An iron detection system determines bacterial swarming initiation and biofilm formation
Lin, Chuan-Sheng; Tsai, Yu-Huan; Chang, Chih-Jung; Tseng, Shun-Fu; Wu, Tsung-Ru; Lu, Chia-Chen; Wu, Ting-Shu; Lu, Jang-Jih; Horng, Jim-Tong; Martel, Jan; Ojcius, David M.; Lai, Hsin-Chih; Young, John D.; Andrews, S. C.; Robinson, A. K.; Rodriguez-Quinones, F.; Touati, D.; Yeom, J.; Imlay, J. A.; Park, W.; Marx, J. J.; Braun, V.; Hantke, K.; Cornelis, P.; Wei, Q.; Vinckx, T.; Troxell, B.; Hassan, H. M.; Verstraeten, N.; Lewis, K.; Hall-Stoodley, L.; Costerton, J. W.; Stoodley, P.; Kearns, D. B.; Losick, R.; Butler, M. T.; Wang, Q.; Harshey, R. M.; Lai, S.; Tremblay, J.; Deziel, E.; Overhage, J.; Bains, M.; Brazas, M. D.; Hancock, R. E.; Partridge, J. D.; Kim, W.; Surette, M. G.; Givskov, M.; Rather, P. N.; Houdt, R. Van; Michiels, C. W.; Mukherjee, S.; Inoue, T.; Frye, J. G.; McClelland, M.; McCarter, L.; Silverman, M.; Matilla, M. A.; Wu, Y.; Outten, F. W.; Singh, P. K.; Parsek, M. R.; Greenberg, E. P.; Welsh, M. J.; Banin, E.; Vasil, M. L.; Wosten, M. M.; Kox, L. F.; Chamnongpol, S.; Soncini, F. C.; Groisman, E. A.; Laub, M. T.; Goulian, M.; Krell, T.; Lai, H. C.; Lin, C. S.; Soo, P. C.; Tsai, Y. H.; Wei, J. R.; Wyckoff, E. E.; Mey, A. R.; Leimbach, A.; Fisher, C. F.; Payne, S. M.; Livak, K. J.; Schmittgen, T. D.; Clarke, M. B.; Hughes, D. T.; Zhu, C.; Boedeker, E. C.; Sperandio, V.; Stintzi, A.; Clarke-Pearson, M. F.; Brady, S. F.; Drake, E. J.; Gulick, A. M.; Qaisar, U.; Rowland, M. A.; Deeds, E. J.; Garcia, C. A.; Alcaraz, E. S.; Franco, M. A.; Rossi, B. N. Passerini de; Mehi, O.; Skaar, E. P.; Visaggio, D.; Nishino, K.; Dietz, P.; Gerlach, G.; Beier, D.; Bustin, S. A.; Schwyn, B.; Neilands, J. B.
(2016) Scientific Reports, volume 6, pp. 1 - 12
(Article)
Abstract
Iron availability affects swarming and biofilm formation in various bacterial species. However, how bacteria sense iron and coordinate swarming and biofilm formation remains unclear. Using Serratia marcescens as a model organism, we identify here a stage-specific iron-regulatory machinery comprising a two-component system (TCS) and the TCS-regulated iron chelator 2-isocyano-6,7-dihydroxycoumarin (ICDH-Coumarin)
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that directly senses and modulates environmental ferric iron (Fe3+) availability to determine swarming initiation and biofilm formation. We demonstrate that the two-component system RssA-RssB (RssAB) directly senses environmental ferric iron (Fe3+) and transcriptionally modulates biosynthesis of flagella and the iron chelator ICDH-Coumarin whose production requires the pvc cluster. Addition of Fe3+, or loss of ICDH-Coumarin due to pvc deletion results in prolonged RssAB signaling activation, leading to delayed swarming initiation and increased biofilm formation. We further show that ICDH-Coumarin is able to chelate Fe3+ to switch off RssAB signaling, triggering swarming initiation and biofilm reduction. Our findings reveal a novel cellular system that senses iron levels to regulate bacterial surface lifestyle.
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Keywords: Bacteriology, Biofilms, Microbial communities
ISSN: 2045-2322
Publisher: NLM (Medline)
(Peer reviewed)
