Effect of Producing Different Phenazines on Bacterial Fitness and Biological Control in Pseudomonas chlororaphis 30-84 |
Yu, Jun Myoung
(Department of Horticultural Sciences, Texas A&M University)
Wang, Dongping (Department of Plant Pathology and Microbiology, Texas A&M University) Pierson, Leland S. III (Department of Plant Pathology and Microbiology, Texas A&M University) Pierson, Elizabeth A. (Department of Horticultural Sciences, Texas A&M University) |
1 | Weller, D. 1983. Colonization of wheat roots by a fluorescent pseudomonad suppressive to take-all. Phytopathology 73:1548-1553. DOI |
2 | Whitchurch, C. B., Tolker-Nielsen, T., Ragas, P. C. and Mattick, J. S. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295:1487-1487. DOI |
3 | Wilkinson, H., Cook, R. and Alldredge, J. 1985. Relation of inoculum size and concentration to infection of wheat roots by Gaeumannomyces graminis var. tritici. Phytopathology 75: 98-103. DOI |
4 | Wood, D. W., Gong, F., Daykin, M. M., Williams, P. and Pierson, L. S., III. 1997. N-acyl-homoserine lactone-mediated regulation of phenazine gene expression by Pseudomonas aureofaciens 30-84 in the wheat rhizosphere. J. Bacteriol. 179:7663-7670. DOI |
5 | Yu, J. M. 2016. Regulation and ecological roles of phenazine biosynthesis in the biological control strain Pseudomonas chlororaphis 30-84. Ph.D. thesis. Texas A&M University, College Station, TX, USA. |
6 | Yu, J. M., Wang, D., Pierson, L. S., III and Pierson, E. A. 2017. Disruption of MiaA provides insights into the regulation of phenazine biosynthesis under suboptimal growth conditions in Pseudomonas chlororaphis 30-84. Microbiology 163:94-108. DOI |
7 | Mavrodi, D. V., Mavrodi, O. V., Parejko, J. A., Bonsall, R. F., Kwak, Y.-S., Paulitz, T. C., Thomashow, L. S. and Weller, D. M. 2012a. Accumulation of the antibiotic phenazine-1-carboxylic acid in the rhizosphere of dryland cereals. Appl. Environ. Microbiol. 78:804-812. DOI |
8 | Mavrodi, D. V., Peever, T. L., Mavrodi, O. V., Parejko, J. A., Raaijmakers, J. M., Lemanceau, P., Mazurier, S., Heide, L., Blankenfeldt, W. and Weller, D. M. 2010. Diversity and evolution of the phenazine biosynthesis pathway. Appl. Environ. Microbiol. 76:866-879. DOI |
9 | Mavrodi, O. V., Mavrodi, D. V., Parejko, J. A., Thomashow, L. S. and Weller, D. M. 2012b. Irrigation differentially impacts populations of indigenous antibiotic-producing Pseudomonas spp. in the rhizosphere of wheat. Appl. Environ. Microbiol. 78:3214-3220. DOI |
10 | Mazzola, M., Cook, R. J., Thomashow, L. S., Weller, D. M. and Pierson, L. S., III. 1992. Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl. Environ. Microbiol. 58:2616-2624. |
11 | Miller, W. G., Leveau, J. H. and Lindow, S. E. 2000. Improved gfp and inaz broad-host-range promoter-probe vectors. Mol. Plant-Microbe Interact. 13:1243-1250. DOI |
12 | Morales, D. K., Jacobs, N. J., Rajamani, S., Krishnamurthy, M., Cubillos-Ruiz, J. R. and Hogan, D. A. 2010. Antifungal mechanisms by which a novel Pseudomonas aeruginosa phenazine toxin kills candida albicans in biofilms. Mol. Microbiol. 78:1379-1392. DOI |
13 | Mulcahy, H., Charron-Mazenod, L. and Lewenza, S. 2008. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4:e1000213. DOI |
14 | O'Toole, G. A. and Kolter, R. 1998. Initiation of biofilm formation in Pseudomonas fluorescens wcs365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-461. DOI |
15 | Pierson, E. A., Wood, D. W., Cannon, J. A., Blachere, F. M. and Pierson, L. S., III. 1998. Interpopulation signaling via n-acylhomoserine lactones among bacteria in the wheat rhizosphere. Mol. Plant-Microbe Interact. 11:1078-1084. DOI |
