An iron detection system determines bacterial swarming initiation and biofilm formation

Chuan-Sheng Lin; Yu-Huan Tsai; Chih-Jung Chang; Shun-Fu Tseng; Tsung-Ru Wu; Chia-Chen Lu; Ting-Shu Wu; Jang-Jih Lu; Jim-Tong Horng; Jan Martel; David M. Ojcius; Hsin-Chih Lai; John D. Young; S. C. Andrews; A. K. Robinson; F. Rodriguez-Quinones; D. Touati; J. Yeom; J. A. Imlay; W. Park; J. J. Marx; V. Braun; K. Hantke; P. Cornelis; Q. Wei; T. Vinckx; B. Troxell; H. M. Hassan; N. Verstraeten; K. Lewis; L. Hall-Stoodley; J. W. Costerton; P. Stoodley; D. B. Kearns; R. Losick; M. T. Butler; Q. Wang; R. M. Harshey; S. Lai; J. Tremblay; E. Deziel; J. Overhage; M. Bains; M. D. Brazas; R. E. Hancock; J. D. Partridge; W. Kim; M. G. Surette; M. Givskov; P. N. Rather; R. Van Houdt; C. W. Michiels; S. Mukherjee; T. Inoue; J. G. Frye; M. McClelland; L. McCarter; M. Silverman; M. A. Matilla; Y. Wu; F. W. Outten; P. K. Singh; M. R. Parsek; E. P. Greenberg; M. J. Welsh; E. Banin; M. L. Vasil; M. M. Wosten; L. F. Kox; S. Chamnongpol; F. C. Soncini; E. A. Groisman; M. T. Laub; M. Goulian; T. Krell; H. C. Lai; C. S. Lin; P. C. Soo; Y. H. Tsai; J. R. Wei; E. E. Wyckoff; A. R. Mey; A. Leimbach; C. F. Fisher; S. M. Payne; K. J. Livak; T. D. Schmittgen; M. B. Clarke; D. T. Hughes; C. Zhu; E. C. Boedeker; V. Sperandio; A. Stintzi; M. F. Clarke-Pearson; S. F. Brady; E. J. Drake; A. M. Gulick; U. Qaisar; M. A. Rowland; E. J. Deeds; C. A. Garcia; E. S. Alcaraz; M. A. Franco; B. N. Passerini de Rossi; O. Mehi; E. P. Skaar; D. Visaggio; K. Nishino; P. Dietz; G. Gerlach; D. Beier; S. A. Bustin; B. Schwyn; J. B. Neilands

doi:10.1038/srep36747

An iron detection system determines bacterial swarming initiation and biofilm formation

Chuan-Sheng Lin, Yu-Huan Tsai, Chih-Jung Chang, Shun-Fu Tseng, Tsung-Ru Wu, Chia-Chen Lu, Ting-Shu Wu, Jang-Jih Lu, Jim-Tong Horng, Jan Martel, David M. Ojcius, Hsin-Chih Lai, John D. Young, S. C. Andrews, A. K. Robinson, F. Rodriguez-Quinones, D. Touati, J. Yeom, J. A. Imlay, W. ParkJ. J. Marx, V. Braun, K. Hantke, P. Cornelis, Q. Wei, T. Vinckx, B. Troxell, H. M. Hassan, N. Verstraeten, K. Lewis, L. Hall-Stoodley, J. W. Costerton, P. Stoodley, D. B. Kearns, R. Losick, M. T. Butler, Q. Wang, R. M. Harshey, S. Lai, J. Tremblay, E. Deziel, J. Overhage, M. Bains, M. D. Brazas, R. E. Hancock, J. D. Partridge, W. Kim, M. G. Surette, M. Givskov, P. N. Rather, R. Van Houdt, C. W. Michiels, S. Mukherjee, T. Inoue, J. G. Frye, M. McClelland, L. McCarter, M. Silverman, M. A. Matilla, Y. Wu, F. W. Outten, P. K. Singh, M. R. Parsek, E. P. Greenberg, M. J. Welsh, E. Banin, M. L. Vasil, M. M. Wosten, L. F. Kox, S. Chamnongpol, F. C. Soncini, E. A. Groisman, M. T. Laub, M. Goulian, T. Krell, H. C. Lai, C. S. Lin, P. C. Soo, Y. H. Tsai, J. R. Wei, E. E. Wyckoff, A. R. Mey, A. Leimbach, C. F. Fisher, S. M. Payne, K. J. Livak, T. D. Schmittgen, M. B. Clarke, D. T. Hughes, C. Zhu, E. C. Boedeker, V. Sperandio, A. Stintzi, M. F. Clarke-Pearson, S. F. Brady, E. J. Drake, A. M. Gulick, U. Qaisar, M. A. Rowland, E. J. Deeds, C. A. Garcia, E. S. Alcaraz, M. A. Franco, B. N. Passerini de Rossi, O. Mehi, E. P. Skaar, D. Visaggio, K. Nishino, P. Dietz, G. Gerlach, D. Beier, S. A. Bustin, B. Schwyn, J. B. Neilands

Research output: Contribution to journal › Article › Academic › peer-review

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.

