Acknowledgement
This research was supported financially by an Alberta Ingenuity Industrial Associateship, Innovotech Inc., and Alberta Agriculture and Forestry. Thanks to Mrs. Liz Middlemiss for technical assistance with SEM imaging.
References
- AAT Bioquest. 2019. Quest graph EC50 calculator. URL https://www.aatbio.com/tools/ec50-calculator [10 April 2022].
- Agarkova, I. V., Lambrecht, P. A., Vidaver, A. K. and Harveson, R. M. 2012. Genetic diversity among Curtobacterium flaccumfaciens pv. flaccumfaciens populations in the American high plains. Can. J. Microbiol. 58:788-801. https://doi.org/10.1139/w2012-052
- Anwar, H., Dasgupta, M. K. and Costerton, J. W. 1990. Testing the susceptibility of bacteria in biofilms to antibacterial agents. Antimicrob. Agents Chemother. 34:2043-2046. https://doi.org/10.1128/AAC.34.11.2043
- ASTM International. 2017. ASTM E2799-17: standard test method for testing disinfectant efficacy against Pseudomonas aeruginosa biofilm using the MBEC assay. URL https://www.astm.org/e2799-17.html [10 April 2022].
- Bigger, J. W. 1944. The bactericidal action of penicillin on Staphylococcus pyogenes. Ir. J. Med. Sci. 19:553-568. https://doi.org/10.1007/BF02948386
- Botti-Marino, M. 2017. Epiphytic survival and biofilm formation of the Goss's wilt pathogen Clavibacter michiganensis subsp. nebraskensis. Ph.D. thesis. Michigan State University, East Lansing, MI, USA.
- Bozzola, J. J. and Russell, L. D. 1992. Electron microscopy: principles and techniques for biologists. Jones and Bartlett Publishers, Boston, MA, USA. 670 pp.
- Bragg, P. D. and Rainnie, D. J. 1974. The effect of silver ions on the respiratory chain of Escherichia coli. Can. J. Microbiol. 20:883-889. https://doi.org/10.1139/m74-135
- Bridier, A., Briandet, R., Thomas, V. and Dubois-Brissonnet, F. 2011. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27:1017-1032. https://doi.org/10.1080/08927014.2011.626899
- Castiblanco, L. F. and Sundin, G. W. 2016. New insights on molecular regulation of biofilm formation in plant-associated bacteria. J. Integr. Plant Biol. 58:362-372. https://doi.org/10.1111/jipb.12428
- Conner, R. L., Balasubramanian, P., Erickson, R. S., Huang, H. C. and Mundel, H. H. 2008. Bacterial wilt resistance in kidney beans. Can. J. Plant Sci. 88:1109-1113. https://doi.org/10.4141/CJPS08074
- De Beer, D., Stoodley, P. and Lewandowski, Z. 1994. Liquid flow in heterogeneous biofilms. Biotechnol. Bioeng. 44:636-641. https://doi.org/10.1002/bit.260440510
- De Beer, D., Stoodley, P. and Lewandowski, Z. 1996. Liquid flow and mass transport in heterogeneous biofilms. Water Res. 30:2761-2765. https://doi.org/10.1016/S0043-1354(96)00141-8
- Demirci, H., Murphy, F., Murphy, E., Gregory, S. T., Dahlberg, A. E. and Jogl, G. 2013. A structural basis for streptomycin-induced misreading of the genetic code. Nat. Commun. 4:1355. https://doi.org/10.1038/ncomms2346
- Gilbert, P. and McBain, A. J. 2001. Biofilms: their impact on heath and their recalcitrance toward biocides. Am. J. Infect. Control 29:252-255. https://doi.org/10.1067/mic.2001.115673
- Grass, G., Rensing, C. and Solioz, M. 2011. Metallic copper as an antimicrobial surface. Appl. Environ. Microbiol. 77:1541-1547. https://doi.org/10.1128/AEM.02766-10
- Harding, M. W. and Daniels, G. C. 2017. In vitro assessment of biofilm formation by soil- and plant-associated microorganisms. In: Biofilms in plant and soil health, eds. by I. Ahmad and F. M. Husain, pp. 253-273. John Wiley & Sons, Ltd., West Sussex, UK.
- Harding, M. W., Howard, R. J., Daniels, G. D., Mobbs, S. L., Lisowski, S. L. I., Allan, N. D., Omar, A. and Olson, M. E. 2011. A multi-well plate method for rapid growth, characterization and biocide sensitivity testing of microbial biofilms on various surface materials. In: Science against microbial pathogens: communicating current research and technological advances, ed. by A. Mendez-Vilas, pp. 872-877. Formatex Research Centre, Badajoz, Spain.
- Harding, M. W., Marques, L. L. R., Howard, R. J. and Olson, M. E. 2010. Biofilm morphologies of plant pathogenic fungi. Am. J. Plant Sci. Biotechnol. 4:43-47.
