Life Below Our Feet: Team Discovers Microbes Thriving in Groundwater, Producing Oxygen in the Dark

WOODS HOLE, Mass. – Nearly a third of Earth’s freshwater resources lie in groundwater – much more than in all lakes, rivers and the atmosphere combined, and exceeded only by the frozen water in polar ice caps. Accordingly, about half of humankind depends on groundwater as a source of drinking water.

Despite the global occurrence and essential importance of groundwater, however, knowledge of the organisms that inhabit it, and how they survive, remains thin.

A recent investigation led by microbial ecologist Emil Ruff of the Marine Biological Laboratory (MBL) has discovered that ancient groundwaters harbor not only diverse and active microbial communities, but also unexpectedly large numbers of microbial cells. Strikingly, some of these microbes seem to produce “dark oxygen” (in the absence of sunlight) in such abundance that the oxygen may nourish not only those microbes, but also may leak into the environment and support other oxygen-reliant microbes that can’t produce it themselves. The study is published today in Nature Communications.

“When doing research, it is common to find surprising results; we just still know very little about the cosmos,” said Ruff. “But it is a highlight to find something so utterly unexpected as oxygen that seems to be produced deep beneath our feet in permanent darkness. At first we thought that we had contaminated all our samples, but additional analyses supported a source of the gas within the aquifers.”  

The study investigated 138 groundwater samples drawn from 14 aquifers that lie beneath more than 80,000 square miles of prairie in the province of Alberta, Canada, an area three times the size of Ireland. The aim was to investigate the biogeochemistry and microbial ecology of a broad range of aquifer environments.

“The leakage of dark oxygen into the groundwaters could have very important consequences relevant for climate change research,” said co-author Marc Strous of the University of Calgary. ”We have indications that the microbes use the groundwater oxygen to consume methane, a greenhouse gas. Especially in the province of Alberta, methane is common in groundwaters and may leak out of the ground into the atmosphere. We will now seek to understand if and how much methane these microbes prevent from being emitted.”

Surprisingly, the team found significantly more microbial cells in older groundwater samples than in younger groundwaters, suggesting these ancient groundwaters have evolved over time to provide energy for microbes to grow. This discovery runs counter to prior studies in subsurface ocean and land ecosystems that found microbial cell density commonly decreases as depth increases, presumably due to energy limitations.

“Counting bacterial cells under a microscope requires enormous patience and skill and is rarely done for large numbers of samples,” said Strous. “Yet, when Isabella Hrabe de Angelis joined Dr. Ruff as a project student she did just that, and spent hundreds of hours behind a microscope. It was thanks to this effort that we could show that these groundwaters are actually productive ecosystems, where everybody had expected them to be subsurface ‘deserts,’ generally devoid of nutrients and energy.”

The study included collaborators from University of Calgary, Canada; Max Planck Institute for Chemistry, Mainz, Germany; Woods Hole Oceanographic Institution, and Alberta Environment and Protected Areas, Calgary, Canada.