16 | Zhou, L., Jiang, H.-X., Sun, S., Yang, D.-D., Jin, K.-M., Zhang, W. and He, Y.-W. 2016. Biotechnological potential of a rhizosphere Pseudomonas aeruginosa strain producing phenazine-1-carboxylic acid and phenazine-1-carboxamide. World J. Micriobiol. Biotech. 32:50. DOI |
17 | Wei, Q. and Ma, L. Z. 2013. Biofilm matrix and its regulation in Pseudomonas aeruginosa. Int. J. Mol. Sci. 14:20983-21005. DOI |
18 | Okshevsky, M. and Meyer, R. L. 2015. The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Crit. Rev. Microbiol. 41:341-352. DOI |
19 | Ownley, B. H., Weller, D. and Thomashow, L. S. 1992. Influence of in situ and in vitro ph on suppression of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens 2-79. Phytopathology 82:178-184. DOI |
20 | Parejko, J. A., Mavrodi, D. V., Mavrodi, O. V., Weller, D. M. and Thomashow, L. S. 2012. Population structure and diversity of phenazine-1-carboxylic acid producing fluorescent Pseudomonas spp. from dryland cereal fields of central washington state (USA). Microb. Ecol. 64:226-241. DOI |
21 | Pierson, L. S., III, Gaffney, T., Lam, S. and Gong, F. 1995. Molecular analysis of genes encoding phenazine biosynthesis in the biological control bacterium pseudomonas aureofaciens 30-84. FEMS Microbiol. Lett. 134:299-307. |
22 | Pierson, L. S., III and Pierson, E. A. 2010. Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. Appl. Microbiol. Biotechnol. 86:1659-1670. DOI |
23 | Pierson, L. S., III and Thomashow, L. S. 1992. Cloning and heterologous expression of the phenazine biosynthetic locus from Pseudomonas aureofaciens 30-84. Mol. Plant-Microbe Interact. 5:330-339. DOI |
24 | Chin-A-Woeng, T. F., Bloemberg, G. V. and Lugtenberg, B. J. 2003. Phenazines and their role in biocontrol by Pseudomonas bacteria. New Phytol. 157:503-523. DOI |
25 | Price-Whelan, A., Dietrich, L. E. and Newman, D. K. 2006. Rethinking 'secondary' metabolism: physiological roles for phenazine antibiotics. Nat. Chem. Biol. 2:71-78. DOI |
26 | Alhede, M., Kragh, K. N., Qvortrup, K., Allesen-Holm, M., van Gennip, M., Christensen, L. D., Jensen, P. O., Nielsen, A. K., Parsek, M. and Wozniak, D. 2011. Phenotypes of non-attached Pseudomonas aeruginosa aggregates resemble surface attached biofilm. PLoS One 6:e27943. DOI |
27 | Baron, S. S., Terranova, G. and Rowe, J. J. 1989. Molecular mechanism of the antimicrobial action of pyocyanin. Curr. Microbiol. 18:223-230. DOI |
28 | Bellin, D. L., Sakhtah, H., Rosenstein, J. K., Levine, P. M., Thimot, J., Emmett, K., Dietrich, L. E. and Shepard, K. L. 2014. Integrated circuit-based electrochemical sensor for spatially resolved detection of redox-active metabolites in biofilms. Nat. Commun. 5:3256. |
29 | Berg, G., Fritze, A., Roskot, N. and Smalla, K. 2001. Evaluation of potential biocontrol rhizobacteria from different host plants of Verticillium dahliae kleb. J. Appl. Microbiol. 91:963-971. DOI |
30 | Cezairliyan, B., Vinayavekhin, N., Grenfell-Lee, D., Yuen, G. J., Saghatelian, A. and Ausubel, F. M. 2013. Identification of Pseudomonas aeruginosa phenazines that kill Caenorhabditis elegans. PLoS Pathog. 9:e1003101. DOI |
31 | Chin-A-Woeng, T. F., Bloemberg, G. V., van der Bij, A. J., van der Drift, K. M., Schripsema, J., Kroon, B., Scheffer, R. J., Keel, C., Bakker, P. A. and Tichy, H.-V. 1998. Biocontrol by phenazine-1-carboxamide-producing Pseudomonas chlororaphis pcl1391 of tomato root rot caused by Fusarium oxysporum f. Sp. radicis-lycopersici. Mol. Plant-Microbe Interact. 11:1069-1077. DOI |
