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A tight tunable range for Ni(II) sensing and buffering in cells.

Andrew W Foster1,2, Rafael Pernil1,2, Carl J Patterson1,2

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Metal sensor affinities adjust to cellular metal levels. The nickel sensor InrS (in vivo) fine-tunes its affinity to match environmental nickel concentrations, not the other way around.

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Area of Science:

  • Biochemistry
  • Molecular Biology
  • Microbiology

Background:

  • Metal-sensing transcriptional regulators exhibit metal affinities that correlate with cellular metal concentrations across a vast dynamic range (>12 orders of magnitude).
  • Understanding the adaptive mechanisms of these regulators is crucial for comprehending cellular metal homeostasis.

Purpose of the Study:

  • To investigate the cause of the co-variation between metal affinities and cellular metal concentrations.
  • To elucidate the regulatory role of the nickel sensor InrS in cyanobacteria.

Main Methods:

  • Determined the structure of the Ni(II) sensor InrS.
  • Engineered cyanobacteria (Synechocystis PCC 6803) with modified InrS variants controlling Ni(II) transporter gene expression.
  • Assessed nickel sensitivity and accumulation in engineered strains.

Main Results:

  • InrS variants with altered Ni(II) affinities were created, affecting nickel exporter and importer gene transcription.
  • Variant strains showed sensitivity to elevated nickel and increased nickel content, though the magnitude of change was modest relative to affinity shifts.
  • All InrS variants maintained their allosteric mechanism for DNA binding inhibition upon metal binding.
  • In vivo nickel response was only observed when sensor sensitivity was optimized for a narrow concentration range (<2 orders of magnitude).

Conclusions:

  • The Ni(II) affinity of the InrS sensor is attuned to cellular nickel concentrations.
  • This attunement allows for precise regulation within a specific environmental range, rather than InrS dictating cellular metal levels.
  • The findings highlight a sophisticated regulatory strategy for maintaining metal homeostasis in cyanobacteria.