Iron and copper requirements of the marine ammonia-oxidising bacterium, Nitrosococcus oceani: an examination of the role of trace metals in the niche differentiation and competition between ammonia-oxidising bacteria and archaea

Poppy Diver, Roxana Shafiee, Joseph T Snow and Rosalind E M Rickaby, University of Oxford, Earth Sciences, Oxford, United Kingdom
Ammonia-oxidation to nitrite, the first step of nitrification, is mediated by ammonia-oxidising bacteria and archaea (AOB and AOA). Ammonia-oxidising archaea of the Thaumarchaeota are globally ubiquitous and abundant in the oceans, constituting as much as 40% of the marine microbial population and dominating marine metatranscriptomes. AOA largely outnumber AOB in the oceans and this widespread success is primarily considered to be due to the higher affinity of AOA for ammonium – an often limiting nutrient in the open ocean. In contrast to AOB, which use iron (Fe)-dense cytochromes, AOA utilise a copper (Cu)-based respiratory system which is widely assumed to provide an ecological advantage to AOA as Fe concentrations are typically 1-2 orders of magnitude lower than Cu in the open ocean. However, recent data from culture experiments bring into question whether AOA are better adapted to Fe-poor regions of the oceans relative to AOB: physiological data indicate that AOA exhibit an Fe requirement that exceeds the needs of numerous ecologically significant marine microorganisms by 1-2 orders of magnitude. In order to clarify the role of key trace metal micronutrients in shaping the niche differentiation and competition between AOA and AOB, we examined the Fe and Cu requirements and uptake strategies of the marine AOB Nitrosococcus oceani. Compared with the AOA, Nitrosopumilus maritimus strain SCM1, we found that N. oceani requires a lower Fe concentration to reach its maximum growth rate (µmax), but is unable to utilise the organically complexed Fe substrate desferrioxamine B (FeDFB) and does not adopt a reductive uptake Fe strategy. The ability of SCM1 to acquire Fe using a reductive uptake strategy allows SCM1 to use a range of chelated-Fe substrates, conferring a competitive advantage to AOA over AOB in an ocean where the majority of Fe is organically complexed. In addition, we found that N. oceani is inhibited more by high Cu concentrations compared with SCM1: at 53 pmol L-1 Cu2+, N. oceani shows a 28% decrease from µmax, while SCM1 shows only a 10% decrease from µmax. Open ocean Cu2+ concentrations are typically in the nanomolar range, so the enhanced ability of SCM1 to tolerate high Cu may also make AOA better ecologically suited than AOB to the trace metal conditions of the modern marine environment.