1887

Abstract

causes fatal infections in immunocompromised individuals and patients with pulmonary disorders.

Agricultural ecosystems are the vast reservoirs of this dreaded pathogen. However, there are limited attempts to analyse the pathogenicity of strains associated with edible plants.

This study aims to (i) elucidate the virulence attributes of strains isolated from the rhizosphere and endophytic niches of cucumber, tomato, eggplant and chili;and (ii) compare these phenotypes with that of previously characterized clinical isolates.

Crystal-violet microtitre assay, swarm plate experiment, gravimetric quantification and sheep blood lysis were performed to estimate the biofilm formation, swarming motility, rhamnolipid production and haemolytic activity, respectively, of strains. In addition, their pathogenicity was also assessed based on their ability to antagonize plant pathogens ( and ) and kill a select nematode ().

Nearly 80 % of the plant-associated strains produced rhamnolipid and exhibited at least one type of lytic activity (haemolysis, proteolysis and lipolysis). Almost 50 % of these strains formed significant levels of biofilm and exhibited swarming motility. The agricultural strains showed significantly higher and lower virulence against the bacterial and fungal pathogens, respectively, compared to the clinical strains. In a maximum of 40 and 100% mortality were induced by the agricultural and clinical strains, respectively.

This investigation shows that in edible plants isolated directly from the farm express virulence and pathogenicity. Furthermore, clinical and agricultural strains antagonized the tested fungal phytopathogens, and . Thus, we recommend using these fungi as simple eukaryotic model systems to test pathogenicity.

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2022-08-10
2024-04-25
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References

  1. Reynolds HY, Levine AS, Wood AE, Zierdt CH, Dale DC et al. Pseudomonas aeruginosa infections: Persisting problems and current research to find new therapies. Ann Intern Med 1975; 82:819–831 [View Article] [PubMed]
    [Google Scholar]
  2. von Graevenitz A. The role of opportunistic bacteria in human disease. Annu Rev Microbiol 1977; 31:447–471 [View Article] [PubMed]
    [Google Scholar]
  3. Rosenthal VD, Bat-Erdene I, Gupta D, Belkebir S, Rajhans P et al. International Nosocomial Infection Control Consortium (INICC) report, data summary of 45 countries for 2012-2017: Device-associated module. Am J Infect Control 2020; 48:423–432 [View Article] [PubMed]
    [Google Scholar]
  4. Radford R, Brahma A, Armstrong M, Tullo AB. Severe sclerokeratitis due to Pseudomonas aeruginosa in noncontact-lens wearers. Eye (Lond) 2000; 14:3–7 [View Article] [PubMed]
    [Google Scholar]
  5. Tate D, Mawer S, Newton A. Outbreak of Pseudomonas aeruginosa folliculitis associated with a swimming pool inflatable. Epidemiol Infect 2003; 130:187–192 [View Article] [PubMed]
    [Google Scholar]
  6. Doustdar F, Karimi F, Abedinyfar Z, Amoli FA, Goudarzi H. Genetic features of Pseudomonas aeruginosa isolates associated with eye infections referred to Farabi Hospital, Tehran, Iran. Int Ophthalmol 2019; 39:1581–1587 [View Article] [PubMed]
    [Google Scholar]
  7. Antibiotic resistance threats in the United States U.S. Department of Health and Human Services Centers for Disease Control and Prevention; 2019 https://www.cdc.gov/drugresistance/biggest-threats.html accessed 22 October 2021
  8. Talebi Bezmin Abadi A, Rizvanov AA, Haertlé T, Blatt NL. World Health Organization report: current crisis of antibiotic resistance. BioNanoSci 2019; 9:778–788 [View Article]
    [Google Scholar]
  9. Clara F. A new bacterial leaf disease of tobacco in the Philippines. Phytopathol 1930; 20:691–706
