Bacterial cyclic diguanylate signaling networks sense temperature

Henrik Almblad; Trevor E. Randall; Fanny Liu; Katherine Leblanc; Ryan A. Groves; Weerayuth Kittichotirat; Geoffrey L. Winsor; Nicolas Fournier; Emily Au; Julie Groizeleau; Jacquelyn D. Rich; Yuefei Lou; Elise Granton; Laura K. Jennings; Larissa A. Singletary; Tara M.L. Winstone; Nathan M. Good; Roger E. Bumgarner; Michael F. Hynes; Manu Singh; Maria Silvina Stietz; Fiona S.L. Brinkman; Ayush Kumar; Ann Karen Cornelia Brassinga; Matthew R. Parsek; Boo Shan Tseng; Ian A. Lewis; Bryan G. Yipp; Justin L. MacCallum; Joe Jonathan Harrison

doi:10.1038/s41467-021-22176-2

Bacterial cyclic diguanylate signaling networks sense temperature

Henrik Almblad
, Trevor E. Randall
, Fanny Liu
, Katherine Leblanc
, Ryan A. Groves
, Weerayuth Kittichotirat
, Geoffrey L. Winsor
, Nicolas Fournier
, Emily Au
, Julie Groizeleau
, Jacquelyn D. Rich
, Yuefei Lou
, Elise Granton
, Laura K. Jennings
, Larissa A. Singletary
, Tara M.L. Winstone
, Nathan M. Good
, Roger E. Bumgarner
, Michael F. Hynes
, Manu Singh

Maria Silvina Stietz, Fiona S.L. Brinkman, Ayush Kumar, Ann Karen Cornelia Brassinga, Matthew R. Parsek, Boo Shan Tseng, Ian A. Lewis, Bryan G. Yipp, Justin L. MacCallum, Joe Jonathan Harrison

Division of Biological and Biomedical Sciences

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

55 Scopus citations

Abstract

Many bacteria use the second messenger cyclic diguanylate (c-di-GMP) to control motility, biofilm production and virulence. Here, we identify a thermosensory diguanylate cyclase (TdcA) that modulates temperature-dependent motility, biofilm development and virulence in the opportunistic pathogen Pseudomonas aeruginosa. TdcA synthesizes c-di-GMP with catalytic rates that increase more than a hundred-fold over a ten-degree Celsius change. Analyses using protein chimeras indicate that heat-sensing is mediated by a thermosensitive Per-Arnt-SIM (PAS) domain. TdcA homologs are widespread in sequence databases, and a distantly related, heterologously expressed homolog from the Betaproteobacteria order Gallionellales also displayed thermosensitive diguanylate cyclase activity. We propose, therefore, that thermotransduction is a conserved function of c-di-GMP signaling networks, and that thermosensitive catalysis of a second messenger constitutes a mechanism for thermal sensing in bacteria.

Original language	English
Article number	1986
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-22176-2
State	Published - Dec 1 2021

Funding

The authors thank Lynne Howell for providing anti-PelC, anti-PelD, and anti-PslG antibodies. T.E.R. and J.D.R. have been supported by a Queen Elizabeth II Scholarship, and H.A. by an Eyes-High Postdoctoral Scholar Award from the University of Calgary. J. J.H. is supported by the Leader’s Opportunity Fund of the Canada Foundation for Innovation (CFI), and a Project Scheme Grant and Canada Research Chair from the Canadian Institutes for Health Research (CIHR).

Funders	Funder number
R01AI077628
University of Calgary
Canadian Institutes of Health Research
Canada Foundation for Innovation

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Almblad, H., Randall, T. E., Liu, F., Leblanc, K., Groves, R. A., Kittichotirat, W., Winsor, G. L., Fournier, N., Au, E., Groizeleau, J., Rich, J. D., Lou, Y., Granton, E., Jennings, L. K., Singletary, L. A., Winstone, T. M. L., Good, N. M., Bumgarner, R. E., Hynes, M. F., ... Harrison, J. J. (2021). Bacterial cyclic diguanylate signaling networks sense temperature. Nature Communications, 12(1), Article 1986. https://doi.org/10.1038/s41467-021-22176-2

@article{a46042bc3b734b888acfc045cb6252fb,

title = "Bacterial cyclic diguanylate signaling networks sense temperature",

abstract = "Many bacteria use the second messenger cyclic diguanylate (c-di-GMP) to control motility, biofilm production and virulence. Here, we identify a thermosensory diguanylate cyclase (TdcA) that modulates temperature-dependent motility, biofilm development and virulence in the opportunistic pathogen Pseudomonas aeruginosa. TdcA synthesizes c-di-GMP with catalytic rates that increase more than a hundred-fold over a ten-degree Celsius change. Analyses using protein chimeras indicate that heat-sensing is mediated by a thermosensitive Per-Arnt-SIM (PAS) domain. TdcA homologs are widespread in sequence databases, and a distantly related, heterologously expressed homolog from the Betaproteobacteria order Gallionellales also displayed thermosensitive diguanylate cyclase activity. We propose, therefore, that thermotransduction is a conserved function of c-di-GMP signaling networks, and that thermosensitive catalysis of a second messenger constitutes a mechanism for thermal sensing in bacteria.",

