Globins Synthesize the Second Messenger Bis-(3′-5′)-Cyclic Diguanosine Monophosphate in Bacteria

Xuehua Wan, Jason R. Tuckerman, Jennifer A. Saito, Tracey Allen K Freitas, James S. Newhouse, Judith R. Denery, Michael Y. Galperin, Gonzalo Gonzalez, Marie Alda Gilles-Gonzalez, Maqsudul Alam

Research output: Contribution to journalArticle

58 Citations (Scopus)

Abstract

Globin-coupled sensors are heme-binding signal transducers in Bacteria and Archaea in which an N-terminal globin controls the activity of a variable C-terminal domain. Here, we report that BpeGReg, a globin-coupled diguanylate cyclase from the whooping cough pathogen Bordetella pertussis, synthesizes the second messenger bis-(3′-5′)-cyclic diguanosine monophosphate (c-di-GMP) upon oxygen binding. Expression of BpeGReg in Salmonella typhimurium enhances biofilm formation, while knockout of the BpeGReg gene of B. pertussis results in decreased biofilm formation. These results represent the first identification a signal ligand for any diguanylate cyclase and provide definitive experimental evidence that a globin-coupled sensor regulates c-di-GMP synthesis and biofilm formation. We propose that the synthesis of c-di-GMP by globin sensors is a widespread phenomenon in bacteria.

Original languageEnglish (US)
Pages (from-to)262-270
Number of pages9
JournalJournal of Molecular Biology
Volume388
Issue number2
DOIs
StatePublished - May 1 2009

Fingerprint

Globins
Second Messenger Systems
Biofilms
Bacteria
Bordetella pertussis
Gene Knockout Techniques
Whooping Cough
Archaea
Salmonella typhimurium
Transducers
Heme
Oxygen
Ligands
diguanylate cyclase

Keywords

  • biofilm
  • c-di-GMP
  • diguanylate cyclase
  • globin
  • oxygen sensor

ASJC Scopus subject areas

  • Molecular Biology

Cite this

Wan, X., Tuckerman, J. R., Saito, J. A., Freitas, T. A. K., Newhouse, J. S., Denery, J. R., ... Alam, M. (2009). Globins Synthesize the Second Messenger Bis-(3′-5′)-Cyclic Diguanosine Monophosphate in Bacteria. Journal of Molecular Biology, 388(2), 262-270. https://doi.org/10.1016/j.jmb.2009.03.015

Globins Synthesize the Second Messenger Bis-(3′-5′)-Cyclic Diguanosine Monophosphate in Bacteria. / Wan, Xuehua; Tuckerman, Jason R.; Saito, Jennifer A.; Freitas, Tracey Allen K; Newhouse, James S.; Denery, Judith R.; Galperin, Michael Y.; Gonzalez, Gonzalo; Gilles-Gonzalez, Marie Alda; Alam, Maqsudul.

In: Journal of Molecular Biology, Vol. 388, No. 2, 01.05.2009, p. 262-270.

