A study of a denitrifying alphaproteobacterium from the Arabian Sea and its N-cycling potential in sub-oxic microzones within the upper water column

Abstract

Deoxygenation, the progressive loss of dissolved oxygen, is accelerating under climate change and is a major threat to the World Ocean. Oxygen is not only essential for the health of the oceans, but diminishing concentrations have profound economic and socio-economic consequences that impact on human society and well-being. Low oxygen waters (O2, <30% saturation) represent ~10% of the ocean volume presently and have expanded by a fifth in the last 50 years. Knowledge of the organisms driving nutrient cycling and biological productivity in these regions is key to predicting and potentially mitigating the effects of deoxygenation. This thesis provides a comprehensive study of a model denitrifying alphaproteobacterium, an isolate from the Arabian Sea; the most intense of the three major Oxygen Minimum Zones. Labrenzia sp. strain 5N and its close relatives are present within both oxic and suboxic waters of the Arabian Sea. It is free-living but in surface waters it is also found in association with the major N2-fixer Trichodesmium. By a combination of growth experiments, biochemical profiling, genomics, proteomics and N-tracing, it was established that this bacterium has the metabolic potential for a number of environmentally and climatically important processes. As well as denitrifying in the absence of oxygen, this bacterium is capable of coupled nitrification and aerobic denitrification. Simultaneous respiration of oxygen and nitrogen oxides by organisms like Labrenzia sp. strain 5N suggests that denitrification may be more widespread in the oceans than is accounted for by current ecosystem models. This is of concern because N is an essential element for all marine life. Any increase in the losses of N across the air/sea boundary as deoxygenation progresses will lead to an accelerating decline in ocean productivity. Of further importance, strain 5N produces environmentally significant amounts of the potent greenhouse gas nitrous oxide as the primary end product of aerobic denitrification. As well as its warming potential, nitrous oxide is the most significant trace gas contributing to stratospheric ozone depletion following the withdrawal of chlorofluorocarbons under the Montreal Protocol. Further investigations of the significance of these oxygen-sensitive metabolic processes, and establishing the scale to which they might drive ecosystem change under future oceanic conditions, is essential for climate change mitigation.