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How oxygen regulates the structure and function of microbial ecosystems

Final Report Summary - OXYGEN (How oxygen regulates the structure and function of microbial ecosystems)

The oxygen project was designed to develop new oxygen-sensing technologies for the determination of oxygen at ultra-low concentrations, and to use these technologies to explore the dynamics of low-oxygen environments in the global ocean and the relationship of microbes and microbial processes to these environments.

Indeed, we feel that we have accomplished nearly all of the objectives that we laid out in our proposal. On the technical side, we were able to develop and implement fluorescent compounds for the detection of oxygen in both the low nano-molar and sub- nanomolar range. By doing so, we have introduced new and robust technologies to the detection of oxygen in low-oxygen environments. Indeed, as part of this development, we have also implemented these new oxygen-sensing technologies into the construction of a portable, in situ measuring device for continuous records of oxygen, conductivity, temperature, pressure, chlorophyll, light, and particle density, in the marine water column.

Overall, we have used these technologies to considerably advance our understanding of the oxygen dynamics in oxygen-minimum zones of the world’s ocean. We have found that oxygen intrusions are common in the very low concentration range, and that these intrusions dramatically influence the microbiology and biogeochemistry of these important regions of the global ocean. We also explored specifically the Bay of Bengal, which had previously been identified as a region with oxygen concentrations below detection, but lacking the biogeochemical features of previously known oxygen-minimum zones. We were able to determine with our new technologies that oxygen, indeed, is present at very low concentrations in the Bay of Bengal. However, despite this, the microbial populations are similar to other more active oxygen minimum zones with the immeasurably low oxygen concentrations. Therefore, we identify the Bay of Bengal as an oxygen-minimum zone at a “tipping point” that could become a major player in controlling the nutrient inventories of the oceans if these last traces of oxygen could be removed.

More broadly, we also explored how oxygen regulates key metabolisms in low-oxygen regions of the global ocean, with predictions as to how further reductions of oxygen content in the oceans might influence global biogeochemistry.

In other technological breakthroughs, we developed incubation systems for exploring the kinetics of oxygen utilization at low-oxygen concentrations, and applied these to obtaining the first-ever measurements of oxygen respiration in low-oxygen marine environments. We have also found that microbes in nature are well adapted to extremely low oxygen concentrations, which gives them a particular advantage in low-oxygen regions of the oceans.

We have also taken our understanding from the modern oceans into the geologic past, and have provided the earliest evidence for oxygen in the Earth’s atmosphere at 3 billion years ago. In a study of rocks from China, we have also provided the first estimate of atmospheric oxygen levels 1.4 billion years ago, and show that they were sufficiently high to support animal respiration, meaning that animals did not evolve in response to increases in oxygen concentration as had previously been thought. Indeed, as part of the Oxygen project, we also, for the first time, explored the oxygen requirements of marine sponges, which can be viewed as analogous to some of the earliest animals evolved.