    [Google Scholar]
  10. Elrod RP, Braun AC. Pseudomonas aeruginosa: its rôle as a plant pathogen. J Bacteriol 1942; 44:633–645 [View Article] [PubMed]
    [Google Scholar]
  11. Ali Siddiqui I, Ehteshamul-Haque S. Suppression of the root rot–root knot disease complex by Pseudomonas aeruginosa in tomato: The influence of inoculum density, nematode populations, moisture and other plant-associated bacteria. Plant Soil 2001; 237:81–89 [View Article]
    [Google Scholar]
  12. Adesemoye AO, Ugoji EO. Evaluating Pseudomonas aeruginosa as plant growth-promoting rhizobacteria in West Africa. Arch Phytopathol Pflanzenschutz 2009; 42:188–200 [View Article]
    [Google Scholar]
  13. Mondal KK, Mani C, Singh J, Dave SR, Tipre DR et al. Fruit rot of tinda caused by Pseudomonas aeruginosa-a new report from India. Plant Dis 2012; 96:141 [View Article]
    [Google Scholar]
  14. Gao J, Wang Y, Wang CW, Lu BH. First report of bacterial root rot of ginseng caused by Pseudomonas aeruginosa in China. Plant Dis 2014; 98:1577 [View Article]
    [Google Scholar]
  15. Yasmin S, Hafeez FY, Rasul G. Evaluation of Pseudomonas aeruginosa Z5 for biocontrol of cotton seedling disease caused by Fusarium oxysporum. Biocontrol Sci Technol 2014; 24:1227–1242 [View Article]
    [Google Scholar]
  16. Radhapriya P, Ramachandran A, Anandham R, Mahalingam S. Pseudomonas aeruginosa RRALC3 enhances the biomass, nutrient and carbon contents of Pongamia pinnata seedlings in degraded forest soil. PLoS ONE 2015; 10:e0139881 [View Article]
    [Google Scholar]
  17. Arif MS, Riaz M, Shahzad SM, Yasmeen T, Akhtar MJ et al. Associative interplay of plant growth promoting rhizobacteria (Pseudomonas aeruginosa QS40) with nitrogen fertilizers improves sunflower (Helianthus annuus L.) productivity and fertility of aridisol. Applied Soil Ecology 2016; 108:238–247 [View Article]
    [Google Scholar]
  18. Durairaj K, Velmurugan P, Park J-H, Chang W-S, Park Y-J et al. Potential for plant biocontrol activity of isolated Pseudomonas aeruginosa and Bacillus stratosphericus strains against bacterial pathogens acting through both induced plant resistance and direct antagonism. FEMS Microbiol Lett 2017; 364:fnx225 [View Article]
    [Google Scholar]
  19. Tiwari P, Singh JS. A plant growth promoting rhizospheric Pseudomonas aeruginosa strain inhibits seed germination in Triticum aestivum (L) and Zea mays (L). Microbiol Res (Pavia) 2017; 8:7233 [View Article]
    [Google Scholar]
  20. Gupta V, Buch A. Pseudomonas aeruginosa predominates as multifaceted rhizospheric bacteria with combined abilities of P-solubilization and biocontrol. J Pure Appl Microbiol 2019; 13:319–328 [View Article]
    [Google Scholar]
  21. Chandra H, Kumari P, Bisht R, Prasad R, Yadav S. Plant growth promoting Pseudomonas aeruginosa from Valeriana wallichii displays antagonistic potential against three phytopathogenic fungi. Mol Biol Rep 2020; 47:6015–6026 [View Article] [PubMed]
    [Google Scholar]
  22. Green SK, Schroth MN, Cho JJ, Kominos SK, Vitanza-jack VB. Agricultural plants and soil as a reservoir for Pseudomonas aeruginosa. Appl Microbiol 1974; 28:987–991 [View Article] [PubMed]
    [Google Scholar]
  23. Cho JJ. Ornamental plants as carriers of Pseudomonas aeruginosa. Phytopathology 1975; 65:425 [View Article]
    [Google Scholar]
  24. Kominos SD, Copeland CE, Grosiak B, Postic B. Introduction of Pseudomonas aeruginosa into a hospital via vegetables. Appl Microbiol 1972; 24:567–570 [View Article] [PubMed]
    [Google Scholar]
  25. Wright C, Kominos SD, Yee RB. Enterobacteriaceae and Pseudomonas aeruginosa recovered from vegetable salads. Appl Environ Microbiol 1976; 31:453–454 [View Article] [PubMed]
    [Google Scholar]
