RirA is a global regulator of iron homeostasis in and related α-proteobacteria. In its [4Fe-4S] cluster-bound form it represses iron uptake by binding to IRO Box sequences upstream of RirA-regulated genes. Under low iron and/or aerobic conditions, [4Fe-4S] RirA undergoes cluster conversion/degradation to apo-RirA, which can no longer bind IRO Box sequences. Here, we apply time-resolved mass spectrometry and electron paramagnetic resonance spectroscopy to determine how the RirA cluster senses iron and O. The data indicate that the key iron-sensing step is the O-independent, reversible dissociation of Fe from [4Fe-4S] to form [3Fe-4S]. The dissociation constant for this process was determined as = ~3 µM, which is consistent with the sensing of 'free' iron in the cytoplasm. O-sensing occurs through enhanced cluster degradation under aerobic conditions, via O-mediated oxidation of the [3Fe-4S] intermediate to form [3Fe-4S]. This work provides a detailed mechanistic/functional view of an iron-responsive regulator.
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