Research output: Contribution to journalArticle

Wan, X, Tuckerman, JR, Saito, JA, Freitas, TAK, Newhouse, JS, Denery, JR, Galperin, MY, Gonzalez, G, Gilles-Gonzalez, MA & Alam, M 2009, 'Globins Synthesize the Second Messenger Bis-(3′-5′)-Cyclic Diguanosine Monophosphate in Bacteria', Journal of Molecular Biology, vol. 388, no. 2, pp. 262-270. https://doi.org/10.1016/j.jmb.2009.03.015
Wan, Xuehua ; Tuckerman, Jason R. ; Saito, Jennifer A. ; Freitas, Tracey Allen K ; Newhouse, James S. ; Denery, Judith R. ; Galperin, Michael Y. ; Gonzalez, Gonzalo ; Gilles-Gonzalez, Marie Alda ; Alam, Maqsudul. / Globins Synthesize the Second Messenger Bis-(3′-5′)-Cyclic Diguanosine Monophosphate in Bacteria. In: Journal of Molecular Biology. 2009 ; Vol. 388, No. 2. pp. 262-270.
@article{95244fc95457477aa79bd243252030c0,
title = "Globins Synthesize the Second Messenger Bis-(3′-5′)-Cyclic Diguanosine Monophosphate in Bacteria",
abstract = "Globin-coupled sensors are heme-binding signal transducers in Bacteria and Archaea in which an N-terminal globin controls the activity of a variable C-terminal domain. Here, we report that BpeGReg, a globin-coupled diguanylate cyclase from the whooping cough pathogen Bordetella pertussis, synthesizes the second messenger bis-(3′-5′)-cyclic diguanosine monophosphate (c-di-GMP) upon oxygen binding. Expression of BpeGReg in Salmonella typhimurium enhances biofilm formation, while knockout of the BpeGReg gene of B. pertussis results in decreased biofilm formation. These results represent the first identification a signal ligand for any diguanylate cyclase and provide definitive experimental evidence that a globin-coupled sensor regulates c-di-GMP synthesis and biofilm formation. We propose that the synthesis of c-di-GMP by globin sensors is a widespread phenomenon in bacteria.",
keywords = "biofilm, c-di-GMP, diguanylate cyclase, globin, oxygen sensor",
author = "Xuehua Wan and Tuckerman, {Jason R.} and Saito, {Jennifer A.} and Freitas, {Tracey Allen K} and Newhouse, {James S.} and Denery, {Judith R.} and Galperin, {Michael Y.} and Gonzalo Gonzalez and Gilles-Gonzalez, {Marie Alda} and Maqsudul Alam",
year = "2009",
month = "5",
day = "1",
doi = "10.1016/j.jmb.2009.03.015",
language = "English (US)",
volume = "388",
pages = "262--270",
journal = "Journal of Molecular Biology",
issn = "0022-2836",
publisher = "Academic Press Inc.",
number = "2",

}

TY - JOUR

T1 - Globins Synthesize the Second Messenger Bis-(3′-5′)-Cyclic Diguanosine Monophosphate in Bacteria

AU - Wan, Xuehua

AU - Tuckerman, Jason R.

AU - Saito, Jennifer A.

AU - Freitas, Tracey Allen K

AU - Newhouse, James S.

AU - Denery, Judith R.

AU - Galperin, Michael Y.

AU - Gonzalez, Gonzalo

AU - Gilles-Gonzalez, Marie Alda

AU - Alam, Maqsudul

PY - 2009/5/1

Y1 - 2009/5/1

N2 - Globin-coupled sensors are heme-binding signal transducers in Bacteria and Archaea in which an N-terminal globin controls the activity of a variable C-terminal domain. Here, we report that BpeGReg, a globin-coupled diguanylate cyclase from the whooping cough pathogen Bordetella pertussis, synthesizes the second messenger bis-(3′-5′)-cyclic diguanosine monophosphate (c-di-GMP) upon oxygen binding. Expression of BpeGReg in Salmonella typhimurium enhances biofilm formation, while knockout of the BpeGReg gene of B. pertussis results in decreased biofilm formation. These results represent the first identification a signal ligand for any diguanylate cyclase and provide definitive experimental evidence that a globin-coupled sensor regulates c-di-GMP synthesis and biofilm formation. We propose that the synthesis of c-di-GMP by globin sensors is a widespread phenomenon in bacteria.

AB - Globin-coupled sensors are heme-binding signal transducers in Bacteria and Archaea in which an N-terminal globin controls the activity of a variable C-terminal domain. Here, we report that BpeGReg, a globin-coupled diguanylate cyclase from the whooping cough pathogen Bordetella pertussis, synthesizes the second messenger bis-(3′-5′)-cyclic diguanosine monophosphate (c-di-GMP) upon oxygen binding. Expression of BpeGReg in Salmonella typhimurium enhances biofilm formation, while knockout of the BpeGReg gene of B. pertussis results in decreased biofilm formation. These results represent the first identification a signal ligand for any diguanylate cyclase and provide definitive experimental evidence that a globin-coupled sensor regulates c-di-GMP synthesis and biofilm formation. We propose that the synthesis of c-di-GMP by globin sensors is a widespread phenomenon in bacteria.

KW - biofilm

KW - c-di-GMP

KW - diguanylate cyclase

KW - globin

KW - oxygen sensor

UR - http://www.scopus.com/inward/record.url?scp=64449088389&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=64449088389&partnerID=8YFLogxK

U2 - 10.1016/j.jmb.2009.03.015

DO - 10.1016/j.jmb.2009.03.015

M3 - Article

C2 - 19285985

AN - SCOPUS:64449088389

VL - 388

SP - 262

EP - 270

JO - Journal of Molecular Biology

JF - Journal of Molecular Biology

SN - 0022-2836

IS - 2

ER -