- Harding, M., Nadworny, P., Buziak, B., Omar, A., Daniels, G. and Feng, J. 2019. Improved methods for treatment of phytopathogenic biofilms: metallic compounds as anti-bacterial coatings and fungicide tank-mix partners. Molecules 24:2312. https://doi.org/10.3390/molecules24122312
- Harrison, J. J., Stremick, C. A., Turner, R. J., Allan, N. D., Olson, M. E. and Ceri, H. 2010. Microtiter susceptibility testing of microbes growing on peg lids: a miniaturized biofilm model for high-throughput screening. Nat. Protoc. 5:1236-1254. https://doi.org/10.1038/nprot.2010.71
- Harveson, R. M. and Schwartz, H. F. 2007. Bacterial diseases of dry edible beans in the Central High Plains. Plant Health Prog. 8:35. https://doi.org/10.1094/php-2007-0125-01-dg
- Harveson, R. M., Schwartz, H. F., Urrea, C. A. and Yonts, C. D. 2015. Bacterial wilt of dry-edible beans in the central high plains of the US: past, present, and future. Plant Dis. 99:1665-1677. https://doi.org/10.1094/PDIS-03-15-0299-FE
- Howard, R. J., Harding, M. W., Daniels, G. C., Mobbs, S. L., Lisowski, S. L. I. and De Boer, S. H. 2015. Efficacy of agricultural disinfectants on biofilms of the bacterial ring rot pathogen, Clavibacter michiganensis subsp. sepedonicus. Can. J. Plant Pathol. 37:273-284. https://doi.org/10.1080/07060661.2015.1078413
- Hsieh, T. F., Huang, H. C., Mundel, H.-H., Conner, R. L., Erickson, R. S. and Balasubramanian, P. M. 2005. Resistance of common bean (Phaseolus vulgaris) to bacterial wilt caused by Curtobacterium flaccumfaciens pv. flaccumfaciens. J. Phytopathol. 153:245-249. https://doi.org/10.1111/j.1439-0434.2005.00963.x
- Huang, H. C., Erickson, R. S., Balasubramanian, P. M., Hsieh, T. F. and Conner, R. L. 2009. Resurgence of bacterial wilt of common bean in North America. Can. J. Plant Pathol. 31:290-300. https://doi.org/10.1080/07060660909507603
- Huang, H. C., Erickson, R. S. and Hsieh, T. F. 2007. Control of bacterial wilt of bean (Curtobacterium flaccumfaciens pv. flaccumfaciens) by seed treatment with Rhizobium leguminosarum. Crop Prot. 26:1055-1061. https://doi.org/10.1016/j.cropro.2006.09.018
- Koczan, J. M., McGrath, M. J., Zhao, Y. and Sundin, G. W. 2009. Contribution of Erwinia amylovora exopolysaccharides amylovoran and levan to biofilm formation: implications in pathogenicity. Phytopathology 99:1237-1244. https://doi.org/10.1094/PHYTO-99-11-1237
- Koutsoudis, M. D., Tsaltas, D., Minogue, T. D. and von Bodman, S. B. 2006. Quorum-sensing regulation governs bacterial adhesion, biofilm development, and host colonization in Pantoea stewartii subspecies stewartii. Proc. Natl. Acad. Sci. U. S. A. 103:5983-5988. https://doi.org/10.1073/pnas.0509860103
- Lewis, K. 2001. Riddle of biofilm resistance. Antimicrob. Agents Chemother. 45:999-1007. https://doi.org/10.1128/AAC.45.4.999-1007.2001
- Marques, L. L. R., Ceri, H., Manfio, G. P., Reid, D. M. and Olson, M. E. 2002. Characterization of biofilm formation by Xylella fastidiosa in vitro. Plant Dis. 86:633-638. https://doi.org/10.1094/pdis.2002.86.6.633
- Mathews, S., Hans, M., Mucklich, F. and Solioz, M. 2013. Contact killing of bacteria on copper is suppressed if bacterialmetal contact is prevented and is induced on iron by copper ions. Appl. Environ. Microbiol. 79:2605-2611. https://doi.org/10.1128/AEM.03608-12
- Miyaue, S., Suzuki, E., Komiyama, Y., Kondo, Y., Morikawa, M. and Maeda, S. 2018. Bacterial memory of persisters: bacterial persister cells can retain their phenotype for days or weeks after withdrawal from colony-biofilm culture. Front. Microbiol. 9:1396. https://doi.org/10.3389/fmicb.2018.01396
- Modak, S. M. and Fox, C. L. Jr. 1973. Binding of silver sulfadiazine to the cellular components of Pseudomonas aeruginosa. Biochem. Pharmacol. 22:2391-2404. https://doi.org/10.1016/0006-2952(73)90341-9
- Mori, Y., Inoue, K., Ikeda, K., Nakayashiki, H., Higashimoto, C., Ohnishi, K., Kiba, A. and Hikichi, Y. 2016. The vascular plant-pathogenic bacterium Ralstonia solanacearum produces biofilms required for its virulence on the surfaces of tomato cells adjacent to intercellular spaces. Mol. Plant Pathol. 17:890-902. https://doi.org/10.1111/mpp.12335
- Nadworny, P., Omotoso, O. and Zheng, Z. 2015. Comparison of oxysilver nitrate and oxysilver bisulfate, Part I: Synthesis and physicochemical properties. Polyhedron 99:204-215. https://doi.org/10.1016/j.poly.2015.07.038
- Osdaghi, E., Taghavi, S. M., Hamzehzarghani, H., Fazliarab, A., Harveson, R. M. and Lamichhane, J. R. 2016. Occurrence and characterization of a new red-pigmented variant of Curtobacterium flaccumfaciens, the causal agent of bacterial wilt of edible dry beans in Iran. Eur. J. Plant Pathol. 146:129-145. https://doi.org/10.1007/s10658-016-0900-3
- Osdaghi, E., Young, A. J. and Harveson, R. M. 2020. Bacterial wilt of dry beans caused by Curtobacterium flaccumfaciens pv. flaccumfaciens: a new threat from an old enemy. Mol. Plant Pathol. 21:605-621. https://doi.org/10.1111/mpp.12926
- Padmavathi, A. R., Bakkiyaraj, D. and Pandian, S. K. 2017. Biochemical and molecular mechanisms in biofilm formation of plant associated bacteria. In: Biofilms in plant and soil health, eds. by I. Ahmad and F. M. Husain, pp. 195-214. John Wiley & Sons, Ltd., West Sussex, UK.