32 | Steinberg, N. and Kolodkin-Gal, I. 2015. The matrix reloaded: How sensing the extracellular matrix synchronizes bacterial communities. J. Bacteriol. 197:2092-2103. DOI |
33 | Ramos, I., Dietrich, L. E., Price-Whelan, A. and Newman, D. K. 2010. Phenazines affect biofilm formation by Pseudomonas aeruginosa in similar ways at various scales. Res. Microbiol. 161:187-191. DOI |
34 | Sambrook, J. and Russell, D. W. 2001. Molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA. |
35 | Selin, C., Habibian, R., Poritsanos, N., Athukorala, S. N., Fernando, D. and De Kievit, T. R. 2009. Phenazines are not essential for Pseudomonas chlororaphis pa23 biocontrol of Sclerotinia sclerotiorum, but do play a role in biofilm formation. FEMS Microbiol. Ecol. 71:73-83. |
36 | Thomashow, L. S. and Weller, D. M. 1988. Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. J. Bacteriol. 170:3499-3508. DOI |
37 | Turner, J. M. and Messenger, A. J. 1986. Occurrence, biochemistry and physiology of phenazine pigment production. Adv. Microb. Physiol. 27:211-275. |
38 | Wang, D., Yu, J. M., Dorosky, R. J., Pierson, L. S., III and Pierson, E. A. 2016. The phenazine 2-hydroxy-phenazine-1-carboxylic acid promotes extracellular DNA release and has broad transcriptomic consequences in Pseudomonas chlororaphis 30-84. PLoS One 11:e0148003. DOI |
39 | Wang, Y., Wilks, J. C., Danhorn, T., Ramos, I., Croal, L. and Newman, D. K. 2011. Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition. J. Bacteriol. 193:3606-3617. DOI |
40 | Wang, Y. and Newman, D. K. 2008. Redox reactions of phenazine antibiotics with ferric (hydr) oxides and molecular oxygen. Envrion. Sci. Technol. 42:2380-2386. DOI |
41 | Das, T., Sehar, S. and Manefield, M. 2013b. The roles of extracellular DNA in the structural integrity of extracellular polymeric substance and bacterial biofilm development. Environ. Microbiol. Rep. 5:778-786. DOI |
42 | Chin-A-Woeng, T. F., Thomas-Oates, J. E., Lugtenberg, B. J. and Bloemberg, G. V. 2001a. Introduction of the phzh gene of Pseudomonas chlororaphis pcl1391 extends the range of biocontrol ability of phenazine-1-carboxylic acid-producing Pseudomonas spp. strains. Mol. Plant-Microbe Interact. 14:1006-1015. DOI |
43 | Chin-A-Woeng, T. F., van den Broek, D., de Voer, G., van der Drift, K. M., Tuinman, S., Thomas-Oates, J. E., Lugtenberg, B. J. and Bloemberg, G. V. 2001b. Phenazine-1-carboxamide production in the biocontrol strain Pseudomonas chlororaphis pcl1391 is regulated by multiple factors secreted into the growth medium. Mol. Plant-Microbe Interact. 14:969-979. DOI |
44 | Das, T., Kutty, S. K., Kumar, N. and Manefield, M. 2013a. Pyocyanin facilitates extracellular DNA binding to Pseudomonas aeruginosa influencing cell surface properties and aggregation. PLoS One 8:e58299. DOI |
45 | Das, T., Kutty, S. K., Tavallaie, R., Ibugo, A. I., Panchompoo, J., Sehar, S., Aldous, L., Yeung, A. W., Thomas, S. R. and Kumar, N. 2015. Phenazine virulence factor binding to extracellular DNA is important for Pseudomonas aeruginosa biofilm formation. Sci. Rep. 5:8398. DOI |
46 | Das, T. and Manefield, M. 2012. Pyocyanin promotes extracellular DNA release in Pseudomonas aeruginosa. PLoS One 7:e46718. DOI |
47 | Das, T., Sharma, P. K., Busscher, H. J., van der Mei, H. C. and Krom, B. P. 2010. Role of extracellular DNA in initial bacterial adhesion and surface aggregation. Appl. Environ. Microbiol. 76:3405-3408. DOI |
