Response of ammonia oxidizing archaea to environmental change and implications for the TEX86 proxy

Nitrification is a critical component of the marine nitrogen cycle and the first step of nitrification is mediated by ammonia oxidizing archaea (AOA). The resilience of AOA past and present is evident in their ubiquitous membrane lipids, glycerol dibiphytanyl glycerol tetraethers (GDGT). The notion that changes in GDGT composition reflected changes in sea surface temperature led to the development of the TEX86 proxy that is used to reconstruct sea surface temperature as far back as the Jurassic. Yet, it is not known if 1) shifts in GDGT composition reflect acclimation by a static community or community change and 2) if AOA adjust GDGTs in response to environmental variables other than temperature. Here we provide compelling evidence that four strains of AOA in pure culture display strain-specific dependence on temperature and oxygen concentration. Oxygen greatly influenced membrane lipid composition, leading to significant increases in TEX86-derived temperatures under oxygen stress. These findings demonstrate that AOA are able to acclimate to change by changing cell envelop architecture but that these changes do not prevent loss of fitness as reflected in their diminished growth rate under non-optimal conditions. Our environmental data from across the North Pacific show taxonomic shifts along environmental gradients in nutrients, temperature and oxygen and that those shifts are accompanied by shifts in GDGTs consistent with laboratory observations. Although the adaptive significance of GDGT compositional changes in response to both temperature and oxygen is unclear, our observations show that AOA likely acclimate and change community composition in response to these variable, with implications for future ocean nitrification and interpretation of archaeal lipid-based paleotemperature proxies, particularly in low-oxygen environments.