  26. Correa CM, Tibana A, Gontijo Filho PP. Vegetables as a source of infection with Pseudomonas aeruginosa in a University and Oncology Hospital of Rio de Janeiro. J Hosp Infect 1991; 18:301–306 [View Article]
    [Google Scholar]
  27. Viswanathan P, Kaur R. Prevalence and growth of pathogens on salad vegetables, fruits and sprouts. Int J Hyg Environ Health 2001; 203:205–213 [View Article]
    [Google Scholar]
  28. Curran B, Morgan JAW, Honeybourne D, Dowson CG. Commercial mushrooms and bean sprouts are a source of Pseudomonas aeruginosa. J Clin Microbiol 2005; 43:5830–5831 [View Article]
    [Google Scholar]
  29. Allydice-Francis K, Brown PD. Diversity of antimicrobial resistance and virulence determinants in Pseudomonas aeruginosa associated with fresh vegetables. Int J Microbiol 2012; 2012:426241 [View Article]
    [Google Scholar]
  30. Ambreetha S, Marimuthu P, Mathee K, Balachandar D. Rhizospheric and endophytic Pseudomonas aeruginosa in edible vegetable plants share molecular and metabolic traits with clinical isolates. J Appl Microbiol 2021 [View Article]
    [Google Scholar]
  31. Mathee K. Forensic investigation into the origin of Pseudomonas aeruginosa PA14 - old but not lost. J Med Microbiol 2018; 67:1019–1021 [View Article] [PubMed]
    [Google Scholar]
  32. Schroth M, Cho J, Green S, Kominos S. Epidemiology of Pseudomonas aeruginosa in agricultural areas. In Young V. eds Pseudomonas Aeruginosa: Ecological Aspects and Patient Colonization New York: Raven Press; 1977 pp 1–29
    [Google Scholar]
  33. Schroth MN, Cho JJ, Green SK, Kominos SD. Epidemiology of Pseudomonas aeruginosa in agricultural areas. J Med Microbiol 2018; 67:1191–1201 [View Article] [PubMed]
    [Google Scholar]
  34. Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG et al. Common virulence factors for bacterial pathogenicity in plants and animals. Science 1995; 268:1899–1902 [View Article] [PubMed]
    [Google Scholar]
  35. Kumar A, Munder A, Aravind R, Eapen SJ, Tümmler B et al. Friend or foe: genetic and functional characterization of plant endophytic Pseudomonas aeruginosa. Environ Microbiol 2013; 15:764–779 [View Article] [PubMed]
    [Google Scholar]
  36. Balasubramanian D, Schneper L, Kumari H, Mathee K. A dynamic and intricate regulatory network determines Pseudomonas aeruginosa virulence. Nucleic Acids Res 2013; 41:1–20 [View Article] [PubMed]
    [Google Scholar]
  37. Moradali MF, Ghods S, Rehm BHA. Pseudomonas aeruginosa lifestyle: a paradigm for adaptation, survival, and persistence. Front Cell Infect Microbiol 2017; 7:1–29 [View Article] [PubMed]
    [Google Scholar]
  38. Holloway BW. Genetic recombination in Pseudomonas aeruginosa. J Gen Microbiol 1955; 13:572–581 [View Article] [PubMed]
    [Google Scholar]
  39. HAYNES WC. Pseudomonas aeruginosa--its characterization and identification. J Gen Microbiol 1951; 5:939–950 [View Article] [PubMed]
    [Google Scholar]
  40. Picard B, Denamur E, Barakat A, Elion J, Goullet P. Genetic heterogeneity of Pseudomonas aeruginosa clinical isolates revealed by esterase electrophoretic polymorphism and restriction fragment length polymorphism of the ribosomal RNA gene region. J Med Microbiol 1994; 40:313–322 [View Article] [PubMed]
    [Google Scholar]
  41. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974; 77:71–94 [View Article] [PubMed]
    [Google Scholar]
  42. O’Toole GA. Microtiter dish biofilm formation assay. J Vis Exp 20112437 [View Article] [PubMed]
    [Google Scholar]
  43. Tremblay J, Déziel E. Improving the reproducibility of Pseudomonas aeruginosa swarming motility assays. J Basic Microbiol 2008; 48:509–515 [View Article] [PubMed]
    [Google Scholar]