Original language	English
Article number	36747
Pages (from-to)	1-12
Number of pages	13
Journal	Scientific Reports
Volume	6
DOIs	https://doi.org/10.1038/srep36747
Publication status	Published - 15 Nov 2016

Keywords

Bacteriology
Biofilms
Microbial communities

Access to Document

10.1038/srep36747

1Final published version, 2.21 MB

http://www.mendeley.com/research/iron-detection-system-determines-bacterial-swarming-initiation-biofilm-formation

Cite this

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., ... Neilands, J. B. (2016). An iron detection system determines bacterial swarming initiation and biofilm formation. Scientific Reports, 6, 1-12. Article 36747. https://doi.org/10.1038/srep36747

@article{5b09337d183c4b24b55e41f5c9e01ee2,

title = "An iron detection system determines bacterial swarming initiation and biofilm formation",

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",

author = "Chuan-Sheng Lin and Yu-Huan Tsai and Chih-Jung Chang and Shun-Fu Tseng and Tsung-Ru Wu and Chia-Chen Lu and Ting-Shu Wu and Jang-Jih Lu and Jim-Tong Horng and Jan Martel and Ojcius, {David M.} and Hsin-Chih Lai and Young, {John D.} and Andrews, {S. C.} and Robinson, {A. K.} and F. Rodriguez-Quinones and D. Touati and J. Yeom and Imlay, {J. A.} and W. Park and Marx, {J. J.} and V. Braun and K. Hantke and P. Cornelis and Q. Wei and T. Vinckx and B. Troxell and Hassan, {H. M.} and N. Verstraeten and K. Lewis and L. Hall-Stoodley and Costerton, {J. W.} and P. Stoodley and Kearns, {D. B.} and R. Losick and Butler, {M. T.} and Q. Wang and Harshey, {R. M.} and S. Lai and J. Tremblay and E. Deziel and J. Overhage and M. Bains and Brazas, {M. D.} and Hancock, {R. E.} and Partridge, {J. D.} and W. Kim and Surette, {M. G.} and M. Givskov and Rather, {P. N.} and Houdt, {R. Van} and Michiels, {C. W.} and S. Mukherjee and T. Inoue and Frye, {J. G.} and M. McClelland and L. McCarter and M. Silverman and Matilla, {M. A.} and Y. Wu and Outten, {F. W.} and Singh, {P. K.} and Parsek, {M. R.} and Greenberg, {E. P.} and Welsh, {M. J.} and E. Banin and Vasil, {M. L.} and Wosten, {M. M.} and Kox, {L. F.} and S. Chamnongpol and Soncini, {F. C.} and Groisman, {E. A.} and Laub, {M. T.} and M. Goulian and T. Krell and Lai, {H. C.} and Lin, {C. S.} and Soo, {P. C.} and Tsai, {Y. H.} and Wei, {J. R.} and Wyckoff, {E. E.} and Mey, {A. R.} and A. Leimbach and Fisher, {C. F.} and Payne, {S. M.} and Livak, {K. J.} and Schmittgen, {T. D.} and Clarke, {M. B.} and Hughes, {D. T.} and C. Zhu and Boedeker, {E. C.} and V. Sperandio and A. Stintzi and Clarke-Pearson, {M. F.} and Brady, {S. F.} and Drake, {E. J.} and Gulick, {A. M.} and U. Qaisar and Rowland, {M. A.} and Deeds, {E. J.} and Garcia, {C. A.} and Alcaraz, {E. S.} and Franco, {M. A.} and Rossi, {B. N. Passerini de} and O. Mehi and Skaar, {E. P.} and D. Visaggio and K. Nishino and P. Dietz and G. Gerlach and D. Beier and Bustin, {S. A.} and B. Schwyn and Neilands, {J. B.}",

year = "2016",

month = nov,

day = "15",

doi = "10.1038/srep36747",

language = "English",

volume = "6",

pages = "1--12",

journal = "Scientific Reports",

issn = "2045-2322",

publisher = "NLM (Medline)",

}

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, DM, Lai, H-C, Young, JD, Andrews, SC, Robinson, AK, Rodriguez-Quinones, F, Touati, D, Yeom, J, Imlay, JA, Park, W, Marx, JJ, Braun, V, Hantke, K, Cornelis, P, Wei, Q, Vinckx, T, Troxell, B, Hassan, HM, Verstraeten, N, Lewis, K, Hall-Stoodley, L, Costerton, JW, Stoodley, P, Kearns, DB, Losick, R, Butler, MT, Wang, Q, Harshey, RM, Lai, S, Tremblay, J, Deziel, E, Overhage, J, Bains, M, Brazas, MD, Hancock, RE, Partridge, JD, Kim, W, Surette, MG, Givskov, M, Rather, PN, Houdt, RV, Michiels, CW, Mukherjee, S, Inoue, T, Frye, JG, McClelland, M, McCarter, L, Silverman, M, Matilla, MA, Wu, Y, Outten, FW, Singh, PK, Parsek, MR, Greenberg, EP, Welsh, MJ, Banin, E, Vasil, ML, Wosten, MM, Kox, LF, Chamnongpol, S, Soncini, FC, Groisman, EA, Laub, MT, Goulian, M, Krell, T, Lai, HC, Lin, CS, Soo, PC, Tsai, YH, Wei, JR, Wyckoff, EE, Mey, AR, Leimbach, A, Fisher, CF, Payne, SM, Livak, KJ, Schmittgen, TD, Clarke, MB, Hughes, DT, Zhu, C, Boedeker, EC, Sperandio, V, Stintzi, A, Clarke-Pearson, MF, Brady, SF, Drake, EJ, Gulick, AM, Qaisar, U, Rowland, MA, Deeds, EJ, Garcia, CA, Alcaraz, ES, Franco, MA, Rossi, BNPD, Mehi, O, Skaar, EP, Visaggio, D, Nishino, K, Dietz, P, Gerlach, G, Beier, D, Bustin, SA, Schwyn, B & Neilands, JB 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

