.
Abstract
Xanthomonas oryzae pv. oryzae (Xoo) causes a devastating bacterial leaf blight in rice. Here, the antimicrobial effects of D-limonene, L-limonene, and its oxidative derivative carveol against Xoo were investigated. We revealed that carveol treatment at ≥ 0.1 mM in liquid culture resulted in significant decrease in Xoo growth rate (> 40%) in a concentration-dependent manner, and over 1 mM, no growth was observed. The treatment with D-limonene and L-limonene also inhibited the Xoo growth but to a lesser extent compared to carveol. These results were further elaborated with the assays of motility, biofilm formation and xanthomonadin production. The carveol treatment over 1 mM caused no motilities, basal level of biofilm formation (< 10%), and significantly reduced xanthomonadin production. The biofilm formation after the treatment with two limonene isomers was decreased in a concentration-dependent manner, but the degree of the effect was not comparable to carveol. In addition, there was negligible effect on the xanthomonadin production mediated by the treatment of two limonene isomers. Field emission-scanning electron microscope (FE-SEM) unveiled that all three compounds used in this study cause severe ultrastructural morphological changes in Xoo cells, showing shrinking, shriveling, and holes on their surface. Moreover, quantitative real-time PCR revealed that carveol and D-limonene treatment significantly down-regulated the expression levels of genes involved in virulence and biofilm formation of Xoo, but not with L-limonene. Together, we suggest that limonenes and carveol will be the candidates of interest in the development of biological pesticides.
참고문헌 (46)
- NIÑO-LIU DO, "Xanthomonas oryzae pathovars : model pathogens of a model crop", Mol. Plant Pathol, 7, pp.303~324 (2006)
- Mansfield J, "Top 10 plant pathogenic bacteria in molecular plant pathology", Mol. Plant Pathol, 13, pp.614~629 (2012)
- Büttner D, "Regulation and secretion of Xanthomonas virulence factors", FEMS Microbiol. Rev, 34, pp.107~133 (2010)
- Branda SS, "Biofilms : the matrix revisited", Trends Microbiol, 13, pp.20~26 (2005)
- Sutherland IW, "Biofilm exopolysaccharides : a strong and sticky framework", Microbiology, 147, pp.3~9 (2001)
- Ramey BE, "Biofilm formation in plant–microbe associations", Curr. Opin. Microbiol, 7, pp.602~609 (2004)
- Lohse MB, "Development and regulation of single-and multi-species Candida albicans biofilms", Nat. Rev. Microbiol, 16, pp.19~31 (2018)
- Tayi L, "Action of multiple cell wall–degrading enzymes is required for elicitation of innate immune responses during Xanthomonas oryzae pv. oryzae infection in rice", Mol. Plant-Microbe Interact, 29, pp.599~608 (2016)
- Jansson P-e, "Structure of the extracellular polysaccharide from Xanthomonas campestris", Carbohydr. Res, 45, pp.275~282 (1975)
- Köplin R, "Genetics of xanthan production in Xanthomonas campestris : the xanA and xanB genes are involved in UDP-glucose and GDP-mannose biosynthesis", J. Bacteriol, 174, pp.191~199 (1992)
- Büttner D, "Getting across-bacterial type III effector proteins on their way to the plant cell", EMBO J, 21, pp.5313~5322 (2002)
- Jones JD, "The plant immune system", Nature, 444, pp.323~329 (2006)
- LaSarre B, "Exploiting quorum sensing to confuse bacterial pathogens", Microbiol. Mol. Biol. Rev, 77, pp.73~111 (2013)
- Tomlin KL, "Quorum-sensing mutations affect attachment and stability of Burkholderia cenocepacia biofilms", Appl. Environ. Microbiol, 71, pp.5208~5218 (2005)
- Barel V, "Virulence and in planta movement of X anthomonas hortorum pv. pelargonii are affected by the diffusible signal factor (DSF)‐dependent quorum sensing system", Mol. Plant Pathol, 16, pp.710~723 (2015)
- Sun J, "D-Limonene : safety and clinical applications", Altern. Med. Rev, 12, pp.259~264 (2007)
- Lee GW, "Direct suppression of a rice bacterial blight (Xanthomonas oryzae pv. oryzae) by monoterpene (S)-limonene", Protoplasma, 253, pp.683~690 (2016)
- Guimarães AC, "Antibacterial activity of terpenes and terpenoids present in essential oils", Molecules, 24, pp.2471~ (2019)
- Dabbah R, "Antimicrobial action of some citrus fruit oils on selected food-borne bacteria", Appl. Microbiol, 19, pp.27~31 (1970)
