Marine ammonia-oxidising archaea and bacteria occupy distinct iron and copper niches

Roxana T Shafiee,Qiong Zhang,Rosalind E M Rickaby,Joseph T Snow,Poppy J Diver

doi:10.1038/s43705-021-00001-7

Abstract

Ammonia oxidation by archaea and bacteria (AOA and AOB), is the first step of nitrification in the oceans. As AOA have an ammonium affinity 200-fold higher than AOB isolates, the chemical niche allowing AOB to persist in the oligotrophic ocean remains unclear. Here we show that marine isolates, Nitrosopumilus maritimus strain SCM1 (AOA) and Nitrosococcus oceani strain C-107 (AOB) have contrasting physiologies in response to the trace metals iron (Fe) and copper (Cu), holding potential implications for their niche separation in the oceans. A greater affinity for unchelated Fe may allow AOB to inhabit shallower, euphotic waters where ammonium supply is high, but competition for Fe is rife. In contrast to AOB, AOA isolates have a greater affinity and toxicity threshold for unchelated Cu providing additional explanation to the greater success of AOA in the marine environment where Cu availability can be highly variable. Using comparative genomics, we predict that the proteomic and metal transport basis giving rise to contrasting physiologies in isolates is widespread across phylogenetically diverse marine AOA and AOB that are not yet available in pure culture. Our results develop the testable hypothesis that ammonia oxidation may be limited by Cu in large tracts of the open ocean and suggest a relatively earlier emergence of AOB than AOA when considered in the context of evolving trace metal availabilities over geologic time.

Highlights

Ammonia-oxidising archaea (AOA) and bacteria (AOB) mediate the first step of nitrification, the stepwise oxidation of ammonium (NH4+) to nitrite (NO2−) and nitrate (NO3−)—the central component of biogeochemical nitrogen cycling
Nitrosococcus oceani C-107 cultures and growth media Polycarbonate culture vessels and culturing apparatus were acid-cleaned in 10% (v/v) TraceMetalTM grade HCl (Fisher Scientific, Loughborough, UK) for 24 (S.A.), S.A. was calculated based on a spherical cell shape and using a radius of 1 μm obtained from SEM imaging (Supplementary Fig. 3), preparing cells using the same protocol as in ref. 23, which is fully outlined in Supplementary Materials
Maximum growth rates in N. oceani between 0.09 and 0.14 pmol L−1 Cu2+ may on the growth of the ammonia-oxidising bacterium, N. oceani appear to result from the expression of a high-affinity Cu uptake strain C-107 with that of the archaeal isolate, N. maritimus strain SCM1 previously published.[21,22]

Summary

Introduction

Ammonia-oxidising archaea (AOA) and bacteria (AOB) mediate the first step of nitrification, the stepwise oxidation of ammonium (NH4+) to nitrite (NO2−) and nitrate (NO3−)—the central component of biogeochemical nitrogen cycling. A third group of aerobic ammonia oxidisers has been identified, mediating complete aerobic ammonia oxidation to nitrate (comammox).[1] AOA widely outnumber their bacterial counterparts in a range of environments including soils,[2] freshwater streams and lakes[3,4,5] and the marine environment.[6,7,8,9,10,11,12] In the oligotrophic open ocean, archaeal amoA genes, an indicator of cell abundance, are up to three orders of magnitude greater than those of AOB,[7,10,11,12,13] hypothesised to be due to the greater affinity of AOA for their shared substrate NH4+.14. We annotated the presence of metal transporter systems to explore whether the genetic basis for the contrasting metal affinities of N

Methods

Results

Conclusion