INT-02 Marine Nitrogen Cycle
Long-term ammonia starvation response of Nitrosopumilus maritimus SCM1 reveals survival strategies of marine ammonia-oxidizing archaea in oligotrophic environments
Lei Hou* , State Key Laboratory of Marine Environmental Science, Xiamen University, 361101 Xiamen, China; Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019, USA
Rachel A. Lundeen, School of Oceanography, University of Washington, Seattle, WA 98195, USA
Laura T. Carlson, School of Oceanography, University of Washington, Seattle, WA 98195, USA
Yao Zhang, State Key Laboratory of Marine Environmental Science, Xiamen University, 361101 Xiamen, China
David A. Stahl, Department of Civil and Environmental Engineering, University of Washington, Seattle, WA 98195, USA
Anitra E. Ingalls, School of Oceanography, University of Washington, Seattle, WA 98195, USA
Wei Qin, Department of Microbiology and Plant Biology and Institute for Environmental Genomics, University of Oklahoma, Norman, OK 73019, USA

Ammonia-oxidizing archaea (AOA), one of the most abundant and ubiquitous groups of microorganisms in marine environments, play a significant role in global nitrogen and carbon cycles. Marine AOA have an unusually high affinity for ammonia and are recognized to control ammonia oxidation to nitrite in oligotrophic coastal and oceanic ecosystems. Likewise, marine AOA make important contributions to carbon fixation, potent greenhouse gas N2O emission, and essential cofactor cobalamin (vitamin B12) provision in the ocean. However, the survival strategies of marine AOA in response to the long-term nutrient deficiency remain largely unclear. We therefore combined proteomic and metabolomic analyses to characterize the response of a model AOA, Nitrosopumilus maritimus strain SCM1, to short-term (1 day) and long-term (up to 7 days) ammonia starvation. The abundance of most ribosomal proteins was significantly downregulated upon ammonia depletion and continuously declined following extended starvation period, indicating a general reduction in translation activity during energy starvation. Carbon fixation pathway intermediates and glutamine levels were substantially decreased in ammonia-starved cells, reflecting lower carbon and nitrogen assimilatory activities during ammonia starvation. Notably, PII proteins were significantly upregulated in response to ammonia deficiency, suggesting they may function in modulating the uptake of ammonia under starvation. The abundance of entire cobalamin biosynthetic pathway enzymes significantly increased upon ammonia starvation. We also found the significant upregulation of the B12-dependent methionine synthase (MetH) and S-adenosylmethionine (SAM) synthetase under ammonia starvation. This is consistent with the increased cellular SAM levels detected in ammonia-starved cells. High SAM levels has also been reported for other microorganisms under cobalamin-replete conditions, suggesting SCM1 invest significant biosynthetic capacity in cobalamin production under ammonia starvation. Overall, the translational response and metabolite pool changes in SCM1 provide new insights into the metabolic consequence of ammonia starvation in marine AOA and inform diagnostic features of physiological states of environmental populations.