- Brennan TC, "Physiological and transcriptional responses of Saccharomyces cerevisiae to d-limonene show changes to the cell wall but not to the plasma membrane", Appl. Environ. Microbiol, 79, pp.3590~3600 (2013)
- Sahu SK, "Niclosamide blocks rice leaf blight by inhibiting biofilm formation of Xanthomonas oryzae", Front. Plant Sci, 9, pp.408~ (2018)
- Singh A, "Thyme oil reduces biofilm formation and impairs virulence of Xanthomonas oryzae", Front. Microbiol, 8, pp.1074~ (2017)
- Livak KJ, "Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method", Methods, 25, pp.402~408 (2001)
- Ncube N, "Assessment techniques of antimicrobial properties of natural compounds of plant origin : current methods and future trends", Afr. J. Biotechnol, 7, pp.1797~1806 (2008)
- Silva LN, "Plant natural products targeting bacterial virulence factors", Chem. Rev, 116, pp.9162~9236 (2016)
- Bjarnsholt T, "Applying insights from biofilm biology to drug development-can a new approach be developed?", Nat. Rev. Drug Dis, 12, pp.791~808 (2013)
- Tharmalingam N, "Inhibitory effect of piperine on Helicobacter pylori growth and adhesion to gastric adenocarcinoma cells", Infect. Agents Cancer, 9, pp.43~ (2014)
- Dusane DH, "Alkaloids modulate motility, biofilm formation and antibiotic susceptibility of uropathogenic Escherichia coli", PLoS One, 9, pp.e112093~ (2014)
- Liaw SJ, "Modulation of swarming and virulence by fatty acids through the RsbA protein in Proteus mirabilis", Infect. Immunity, 72, pp.6836~6845 (2004)
- Jakobsen TH, "Food as a source for quorum sensing inhibitors : iberin from horseradish revealed as a quorum sensing inhibitor of Pseudomonas aeruginosa", Appl. Environ. Microbiol, 78, pp.2410~2421 (2012)
- Choi SC, "Inhibitory effects of 4-hydroxy-2, 5-dimethyl-3(2H)-furanone(HDMF)on acylhomoserine lactone-mediated virulence factor production and biofilm formation in Pseudomonas aeruginosa PAO1", J. Microbiol, 52, pp.734~742 (2014)
- Jarrell KF, "The surprisingly diverse ways that prokaryotes move", Nat. Rev. Microbiol, 6, pp.466~476 (2008)
- Kearns DB, "A field guide to bacterial swarming motility", Nat. Rev. Microbiol, 8, pp.634~644 (2010)
- O'Toole GA, "Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development", Mol. Microbiol, 30, pp.295~304 (1998)
- De Kerchove AJ, "Calcium and magnesium cations enhance the adhesion of motile and nonmotile Pseudomonas aeruginosa on alginate films", Langmuir, 24, pp.3392~3399 (2008)
- Chen X, "Melatonin treatment inhibits the growth of Xanthomonas oryzae pv. oryzae", Front. Microbiol, 9, pp.2280~ (2018)
- Kerekes EB, "Anti-biofilm forming and anti-quorum sensing activity of selected essential oils and their main components on food-related micro-organisms", J. Appl. Microbiol, 115, pp.933~942 (2013)
- Wilson C, "Quantitative and qualitative assessment methods for biofilm growth: a mini-review", Res. Rev. J. Eng. Technol, 6 (2017)
- He YW, "Chemical structure, biological roles, biosynthesis and regulation of the yellow xanthomonadin pigments in the phytopathogenic genus Xanthomonas", Mol. Plant Microbe Interact, 33, pp.705~714 (2020)
- Poplawsky A, "Biological role of xanthomonadin pigments in Xanthomonas campestris pv. campestris", Appl. Environ. Microbiol, 66, pp.5123~5127 (2000)
- Shi W, "Antimicrobial peptide melittin against Xanthomonas oryzae pv. oryzae, the bacterial leaf blight pathogen in rice", Appl. Microbiol. Biotechnol, 100, pp.5059~5067 (2016)
- Xu Y, "Status of streptomycin resistance development in Xanthomonas oryzae pv. oryzae and Xanthomonas oryzae pv. oryzicola in China and their resistance characters", J. Phytopathol, 158, pp.601~608 (2010)
- Gupta A, "Strategic approach of multifaceted antibacterial mechanism of limonene traced in Escherichia coli", Sci. Rep, 11, pp.13816~ (2021)
- Vojnov AA, "Expression of the gum operon directing xanthan biosynthesis in Xanthomonas campestris and its regulation in planta", Mol. Plant Microbe Interact, 14, pp.768~774 (2001)
- He YW, "Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSFfamily signals in regulation of virulence factor production", BMC Microbiol, 10, pp.187~ (2010)
- Ryan RP, "Communication with a growing family : diffusible signal factor(DSF)signaling in bacteria", Trends Microbiol, 19, pp.145~152 (2011)