  44. Siegmund I, Wagner F. New method for detecting rhamnolipids excreted by Pseudomonas species during growth on mineral agar. Biotechnol Tech 1991; 5:265–268 [View Article]
    [Google Scholar]
  45. Zhang Y, Miller RM. Enhanced octadecane dispersion and biodegradation by a Pseudomonas rhamnolipid surfactant (biosurfactant). Appl Environ Microbiol 1992; 58:3276–3282 [View Article] [PubMed]
    [Google Scholar]
  46. Gunther NW 4th, Nuñez A, Fett W, Solaiman DKY. Production of rhamnolipids by Pseudomonas chlororaphis, a nonpathogenic bacterium. Appl Environ Microbiol 2005; 71:2288–2293 [View Article] [PubMed]
    [Google Scholar]
  47. Williams REO, Harper GJ. Staphylococcal haemolysins on sheep-blood agar with evidence for a fourth haemolysin. J Pathol Bacteriol 1947; 59:69–78 [View Article] [PubMed]
    [Google Scholar]
  48. Atlas RM. Handbook of Microbiological Lawrence Parks, London: CRC press; 1993
    [Google Scholar]
  49. Georgescu M, Gheorghe I, Curutiu C, Lazar V, Bleotu C et al. Virulence and resistance features of Pseudomonas aeruginosa strains isolated from chronic leg ulcers. BMC Infect Dis 2016; 16 Suppl 1:1–28 [View Article] [PubMed]
    [Google Scholar]
  50. Ali MA, Ren H, Ahmed T, Luo J, An Q et al. Antifungal effects of rhizospheric Bacillus species against bayberry twig blight pathogen Pestalotiopsis versicolor. Agronomy 2020; 10:1811 [View Article]
    [Google Scholar]
  51. Riungu GM, Muthomi JW, Narla RD, Wagacha JM, Gathumbi JK. Management of Fusarium head blight of wheat and deoxynivalenol accumulation using antagonistic microorganisms. Plant Pathol J 2008; 7:13–19 [View Article]
    [Google Scholar]
  52. Lertcanawanichakul M, Sawangnop S. A comparison of two methods used for measuring the antagonistic activity of Bacillus species. Walailak J Sci & Technol 2011; 5:161–171
    [Google Scholar]
  53. Lo Giudice A, Brilli M, Bruni V, De Domenico M, Fani R et al. Bacterium-bacterium inhibitory interactions among psychrotrophic bacteria isolated from Antarctic seawater (Terra Nova Bay, Ross Sea). FEMS Microbiol Ecol 2007; 60:383–396 [View Article] [PubMed]
    [Google Scholar]
  54. Tan M-W, Mahajan-Miklos S, Ausubel FM. Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci U S A 1999; 96:715–720 [View Article] [PubMed]
    [Google Scholar]
  55. Adonizio A, Kong K-F, Mathee K. Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa by South Florida plant extracts. Antimicrob Agents Chemother 2008; 52:198–203 [View Article] [PubMed]
    [Google Scholar]
  56. Römling U, Fiedler B, Bosshammer J, Grothues D, Greipel J et al. Epidemiology of chronic Pseudomonas aeruginosa infections in cystic fibrosis. J Infect Dis 1994; 170:1616–1621 [View Article] [PubMed]
    [Google Scholar]
  57. Bjarnsholt T, Jensen , Fiandaca MJ, Pedersen J, Hansen CR et al. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr Pulmonol 2009; 44:547–558 [View Article] [PubMed]
    [Google Scholar]
  58. Overhage J, Bains M, Brazas MD, Hancock REW. Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol 2008; 190:2671–2679 [View Article] [PubMed]
    [Google Scholar]
  59. Coleman SR, Pletzer D, Hancock REW. Contribution of swarming motility to dissemination in a Pseudomonas aeruginosa murine skin abscess infection model. J Infect Dis 2021; 224:726–733 [View Article] [PubMed]
    [Google Scholar]
  60. Coleman SR, Blimkie T, Falsafi R, Hancock REW. Multidrug adaptive resistance of Pseudomonas aeruginosa swarming cells. Antimicrob Agents Chemother 2020; 64:e01999–01919 [View Article] [PubMed]
    [Google Scholar]
  61. McClure CD, Schiller NL. Effects of Pseudomonas aeruginosa rhamnolipids on human monocyte-derived macrophages. J Leukoc Biol 1992; 51:97–102 [View Article] [PubMed]
    [Google Scholar]
