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

Abstract

Ammonia-oxidising archaea (AOA) mediate the rate-limiting step of nitrification, the central component of the marine nitrogen cycle that converts ammonia to nitrite then nitrate. Competition with phytoplankton for ammonium and light inhibition are considered to restrict AOA activity to below the photic zone, but observations of surface nitrification now demand a further understanding of the factors driving AOA distribution and activity. Pico- to nanomolar 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 role of Fe in AOA growth despite the process of ammonia oxidation being considered to rely on the micronutrient. Here we investigate the Fe requirements and Fe uptake strategies of the Nitrosopumilus maritimus strain SCM1, a strain representative of globally abundant marine AOA. Using trace metal clean culturing techniques, we found that N. maritimus growth is determined by Fe availability, displaying a free inorganic Fe (Fe′) half saturation constant 1–2 orders of magnitude greater for cell growth than numerous marine phytoplankton and heterotrophic bacterial species driven by a reduced affinity for Fe′. In addition, we discovered that whilst unable to produce siderophores to enhance access to Fe, N. maritimus is able to use the exogenous siderophore desferrioxamine B (DFB), likely through a reductive uptake pathway analogous to that demonstrated in phytoplankton. Our work suggests AOA growth in surface waters may be Fe limited and advances our understanding of AOA physiology on the cellular and mechanistic levels with implications for ecosystem dynamics and the biogeochemical N-cycle.

Changing Biogeochemistry of the Southern Ocean and Its Ecosystem Implications

“…Nitrification is favoured in winter due to low light and reduced competition for ammonium (Olson, 1981;Ward, 2005;Smith et al, 2014). This effect may be augmented by enhanced iron availability (Shafiee et al, 2019) and, south of the Polar Front, by mixed-layer ammonium accumulation (Figure 2d) resulting from an enhanced microbial loop in late summer/autumn (Becquevort et al, 2000;Dennett et al, 2001;Lourey et al, 2003). Currently, the implications of nutrient (re)cycling within the seasonally varying mixed layer for Southern Ocean carbon production and export remain poorly understood.…”

Nitrification and nitrous oxide dynamics in the Southern California Bight

“…Nitrification is often thought to be inhibited by light and to only occur in waters below the euphotic zone (Merbt et al 2012). However, it has also been hypothesized that nitrification is controlled by competition with phytoplankton in the surface ocean for ammonium (; Smith et al 2014; Wan et al 2018) and micronutrients (Shiozaki et al 2016; Shafiee et al 2019) or by top‐down factors such as grazing and viral lysis (Zakem et al 2018). Despite the important implications for understanding the controls on carbon export, the circumstances under which nitrification is important to the euphotic zone N budget remain unclear.…”

Regulated Iron Siderophore Production of the Halophilic Archaeon Haloferax volcanii

“…Only about five publications on siderophores and Archaea exist, not always reporting the ability to produce siderophores. Very recently, it was described that the ammonia-oxidizing archaeon Nitrosopumilus maritimus is unable to produce its own siderophore, but that it can use an exogenous siderophore for iron uptake [6]. Earlier, it was described that five of nine Indian isolates of seven different genera of halophilic Archaea are capable of siderophore production [7].…”