Abstract:
Ammonia-oxidizing archaea (AOA) are one of the most abundant prokaryotes in the ocean and span diverse oceanic provinces. In addition to having a dominant role in marine nitrification, they are implicated as a major source of atmospherically active gases methane and nitrogen oxides. However, the scarcity of cultured isolates for laboratory study has hindered developing an understanding of specific metabolic traits and physicochemical factors controlling their activities and distribution. Three new marine AOA (Nitrosopumilus cobalaminigenes, N. oxyclinae, and N. ureaphilus) were isolated and characterized, and they show distinct adaptations to pH, salinity, temperature, light, and reactive oxygen species relative to the model AOA Nitrosopumilus maritimus. Increases in nitrous oxide (N₂O) production in response to decreasing oxygen (O₂) tensions was quantified and found consistent with an AOA contribution to the accumulation of N₂O in suboxic regions of oxygen minimum zones. Normal growth of N. maritimus was shown to be coupled with balanced production and consumption of nitric oxide (NO). A central role of NO in archaeal ammonia oxidation was confirmed by specific inhibition using an NO-scavenger (2-phenyl-4,4,5,5,-tetramethylimidazoline-1-oxyl-3-oxide). The determination of high cellular quotas of cobalamin now implicates the AOA as major contributors to cobalamin in seawater. Transcriptomics and proteomics studies showed that the entire cobalamin biosynthesis pathway is regulated by the level of nitrosative stress, suggesting that an interplay between NO production and cobalamin synthesis is central to the ecophysiology of marine AOA. Apart from having a major influence on the nitrogen cycle, their glycerol dibiphytanyl glycerol tetraether (GDGT) membrane lipids are widely used to reconstruct past sea surface temperatures by means of TEX₈₆ paleothermometer. However, the TEX₈₆ proxy must now be reevaluated in consideration of the observation that O₂ concentration greatly influences GDGT composition, leading to significant increases in TEX86-derived temperatures with increasing O₂ limitation. Together, these findings highlight an unexpected adaptive capacity of marine AOA and provide new understanding of the physiological, biochemical, and multi-omics basis of their remarkable ecological success in marine systems.