Nitrogen powering life in an active serpentinising system - an analogue to early life on Earth

How did life begin on Earth? While disagreements remain, one thing for certain is that the first life needed water, a source of energy and non-biologically made organic compounds; and the best candidate for the first life was a microbe. To find these on early Earth, the best place to look would be where water met unreacted rocks from the Earth's interior. Mantle rocks called peridotites, normally residing >6 km below the seafloor or 40 km below land surface, could be brought to surface by overthrust along plate boundaries due to plate tectonics. These peridotites are a reservoir of reduced metallic components, especially iron, which react with water when exposed to form gaseous hydrogen (H2). This then triggers a series of spontaneous reactions that release energy and turn carbon dioxide (CO2) into bicarbonate and methane (CH4), and other simple organic compounds. These reactions, collectively known as 'serpentinisation', thus provide the ideal setting for the emergence of life. Today, these occur in low-temperature hydrothermal systems on the seafloor, or in 'ophiolites', ancient ocean crust and upper mantle that got uplifted on land such as that found in the Sultanate of Oman. These are likely the best modern analogues of the first cradle of life. Many studies have been conducted to date using these systems to try to understand how the biosphere has been evolving on Earth and perhaps on other planets.

Missing in all these investigations, however, is the source of nitrogen (N), the key element used to make DNA, enzymes and proteins. Biological growth in many ecosystems today is limited by the availability of N. Although substantial amounts of N have been present in the atmosphere as gaseous N2 since early Earth, for life to use this N the strong triple bond of N2 has to be broken, and it takes considerable energy. N could also have come as nitrite (NO2) and nitrate (NO3), but both first had to be made by lightning from atmospheric N2, and then rained into the ocean before coming in contact with exposed mantle peridotites. Recently, rock analyses have found that ammonium (NH4+) sometimes replaces certain metals (e.g. potassium) in minerals such that the solid Earth holds ~7 times the N as the atmosphere. Hence, if life can tap into this immense N source, the early biosphere would not be N-limited.

On the other hand, N can exist in several forms of varying electrochemical potentials, and so its many transformations can occur spontaneously with other chemicals to generate energy to support life. Most notably, NO3 is the first-choice alternative used for breathing (respiration) when oxygen runs out, thereby burning 'food' (organic carbon) into CO2 to obtain the necessary energy for life metabolisms. Meanwhile, some microbes may harness the energy from the reactions between NO2 and NH4+ or CH4 to make their own food from CO2, akin to plants performing photosynthesis but with chemical energy instead of sunlight. Therefore, as various N-forms are present in modern subsurface serpentinising systems, various N-transformations may occur to power the microbiome within. The activities of these reactions and their impacts on the environment have never been assessed, nonetheless.

This project seeks to examine how subsurface biosphere acquires N, and how subsurface N-cycling operates and interacts with the subsurface biosphere in a serpentinising system. We will use the rare heavy form of N -15N- to track N-transformations by microbes, and 15N-content in rocks and fluids as tracers, combined with state-of-the-art bioimaging and gene expression, to assess how microbes obtain their cellular N, and to what extent N-transformations are 'actively' powering subsurface life. We will use the Oman ophiolite, the world's largest, best exposed block of oceanic crust and upper mantle as a model active serpentinising system, given its easy access and the newly drilled deep boreholes and drill cores made available by the Oman Drilling Project.