  62. McClure CD, Schiller NL. Inhibition of macrophage phagocytosis by Pseudomonas aeruginosa rhamnolipids in vitro and in vivo. Curr Microbiol 1996; 33:109–117 [View Article] [PubMed]
    [Google Scholar]
  63. Zulianello L, Canard C, Köhler T, Caille D, Lacroix J-S et al. Rhamnolipids are virulence factors that promote early infiltration of primary human airway epithelia by Pseudomonas aeruginosa. Infect Immun 2006; 74:3134–3147 [View Article] [PubMed]
    [Google Scholar]
  64. Kim SK, Kim YC, Lee S, Kim JC, Yun MY et al. Insecticidal activity of rhamnolipid isolated from Pseudomonas sp. EP-3 against green peach aphid (Myzus persicae). J Agric Food Chem 2011; 59:934–938 [View Article] [PubMed]
    [Google Scholar]
  65. Yan F, Xu S, Guo J, Chen Q, Meng Q et al. Biocontrol of post-harvest Alternaria alternata decay of cherry tomatoes with rhamnolipids and possible mechanisms of action. J Sci Food Agric 2015; 95:1469–1474 [View Article] [PubMed]
    [Google Scholar]
  66. Sancheti A, Ju L-K. Eco-friendly rhamnolipid based fungicides for protection of soybeans from Phytophthora sojae. Pest Manag Sci 2019; 75:3031–3038 [View Article] [PubMed]
    [Google Scholar]
  67. Monnier N, Furlan A, Botcazon C, Dahi A, Mongelard G et al. Rhamnolipids from Pseudomonas aeruginosa are elicitors triggering Brassica napus protection against Botrytis cinerea without physiological disorders. Front Plant Sci 2018; 9: [View Article]
    [Google Scholar]
  68. Ostroff RM, Wretlind B, Vasil ML. Mutations in the hemolytic-phospholipase C operon result in decreased virulence of Pseudomonas aeruginosa PAO1 grown under phosphate-limiting conditions. Infect Immun 1989; 57:1369–1373 [View Article] [PubMed]
    [Google Scholar]
  69. Wargo MJ, Gross MJ, Rajamani S, Allard JL, Lundblad LKA et al. Hemolytic phospholipase C inhibition protects lung function during Pseudomonas aeruginosa infection. Am J Respir Crit Care Med 2011; 184:345–354 [View Article] [PubMed]
    [Google Scholar]
  70. Sakthivel N, Gnanamanickam S. Toxicity of Pseudomonas fluorescens towards rice sheath-rot pathogen Acrocylindrium oryzae saw. Curr Sci 1986; 55: [View Article]
    [Google Scholar]
  71. Mahajan-Miklos S, Tan M-W, Rahme LG, Ausubel FM. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 1999; 96:47–56 [View Article] [PubMed]
    [Google Scholar]
  72. Nithya A, Babu S. Prevalence of plant beneficial and human pathogenic bacteria isolated from salad vegetables in India. BMC Microbiol 2017; 17:64 [View Article] [PubMed]
    [Google Scholar]
  73. Lebeda A, Kudela V, Jedlickova Z. Pathogenicity of Pseudomonas aeruginosa for plants and animals. Acta Phytopathol Acad Sci Hung 1984; 19:271–284
    [Google Scholar]
  74. Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ et al. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 2000; 407:762–764 [View Article] [PubMed]
    [Google Scholar]
  75. Nixon GM, Armstrong DS, Carzino R, Carlin JB, Olinsky A et al. Clinical outcome after early Pseudomonas aeruginosa infection in cystic fibrosis. J Pediatr 2001; 138:699–704 [View Article] [PubMed]
    [Google Scholar]
  76. Ali SkZ, Sandhya V, Grover M, Kishore N, Rao LV et al. Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biol Fertil Soils 2009; 46:45–55 [View Article]
    [Google Scholar]
  77. Tank N, Saraf M. Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J Plant Interact 2010; 5:51–58 [View Article]
    [Google Scholar]
  78. Sarma RK, Saikia R. Alleviation of drought stress in mung bean by strain Pseudomonas aeruginosa GGRJ21. Plant Soil 2013; 377:111–126 [View Article]
    [Google Scholar]
  79. Kumawat KC, Sharma P, Sirari A, Singh I, Gill BS et al. Synergism of Pseudomonas aeruginosa (LSE-2) nodule endophyte with Bradyrhizobium sp. (LSBR-3) for improving plant growth, nutrient acquisition and soil health in soybean. World J Microbiol Biotechnol 2019; 35:47 [View Article] [PubMed]