author = "Henrik Almblad and Randall, \{Trevor E.\} and Fanny Liu and Katherine Leblanc and Groves, \{Ryan A.\} and Weerayuth Kittichotirat and Winsor, \{Geoffrey L.\} and Nicolas Fournier and Emily Au and Julie Groizeleau and Rich, \{Jacquelyn D.\} and Yuefei Lou and Elise Granton and Jennings, \{Laura K.\} and Singletary, \{Larissa A.\} and Winstone, \{Tara M.L.\} and Good, \{Nathan M.\} and Bumgarner, \{Roger E.\} and Hynes, \{Michael F.\} and Manu Singh and Stietz, \{Maria Silvina\} and Brinkman, \{Fiona S.L.\} and Ayush Kumar and Brassinga, \{Ann Karen Cornelia\} and Parsek, \{Matthew R.\} and Tseng, \{Boo Shan\} and Lewis, \{Ian A.\} and Yipp, \{Bryan G.\} and MacCallum, \{Justin L.\} and Harrison, \{Joe Jonathan\}",

note = "Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

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doi = "10.1038/s41467-021-22176-2",

language = "English",

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Almblad, H, Randall, TE, Liu, F, Leblanc, K, Groves, RA, Kittichotirat, W, Winsor, GL, Fournier, N, Au, E, Groizeleau, J, Rich, JD, Lou, Y, Granton, E, Jennings, LK, Singletary, LA, Winstone, TML, Good, NM, Bumgarner, RE, Hynes, MF, Singh, M, Stietz, MS, Brinkman, FSL, Kumar, A, Brassinga, AKC, Parsek, MR, Tseng, BS, Lewis, IA, Yipp, BG, MacCallum, JL & Harrison, JJ 2021, 'Bacterial cyclic diguanylate signaling networks sense temperature', Nature Communications, vol. 12, no. 1, 1986. https://doi.org/10.1038/s41467-021-22176-2

TY - JOUR

T1 - Bacterial cyclic diguanylate signaling networks sense temperature

AU - Almblad, Henrik

AU - Randall, Trevor E.

AU - Liu, Fanny

AU - Leblanc, Katherine

AU - Groves, Ryan A.

AU - Kittichotirat, Weerayuth

AU - Winsor, Geoffrey L.

AU - Fournier, Nicolas

AU - Au, Emily

AU - Groizeleau, Julie

AU - Rich, Jacquelyn D.

AU - Lou, Yuefei

AU - Granton, Elise

AU - Jennings, Laura K.

AU - Singletary, Larissa A.

AU - Winstone, Tara M.L.

AU - Good, Nathan M.

AU - Bumgarner, Roger E.

AU - Hynes, Michael F.

AU - Singh, Manu

AU - Stietz, Maria Silvina

AU - Brinkman, Fiona S.L.

AU - Kumar, Ayush

AU - Brassinga, Ann Karen Cornelia

AU - Parsek, Matthew R.

AU - Tseng, Boo Shan

AU - Lewis, Ian A.

AU - Yipp, Bryan G.

AU - MacCallum, Justin L.

AU - Harrison, Joe Jonathan

PY - 2021/12/1

Y1 - 2021/12/1

N2 - Many bacteria use the second messenger cyclic diguanylate (c-di-GMP) to control motility, biofilm production and virulence. Here, we identify a thermosensory diguanylate cyclase (TdcA) that modulates temperature-dependent motility, biofilm development and virulence in the opportunistic pathogen Pseudomonas aeruginosa. TdcA synthesizes c-di-GMP with catalytic rates that increase more than a hundred-fold over a ten-degree Celsius change. Analyses using protein chimeras indicate that heat-sensing is mediated by a thermosensitive Per-Arnt-SIM (PAS) domain. TdcA homologs are widespread in sequence databases, and a distantly related, heterologously expressed homolog from the Betaproteobacteria order Gallionellales also displayed thermosensitive diguanylate cyclase activity. We propose, therefore, that thermotransduction is a conserved function of c-di-GMP signaling networks, and that thermosensitive catalysis of a second messenger constitutes a mechanism for thermal sensing in bacteria.

AB - Many bacteria use the second messenger cyclic diguanylate (c-di-GMP) to control motility, biofilm production and virulence. Here, we identify a thermosensory diguanylate cyclase (TdcA) that modulates temperature-dependent motility, biofilm development and virulence in the opportunistic pathogen Pseudomonas aeruginosa. TdcA synthesizes c-di-GMP with catalytic rates that increase more than a hundred-fold over a ten-degree Celsius change. Analyses using protein chimeras indicate that heat-sensing is mediated by a thermosensitive Per-Arnt-SIM (PAS) domain. TdcA homologs are widespread in sequence databases, and a distantly related, heterologously expressed homolog from the Betaproteobacteria order Gallionellales also displayed thermosensitive diguanylate cyclase activity. We propose, therefore, that thermotransduction is a conserved function of c-di-GMP signaling networks, and that thermosensitive catalysis of a second messenger constitutes a mechanism for thermal sensing in bacteria.

UR - https://www.scopus.com/pages/publications/85103745747

U2 - 10.1038/s41467-021-22176-2

DO - 10.1038/s41467-021-22176-2

M3 - Article

C2 - 33790266

AN - SCOPUS:85103745747

SN - 2041-1723

VL - 12

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 1986

ER -

Bacterial cyclic diguanylate signaling networks sense temperature

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