Entrainment of the Circadian Clock of the Enteric Bacterium Klebsiella aerogenes by Temperature Cycles

Jiffin K. Paulose; Charles V. Cassone; Kinga B. Graniczkowska; Vincent M. Cassone

doi:10.1016/j.isci.2019.09.007

Entrainment of the Circadian Clock of the Enteric Bacterium Klebsiella aerogenes by Temperature Cycles

Jiffin K. Paulose, Charles V. Cassone, Kinga B. Graniczkowska, Vincent M. Cassone

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

26 Scopus citations

Abstract

The gastrointestinal bacterium Klebsiella (née Enterobacter) aerogenes expresses an endogenously generated, temperature-compensated circadian rhythm in swarming motility. We hypothesized that this rhythm may be synchronized/entrained in vivo by body temperature (T_B). To determine entrainment, cultures expressing bioluminescence were exposed to temperature cycles of 1°C (35°C–36°C) or 3°C (34°C–37°C) in amplitude at periods (T-cycles) of T = 22, T = 24, or T = 28 h. Bacteria entrained to all T-cycles at both amplitudes and with stable phase relationships. A high-amplitude phase response curve (PRC) in response to 1-h pulses of 3°C temperature spike (34°C–37°C) at different circadian phases was constructed, revealing a Type-0 phase resetting paradigm. Furthermore, real-time bioluminescence imaging revealed a spatiotemporal pattern to the circadian rhythm. These data are consistent with the hypothesis that the K. aerogenes circadian clock entrains to its host via detection of and phase shifting to the daily pattern of T_B.

Original language	English
Pages (from-to)	1202-1213
Number of pages	12
Journal	iScience
Volume	19
DOIs	https://doi.org/10.1016/j.isci.2019.09.007
State	Published - Sep 27 2019

Bibliographical note

Funding Information:
The Cassone lab is supported by NIH R01 GM118541 , HHMI Sustaining Excellence Award 52008116, and KSEF-3783-020 . The authors would like to thank Clifford Harpole for helpful discussion during the course of this research.

Publisher Copyright:
© 2019 The Author(s)

Keywords

Biological Sciences
Chronobiology
Microbiology

ASJC Scopus subject areas

General

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10.1016/j.isci.2019.09.007

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title = "Entrainment of the Circadian Clock of the Enteric Bacterium Klebsiella aerogenes by Temperature Cycles",

abstract = "The gastrointestinal bacterium Klebsiella (n{\'e}e Enterobacter) aerogenes expresses an endogenously generated, temperature-compensated circadian rhythm in swarming motility. We hypothesized that this rhythm may be synchronized/entrained in vivo by body temperature (TB). To determine entrainment, cultures expressing bioluminescence were exposed to temperature cycles of 1°C (35°C–36°C) or 3°C (34°C–37°C) in amplitude at periods (T-cycles) of T = 22, T = 24, or T = 28 h. Bacteria entrained to all T-cycles at both amplitudes and with stable phase relationships. A high-amplitude phase response curve (PRC) in response to 1-h pulses of 3°C temperature spike (34°C–37°C) at different circadian phases was constructed, revealing a Type-0 phase resetting paradigm. Furthermore, real-time bioluminescence imaging revealed a spatiotemporal pattern to the circadian rhythm. These data are consistent with the hypothesis that the K. aerogenes circadian clock entrains to its host via detection of and phase shifting to the daily pattern of TB.",

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author = "Paulose, {Jiffin K.} and Cassone, {Charles V.} and Graniczkowska, {Kinga B.} and Cassone, {Vincent M.}",

note = "Funding Information: The Cassone lab is supported by NIH R01 GM118541 , HHMI Sustaining Excellence Award 52008116, and KSEF-3783-020 . The authors would like to thank Clifford Harpole for helpful discussion during the course of this research. Publisher Copyright: {\textcopyright} 2019 The Author(s)",

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AU - Graniczkowska, Kinga B.

AU - Cassone, Vincent M.

N1 - Funding Information: The Cassone lab is supported by NIH R01 GM118541 , HHMI Sustaining Excellence Award 52008116, and KSEF-3783-020 . The authors would like to thank Clifford Harpole for helpful discussion during the course of this research. Publisher Copyright: © 2019 The Author(s)

PY - 2019/9/27

Y1 - 2019/9/27

N2 - The gastrointestinal bacterium Klebsiella (née Enterobacter) aerogenes expresses an endogenously generated, temperature-compensated circadian rhythm in swarming motility. We hypothesized that this rhythm may be synchronized/entrained in vivo by body temperature (TB). To determine entrainment, cultures expressing bioluminescence were exposed to temperature cycles of 1°C (35°C–36°C) or 3°C (34°C–37°C) in amplitude at periods (T-cycles) of T = 22, T = 24, or T = 28 h. Bacteria entrained to all T-cycles at both amplitudes and with stable phase relationships. A high-amplitude phase response curve (PRC) in response to 1-h pulses of 3°C temperature spike (34°C–37°C) at different circadian phases was constructed, revealing a Type-0 phase resetting paradigm. Furthermore, real-time bioluminescence imaging revealed a spatiotemporal pattern to the circadian rhythm. These data are consistent with the hypothesis that the K. aerogenes circadian clock entrains to its host via detection of and phase shifting to the daily pattern of TB.

AB - The gastrointestinal bacterium Klebsiella (née Enterobacter) aerogenes expresses an endogenously generated, temperature-compensated circadian rhythm in swarming motility. We hypothesized that this rhythm may be synchronized/entrained in vivo by body temperature (TB). To determine entrainment, cultures expressing bioluminescence were exposed to temperature cycles of 1°C (35°C–36°C) or 3°C (34°C–37°C) in amplitude at periods (T-cycles) of T = 22, T = 24, or T = 28 h. Bacteria entrained to all T-cycles at both amplitudes and with stable phase relationships. A high-amplitude phase response curve (PRC) in response to 1-h pulses of 3°C temperature spike (34°C–37°C) at different circadian phases was constructed, revealing a Type-0 phase resetting paradigm. Furthermore, real-time bioluminescence imaging revealed a spatiotemporal pattern to the circadian rhythm. These data are consistent with the hypothesis that the K. aerogenes circadian clock entrains to its host via detection of and phase shifting to the daily pattern of TB.

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Entrainment of the Circadian Clock of the Enteric Bacterium Klebsiella aerogenes by Temperature Cycles

Abstract

Bibliographical note

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