A cytoplasmic chemoreceptor and reactive oxygen species mediate bacterial chemotaxis to copper

Gwennaëlle Louis, Pauline Cherry, Catherine Michaux, Sophie Rahuel-Clermont, Marc Dieu, Françoise Tilquin, Laurens Maertens, Rob Van Houdt, Patricia Renard, Eric Perpete, Jean Yves Matroule

Research outputpeer-review


Chemotaxis is a widespread strategy used by unicellular and multicellular living organisms to maintain their fitness in stressful environments. We previously showed that bacteria can trigger a negative chemotactic response to a copper (Cu)-rich environment. Cu ion toxicity on bacterial cell physiology has been mainly linked to mismetallation events and reactive oxygen species (ROS) production, although the precise role of Cu-generated ROS remains largely debated. Here, using inductively coupled plasma optical emission spectrometry on cell fractionates, we found that the cytoplasmic Cu ion content mirrors variations of the extracellular Cu ion concentration. ROS-sensitive fluorescent probe and biosensor allowed us to show that the increase of cytoplasmic Cu ion content triggers a dose-dependent oxidative stress, which can be abrogated by superoxide dismutase and catalase overexpression. The inhibition of ROS production in the cytoplasm not only improves bacterial growth but also impedes Cu chemotaxis, indicating that ROS derived from cytoplasmic Cu ions mediate the control of bacterial chemotaxis to Cu. We also identified the Cu chemoreceptor McpR, which binds Cu ions with low affinity, suggesting a labile interaction. In addition, we demonstrate that the cysteine 75 and histidine 99 within the McpR sensor domain are key residues in Cu chemotaxis and Cu coordination. Finally, we discovered that in vitro both Cu(I) and Cu(II) ions modulate McpR conformation in a distinct manner. Overall, our study provides mechanistic insights on a redox-based control of Cu chemotaxis, indicating that the cellular redox status can play a key role in bacterial chemotaxis.

Original languageEnglish
Article number105207
Number of pages11
JournalJournal of Biological Chemistry
Issue number10
StatePublished - Oct 2023

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

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