Ammonia-oxidizing archaea (AOA) are among the most abundant microorganisms in the ocean, playing a fundamental role in the marine nitrogen cycle. Although temperature and trace metal availability each individually influence the growth and activity of marine AOA, there is still only a very limited understanding of the interactive effects of these two major factors on AOA in the rapidly changing ocean. Here, we show that the iron requirements of the model marine AOA species Nitrosopumilus maritimus SCM1 are highly sensitive to temperature changes. A 5ºC increase in growth temperature reduced SCM1 iron requirements by > 80%, and was associated with a substantial increase in iron use efficiencies (IUE, mol C fixed/hr/mol cellular Fe) under iron-limited and warming conditions. Thermally enhanced IUE thus enables SCM1 to more efficiently utilize scarce available iron supplies to support its growth. Based on comprehensive analysis of whole-cell proteomic responses to iron limitation at various temperatures, our study revealed that the proteomic profiles under iron-limited conditions were noticeably distinct from those observed under iron-replete conditions, and the profiles at 32˚C differed from those at lower temperatures (23 ˚C and 27 ˚C). In particular, the cystathionine β-synthase (CBS) domain and universal stress protein A (UspA) may have a specific function as a high temperature response protein in N. maritimus. The translation of a ferredoxin gene was depressed at growth limiting iron concentrations. In contrast, the expression of a copper-dependent plastocyanin gene was significantly increased in response to iron limitation. The downregulation of ferredoxin and upregulation of plastocyanin were particularly pronounced as growth temperatures increased, suggesting a temperature-dependent regulation mechanism. Together, these findings suggest that marine AOA may be able to leverage current and future elevated temperatures to better adapt to living in widespread iron-depleted regions of the ocean.

ammonia-oxidizing archaea, ocean warming, iron use efficiency, proteomics