Iron requirements and uptake strategies of the globally abundant marine ammonia-oxidising archaeon, Nitrosopumilus maritimus strain SCM1

The Thaumarchaeota mediate ammonia oxidation to nitrite and are widespread in the marine environment, constituting up to 40% of the microbial population and dominating marine metatranscriptomes. Light inhibition and poor competitiveness with phytoplankton for ammonium are currently considered to restrict Thaumarchaeota activity to below the photic zone, but observations of ammonia oxidation in surface waters now demand a further understanding of the factors which control Thaumarchaeota distribution and activity. Low concentrations of iron (Fe) limit the growth of microorganisms in a significant portion of the world’s surface oceans, yet there is no examination of the Fe requirements of Thaumarchaeota despite genomic and transcriptomic data implicating a key role for Fe in ammonia oxidation. We investigated the physiological and proteomic response of the thaumarchaeon Nitrosopumilus maritimus strain SCM1 to Fe limitation. We show that SCM1 requires up to 2-orders of magnitude greater concentrations of free inorganic Fe (Fe´) to obtain maximum growth rates compared with numerous marine phytoplankton and heterotrophic bacteria due to both a significant intracellular Fe-quota and a low affinity for Fe´. Proteomic analysis suggests that the high Fe-quota is underpinned by ferredoxin proteins which are among the most abundant proteins in the proteome of SCM1 but which reduce in abundance in response to iron-limitation. We demonstrated that while SCM1 can grow using organically bound Fe as an Fe source, SCM1 has a lower affinity for this substrate compared with other marine microorganisms. The poor competitiveness of SCM1 for environmentally relevant Fe-substrates suggests that AOA may be iron limited in a significant portion of the world’s surface waters but are well suited to their niche at the base of the photic zone where competition for Fe is alleviated, as phytoplankton and heterotrophic bacteria become light and dissolved organic carbon limited, respectively.