TY - JOUR

T1 - An iron detection system determines bacterial swarming initiation and biofilm formation

AU - Lin, Chuan-Sheng

AU - Tsai, Yu-Huan

AU - Chang, Chih-Jung

AU - Tseng, Shun-Fu

AU - Wu, Tsung-Ru

AU - Lu, Chia-Chen

AU - Wu, Ting-Shu

AU - Lu, Jang-Jih

AU - Horng, Jim-Tong

AU - Martel, Jan

AU - Ojcius, David M.

AU - Lai, Hsin-Chih

AU - Young, John D.

AU - Andrews, S. C.

AU - Robinson, A. K.

AU - Rodriguez-Quinones, F.

AU - Touati, D.

AU - Yeom, J.

AU - Imlay, J. A.

AU - Park, W.

AU - Marx, J. J.

AU - Braun, V.

AU - Hantke, K.

AU - Cornelis, P.

AU - Wei, Q.

AU - Vinckx, T.

AU - Troxell, B.

AU - Hassan, H. M.

AU - Verstraeten, N.

AU - Lewis, K.

AU - Hall-Stoodley, L.

AU - Costerton, J. W.

AU - Stoodley, P.

AU - Kearns, D. B.

AU - Losick, R.

AU - Butler, M. T.

AU - Wang, Q.

AU - Harshey, R. M.

AU - Lai, S.

AU - Tremblay, J.

AU - Deziel, E.

AU - Overhage, J.

AU - Bains, M.

AU - Brazas, M. D.

AU - Hancock, R. E.

AU - Partridge, J. D.

AU - Kim, W.

AU - Surette, M. G.

AU - Givskov, M.

AU - Rather, P. N.

AU - Houdt, R. Van

AU - Michiels, C. W.

AU - Mukherjee, S.

AU - Inoue, T.

AU - Frye, J. G.

AU - McClelland, M.

AU - McCarter, L.

AU - Silverman, M.

AU - Matilla, M. A.

AU - Wu, Y.

AU - Outten, F. W.

AU - Singh, P. K.

AU - Parsek, M. R.

AU - Greenberg, E. P.

AU - Welsh, M. J.

AU - Banin, E.

AU - Vasil, M. L.

AU - Wosten, M. M.

AU - Kox, L. F.

AU - Chamnongpol, S.

AU - Soncini, F. C.

AU - Groisman, E. A.

AU - Laub, M. T.

AU - Goulian, M.

AU - Krell, T.

AU - Lai, H. C.

AU - Lin, C. S.

AU - Soo, P. C.

AU - Tsai, Y. H.

AU - Wei, J. R.

AU - Wyckoff, E. E.

AU - Mey, A. R.

AU - Leimbach, A.

AU - Fisher, C. F.

AU - Payne, S. M.

AU - Livak, K. J.

AU - Schmittgen, T. D.

AU - Clarke, M. B.

AU - Hughes, D. T.

AU - Zhu, C.

AU - Boedeker, E. C.

AU - Sperandio, V.

AU - Stintzi, A.

AU - Clarke-Pearson, M. F.

AU - Brady, S. F.

AU - Drake, E. J.

AU - Gulick, A. M.

AU - Qaisar, U.

AU - Rowland, M. A.

AU - Deeds, E. J.

AU - Garcia, C. A.

AU - Alcaraz, E. S.

AU - Franco, M. A.

AU - Rossi, B. N. Passerini de

AU - Mehi, O.

AU - Skaar, E. P.

AU - Visaggio, D.

AU - Nishino, K.

AU - Dietz, P.

AU - Gerlach, G.

AU - Beier, D.

AU - Bustin, S. A.

AU - Schwyn, B.

AU - Neilands, J. B.

PY - 2016/11/15

Y1 - 2016/11/15

N2 - 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.

AB - 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.

KW - Bacteriology

KW - Biofilms

KW - Microbial communities

U2 - 10.1038/srep36747

DO - 10.1038/srep36747

M3 - Article

C2 - 27845335

SN - 2045-2322

VL - 6

SP - 1

EP - 12

JO - Scientific Reports

JF - Scientific Reports

M1 - 36747

ER -

An iron detection system determines bacterial swarming initiation and biofilm formation

Abstract

Keywords

Access to Document

Fingerprint

Cite this