- Picioreanu, C., van Loosdrecht, M. C. M. and Heijnen, J. J. 2000. Effect of diffusive and convective substrate transport on biofilm structure formation: a two-dimensional modeling study. Biotechnol. Bioeng. 69:504-515. https://doi.org/10.1002/1097-0290(20000905)69:5<504::AID-BIT5>3.0.CO;2-S
- Ramey, B. E., Koutsoudis, M., von Bodman, S. B. and Fuqua, C. 2004. Biofilm formation in plant-microbe associations. Curr. Opin. Microbiol. 7:602-609. https://doi.org/10.1016/j.mib.2004.10.014
- Reichhardt, C. and Parsek, M. R. 2019. Confocal laser scanning microscopy for analysis of Pseudomonas aeruginosa biofilm architecture and matrix localization. Front Microbiol. 10:677. https://doi.org/10.3389/fmicb.2019.00677
- Russell, A. D. and Hugo, W. B. 1994. Antimicrobial activity and action of silver. Prog. Med. Chem. 31:351-370. https://doi.org/10.1016/S0079-6468(08)70024-9
- Slawson, R. M., Trevors, J. T. and Lee, H. 1992. Silver accumulation and resistance in Pseudomonas stutzeri. Arch. Microbiol. 158:398-404. https://doi.org/10.1007/BF00276299
- Stewart, P. S. 2015. Antimicrobial tolerance in biofilms. Microbiol. Spectr. 3:10.1128/microbiolspec.MB-0010-2014.
- Stewart, P. S., White, B., Boegli, L., Hamerly, T., Williamson, K. S., Franklin, M. J., Bothner, B., James, G. A., Fisher, S., Vital-Lopez, F. G. and Wallqvist, A. 2019. Conceptual model of biofilm antibiotic tolerance that integrates phenomena of diffusion, metabolism, gene expression, and physiology. J. Bacteriol. 22:e00307-19.
- Tarbah, F. and Goodman, R. N. 1987. Systemic spread of Agrobacterium tumefaciens biovar 3 in the vascular system of grapes. Phytopathology 77:915-920. https://doi.org/10.1094/Phyto-77-915
- Urrea, C. A., Harveson, R. M., Nielsen, K. and Venegas, J. 2008. Identification of sources of bacterial wilt resistance in dry beans (Phaseolus vulgaris L.). Ann. Rep. Bean Improv. Coop. 51:58-59.
- Velmourougane, K., Prasanna, R. and Saxena, A. K. 2017. Agriculturally important microbial biofilms: present status and future prospects. J. Basic Microbiol. 57:548-573. https://doi.org/10.1002/jobm.201700046
- Villa, F., Cappitelli, F., Cortesi, P. and Kunova, A. 2017. Fungal biofilms: targets for the development of novel strategies in plant disease management. Front Microbiol. 8:654.
- Wilking J. N., Zaburdaev, N., De Volder, M., Losick, R., Brenner, M. P. and Weitz, D. A. 2002. Liquid transport facilitated by channels in Bacillus subtilis biofilms. Proc. Natl. Acad. Sci. U. S. A. 110:848-852.
- Wilking, J. N., Zaburdaev, V., De Volder, M., Losick, R., Brenner, M. P. and Weitz, D. A. 2013. Liquid transport facilitated by channels in Bacillus subtilis biofilms. Proc. Natl. Acad. Sci. U. S. A. 110:848-852. https://doi.org/10.1073/pnas.1216376110
- Wood, T. K. 2017. Strategies for combating persister cell and biofilm infections. Microb. Biotechnol. 10:1054-1056. https://doi.org/10.1111/1751-7915.12774
- Yan, J. and Bassler, B. L. 2019. Surviving as a community: antibiotic tolerance and persistence in bacterial biofilms. Cell Host Microbe. 26:15-21. https://doi.org/10.1016/j.chom.2019.06.002