    [Google Scholar]
  80. Tremblay J, Déziel E. Gene expression in Pseudomonas aeruginosa swarming motility. BMC Genomics 2010; 11:587 [View Article] [PubMed]
    [Google Scholar]
  81. Goebel W, Chakraborty T, Kreft J. Bacterial hemolysins as virulence factors. Anton Leeuw Int J G 1988; 54:453–463 [View Article] [PubMed]
    [Google Scholar]
  82. Woods PW, Haynes ZM, Mina EG, Marques CNH. Maintenance of S. aureus in co-culture with P. aeruginosa while growing as biofilms. Front Microbiol 2019; 9: [View Article]
    [Google Scholar]
  83. Darby C, Cosma CL, Thomas JH, Manoil C. Lethal paralysis of Caenorhabditis elegans by Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 1999; 96:15202–15207 [View Article] [PubMed]
    [Google Scholar]
  84. Heck LW, Morihara K, McRae WB, Miller EJ. Specific cleavage of human type III and IV collagens by Pseudomonas aeruginosa elastase. Infect Immun 1986; 51:115–118 [View Article] [PubMed]
    [Google Scholar]
  85. Parmely M, Gale A, Clabaugh M, Horvat R, Zhou WW. Proteolytic inactivation of cytokines by Pseudomonas aeruginosa. Infect Immun 1990; 58:3009–3014 [View Article] [PubMed]
    [Google Scholar]
  86. König B, Jaeger KE, Sage AE, Vasil ML, König W. Role of Pseudomonas aeruginosa lipase in inflammatory mediator release from human inflammatory effector cells (platelets, granulocytes, and monocytes. Infect Immun 1996; 64:3252–3258 [View Article] [PubMed]
    [Google Scholar]
  87. Barker AP, Vasil AI, Filloux A, Ball G, Wilderman PJ et al. A novel extracellular phospholipase C of Pseudomonas aeruginosa is required for phospholipid chemotaxis. Mol Microbiol 2004; 53:1089–1098 [View Article] [PubMed]
    [Google Scholar]
  88. Pinna A, Usai D, Sechi LA, Molicotti P, Zanetti S et al. Detection of virulence factors in Pseudomonas aeruginosa strains isolated from contact lens-associated corneal ulcers. Cornea 2008; 27:320–326 [View Article] [PubMed]
    [Google Scholar]
  89. Kim BS, Lee JY, Hwang BK. In vivo control and in vitro antifungal activity of rhamnolipid B, a glycolipid antibiotic, against Phytophthora capsici and Colletotrichum orbiculare. Pest Manag Sci 2000; 56:1029–1035 [View Article]
    [Google Scholar]
  90. Grosso-Becerra M-V, González-Valdez A, Granados-Martínez M-J, Morales E, Servín-González L et al. Pseudomonas aeruginosa ATCC 9027 is a non-virulent strain suitable for mono-rhamnolipids production. Appl Microbiol Biotechnol 2016; 100:9995–10004 [View Article] [PubMed]
    [Google Scholar]
  91. Parmeter JR Rhizoctonia Solani, Biology and Pathology Univ of California Press; 1970
    [Google Scholar]
  92. Martin FN, Loper JE. Soilborne plant diseases caused by Pythium spp.: Ecology, epidemiology, and prospects for biological control. Crit Rev Plant Sci 2010; 18:111–181 [View Article]
    [Google Scholar]
  93. Michielse CB, Rep M. Pathogen profile update: Fusarium oxysporum. Mol Plant Pathol 2009; 10:311–324 [View Article] [PubMed]
    [Google Scholar]
  94. Lodhi AM, Khanzada MA, Shahzad S, Ghaffar A, Lévesque C. Prevalence of Pythium aphanidermatum in agro-ecosystem of Sindh province of Pakistan. Pak J Bot 2013; 45:635–642
    [Google Scholar]
  95. Swings J, Van Den Mooter M, Vauterin L, Hoste B, Gillis M et al. Reclassification of the causal agents of bacterial blight (Xanthomonas campestris pv. oryzae) and bacterial leaf streak (Xanthomonas campestris pv. oryzicola) of rice as pathovars of Xanthomonas oryzae (ex Ishiyama 1922) sp. nov., nom. rev. Int J Syst Bacteriol 1990; 40:309–311 [View Article]
    [Google Scholar]
  96. Sudhakar T, Karpagam S, Premkumar J. Biosynthesis, antibacterial activity of pyocyanin pigment produced by Pseudomonas aeruginosa SU1. J Chem Pharm Res 2015; 7:921–924
