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

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^*

^*Corresponding author for this work

Institute of Microbiology and Immunology

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

35 Scopus citations

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 (Fe ³⁺) availability to determine swarming initiation and biofilm formation. We demonstrate that the two-component system RssA-RssB (RssAB) directly senses environmental ferric iron (Fe ³⁺) and transcriptionally modulates biosynthesis of flagella and the iron chelator ICDH-Coumarin whose production requires the pvc cluster. Addition of Fe ³⁺, 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 Fe ³⁺ 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
Journal	Scientific reports
Volume	6
DOIs	https://doi.org/10.1038/srep36747
State	Published - 15 Nov 2016

Access to Document

10.1038/srep36747

Cite this

@article{f5a7867985984dae9e2e4610c91089b0,

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 (Fe 3+) availability to determine swarming initiation and biofilm formation. We demonstrate that the two-component system RssA-RssB (RssAB) directly senses environmental ferric iron (Fe 3+) and transcriptionally modulates biosynthesis of flagella and the iron chelator ICDH-Coumarin whose production requires the pvc cluster. Addition of Fe 3+, 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 Fe 3+ 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.",

author = "Lin, {Chuan Sheng} and Tsai, {Yu Huan} and Chang, {Chih Jung} and Tseng, {Shun Fu} and Wu, {Tsung Ru} and Lu, {Chia Chen} and Wu, {Ting Shu} and Lu, {Jang Jih} and Horng, {Jim Tong} and Jan Martel and Ojcius, {David M.} and Lai, {Hsin Chih} and Young, {John D.}",

note = "Publisher Copyright: {\textcopyright} 2016 The Author(s).",

year = "2016",

month = nov,

day = "15",

doi = "10.1038/srep36747",

language = "English",

volume = "6",

journal = "Scientific reports",

issn = "2045-2322",

publisher = "Nature Publishing Group",

}

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.

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 (Fe 3+) availability to determine swarming initiation and biofilm formation. We demonstrate that the two-component system RssA-RssB (RssAB) directly senses environmental ferric iron (Fe 3+) and transcriptionally modulates biosynthesis of flagella and the iron chelator ICDH-Coumarin whose production requires the pvc cluster. Addition of Fe 3+, 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 Fe 3+ 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 (Fe 3+) availability to determine swarming initiation and biofilm formation. We demonstrate that the two-component system RssA-RssB (RssAB) directly senses environmental ferric iron (Fe 3+) and transcriptionally modulates biosynthesis of flagella and the iron chelator ICDH-Coumarin whose production requires the pvc cluster. Addition of Fe 3+, 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 Fe 3+ 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.

UR - http://www.scopus.com/inward/record.url?scp=84995511086&partnerID=8YFLogxK

U2 - 10.1038/srep36747

DO - 10.1038/srep36747

M3 - Article

C2 - 27845335

AN - SCOPUS:84995511086

SN - 2045-2322

VL - 6

JO - Scientific reports

JF - Scientific reports

M1 - 36747

ER -

An iron detection system determines bacterial swarming initiation and biofilm formation

Abstract

Access to Document

Other files and links

Fingerprint

Cite this