48 | Delaney, S. M., Mavrodi, D. V., Bonsall, R. F. and Thomashow, L. S. 2001. Phzo, a gene for biosynthesis of 2-hydroxylated phenazine compounds in Pseudomonas aureofaciens 30-84. J. Bacteriol. 183:318-327. DOI |
49 | Ghosh, P. K. and Maiti, T. K. 2016. Structure of extracellular polysaccharides (eps) produced by rhizobia and their functions in legume-bacteria symbiosis. Achiev. Life Sci. 10:136-143. DOI |
50 | Flemming, H.-C. and Wingender, J. 2010. The biofilm matrix. Nat. Rev. Microbiol. 8:623-633. DOI |
51 | Gibson, J., Sood, A. and Hogan, D. A. 2009. Pseudomonas aeruginosa-candida albicans interactions: localization and fungal toxicity of a phenazine derivative. Appl. Environ. Microbiol. 75:504-513. DOI |
52 | Gloag, E. S., Turnbull, L., Huang, A., Vallotton, P., Wang, H., Nolan, L. M., Mililli, L., Hunt, C., Lu, J. and Osvath, S. R. 2013. Self-organization of bacterial biofilms is facilitated by extracellular DNA. Proc. Natl. Acad. Sci. U.S.A. 110:11541-11546. DOI |
53 | Gu, M. and Imlay, J. A. 2011. The soxrs response of Escherichia coli is directly activated by redox-cycling drugs rather than by superoxide. Mol. Microbiol. 79:1136-1150. DOI |
54 | Gunn, J. S., Bakaletz, L. O. and Wozniak, D. J. 2016. What's on the outside matters: the role of the extracellular polymeric substance of gram-negative biofilms in evading host immunity and as a target for therapeutic intervention. J. Biol. Chem. 291:12538-12546. DOI |
55 | Haas, D. and Defago, G. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3:307-319. DOI |
56 | Hassett, D., Charniga, L., Bean, K., Ohman, D. and Cohen, M. S. 1992. Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of a manganese-cofactored superoxide dismutase. Infect. Immun. 60:328-336. |
57 | Flaishman, M., Eyal, Z., Voisard, C. and Haas, D. 1990. Suppression of Septoria tritici by phenazine-or siderophore-deficient mutants of Pseudomonas. Curr. Microbiol. 20:121-124. DOI |
58 | Liu, G. Y. and Nizet, V. 2009. Color me bad: microbial pigments as virulence factors. Trends Microbiol. 17:406-413. DOI |
59 | Haynes, W. C., Stodola, F. H., Locke, J. M., Pridham, T. G., Conway, H. F., Sohns, V. E. and Jackson, R. W. 1956. Pseudomonas aureofaciens kluyver and phenazine -carboxylic acid, its characteristic pigment. J. Bacteriol. 72:412. |
60 | Jayathilake, P. G., Jana, S., Rushton, S., Swailes, D., Bridgens, B., Curtis, T. and Chen, J. 2017. Extracellular polymeric substance production and aggregated bacteria colonization influence the competition of microbes in biofilms. Front. Microbiol. 8:1865. DOI |
61 | Maddula, V. S., Pierson, E. A. and Pierson, L. S., III. 2008. Altering the ratio of phenazines in Pseudomonas chlororaphis (aureofaciens) strain 30-84: effects on biofilm formation and pathogen inhibition. J. Bacteriol. 190:2759-2766. DOI |
62 | Maddula, V. S., Zhang, Z., Pierson, E. A. and Pierson, L. S., III. 2006. Quorum sensing and phenazines are involved in biofilm formation by Pseudomonas chlororaphis (aureofaciens) strain 30-84. Microb. Ecol. 52:289-301. DOI |
63 | Mann, E. E. and Wozniak, D. J. 2012. Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol. Rev. 36:893-916. DOI |
64 | Mavrodi, D. V., Blankenfeldt, W. and Thomashow, L. S. 2006. Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu. Rev. Phytopathol. 44:417-445. DOI |
65 | Mavrodi, D. V., Bonsall, R. F., Delaney, S. M., Soule, M. J., Phillips, G. and Thomashow, L. S. 2001. Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa pao1. J. Bacteriol. 183:6454-6465. DOI |