    [Google Scholar]
  97. Mahmoud SY, Ziedan E-S, Farrag ES, Kalafalla RS, Ali AM. Antifungal activity of pyocyanin produced by Pseudomonas aeruginosa against Fusarium oxysporum schlech a root-rot phytopathogenic fungi. Int J PharmTech Res 2016; 9:43–50
    [Google Scholar]
  98. Chen J, Wu Q, Hua Y, Chen J, Zhang H et al. Potential applications of biosurfactant rhamnolipids in agriculture and biomedicine. Appl Microbiol Biotechnol 2017; 101:8309–8319 [View Article] [PubMed]
    [Google Scholar]
  99. DeBritto S, Gajbar TD, Satapute P, Sundaram L, Lakshmikantha RY et al. Isolation and characterization of nutrient dependent pyocyanin from Pseudomonas aeruginosa and its dye and agrochemical properties. Sci Rep 2020; 10:1542 [View Article] [PubMed]
    [Google Scholar]
  100. Kirienko NV, Cezairliyan BO, Ausubel FM. Pseudomonas aeruginosa PA14 pathogenesis in Caenorhabditis elegans. In Filloux A, Ramos J-L. eds Pseudomonas Methods and Protocols New York, NY: Springer New York; 2014 pp 653–669
    [Google Scholar]
  101. Andrew PA, Nicholas WL. Effect of bacteria on dispersal of Caenorhabditis elegans (Rhabditidae). Nematol 1976; 22:451–461 [View Article]
    [Google Scholar]
  102. Feinbaum RL, Urbach JM, Liberati NT, Djonovic S, Adonizio A et al. Genome-wide identification of Pseudomonas aeruginosa virulence-related genes using a Caenorhabditis elegans infection model. PLoS Pathog 2012; 8:e1002813 [View Article] [PubMed]
    [Google Scholar]
  103. Jaffar-Bandjee MC, Lazdunski A, Bally M, Carrère J, Chazalette JP et al. Production of elastase, exotoxin A, and alkaline protease in sputa during pulmonary exacerbation of cystic fibrosis in patients chronically infected by Pseudomonas aeruginosa. J Clin Microbiol 1995; 33:924–929 [View Article] [PubMed]
    [Google Scholar]
  104. Alonso A, Rojo F, Martínez JL. Environmental and clinical isolates of Pseudomonas aeruginosa show pathogenic and biodegradative properties irrespective of their origin. Environ Microbiol 1999; 1:421–430 [View Article] [PubMed]
    [Google Scholar]
  105. Vives-Flórez M, Garnica D. Comparison of virulence between clinical and environmental Pseudomonas aeruginosa isolates. Int Microbiol 2006; 9:247–252 [PubMed]
    [Google Scholar]
  106. Hall S, McDermott C, Anoopkumar-Dukie S, McFarland AJ, Forbes A et al. Cellular effects of pyocyanin, a secreted virulence factor of Pseudomonas aeruginosa. Toxins (Basel) 2016; 8:236–244 [View Article]
    [Google Scholar]
  107. Ruiz-Roldán L, Rojo-Bezares B, de Toro M, López M, Toledano P et al. Antimicrobial resistance and virulence of Pseudomonas spp. among healthy animals: concern about exolysin ExlA detection. Sci Rep 2020; 10:11667 [View Article]
    [Google Scholar]
  108. Wheater DWF, Mara DD, Jawad L, Oragui J. Pseudomonas aeruginosa and Escherichia coli in sewage and fresh water. Water Res 1980; 14:713–721 [View Article]
    [Google Scholar]
  109. Mavrodi OV, Mavrodi DV, Parejko JA, Thomashow LS, Weller DM. Irrigation differentially impacts populations of indigenous antibiotic-producing Pseudomonas spp. in the rhizosphere of wheat. Appl Environ Microbiol 2012; 78:3214–3220 [View Article]
    [Google Scholar]
  110. Slekovec C, Plantin J, Cholley P, Thouverez M, Talon D et al. Tracking down antibiotic-resistant Pseudomonas aeruginosa isolates in a wastewater network. PLoS One 2012; 7:e49300 [View Article]
    [Google Scholar]
  111. Orlofsky E, Bernstein N, Sacks M, Vonshak A, Benami M et al. Comparable levels of microbial contamination in soil and on tomato crops after drip irrigation with treated wastewater or potable water. Agric Ecosyst Environ 2016; 215:140–150 [View Article]
    [Google Scholar]
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