An iron detection system determines bacterial swarming initiation and biofilm formation

Publication date

2016-11-15

Authors

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

Editors

Advisors

Supervisors

Document Type

Article
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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) 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.

Keywords

Bacteriology, Biofilms, Microbial communities

Citation

Lin, C-S, Tsai, Y-H, Chang, C-J, Tseng, S-F, Wu, T-R, Lu, C-C, Wu, T-S, Lu, J-J, Horng, J-T, Martel, J, Ojcius, D M, Lai, H-C, Young, J 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 V, 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 P D, Mehi, O, Skaar, E P, Visaggio, D, Nishino, K, Dietz, P, Gerlach, G, Beier, D, Bustin, S A, Schwyn, B & Neilands, J B 2016, 'An iron detection system determines bacterial swarming initiation and biofilm formation', Scientific Reports, vol. 6, 36747, pp. 1-12. https://doi.org/10.1038/srep36747