Ecophysiology of marine ammonia-oxidizing archaea

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. In this thesis, I report the isolation and characterization of three new marine AOA (strains HCA1, HCE1, and PS0) and show distinct adaptations to pH, salinity, temperature, light, and reactive oxygen species relative to the model AOA Nitrosopumilus maritimus strain SCM1. 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 strain SCM1 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. Gene expression 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.