The Divergent AmoC 3 Subunit of Ammonia Monooxygenase Functions as Part of a Stress Response System in Nitrosomonas europaea

Abstract

ABSTRACT The ammonia monooxygenase of chemolithotrophic ammonia-oxidizing bacteria (AOB) catalyzes the first step in ammonia oxidation by converting ammonia to hydroxylamine. The monooxygenase of Nitrosomonas europaea is encoded by two nearly identical operon copies ( amoCAB 1 , 2 ). Several AOB, including N. europaea , also possess a divergent monocistronic copy of amoC ( amoC 3 ) of unknown function. Previous work suggested a possible functional role for amoC 3 as part of the σ E stress response regulon during the recovery of N. europaea from extended ammonia starvation, thus indicating its importance during the exit of cells from starvation. We here used global transcription analysis to show that expression of amoC 3 is part of a general poststarvation cellular response system in N. europaea . We also found that amoC 3 is required for an efficient response to some stress conditions, as deleting this gene impaired growth at elevated temperatures and recovery following starvation under high oxygen tensions. Deletion of the σ 32 global stress response regulator demonstrated that the heat shock regulon plays a significant role in mediating the recovery of N. europaea from starvation. These findings provide the first described phenotype associated with the divergent AmoC 3 subunit which appears to function as a stress-responsive subunit capable of maintaining ammonia oxidation activity under stress conditions. While this study was limited to starvation and heat shock, it is possible that the AmoC 3 subunit may be responsive to other membrane stressors (e.g., solvent or osmotic shocks) that are prevalent in the environments of AOB.