Sulfur and Nitrogen Metabolism Critical in Deep Continental Ecosystems

Buried in Earth’s crust, in cracks and crevices kilometers below the surface, is a complex ecosystem of microbes and viruses. This ecological niche is challenging, and the organisms populating the deep biosphere must survive in the absence of sunlight, on extremely limited resources.

A new study published in the Proceedings of the National Academy of Sciences by a team of researchers including several DCO scientists and led by Maggie Lau (Princeton University, USA) takes a look at this ecosystem, and investigates how microbes work together to survive [1].

The team took samples of water from a mine in the Witwatersrand Basin in South Africa, 1.3km deep underground. This water, trapped for tens of thousands to millions of years in narrow cracks in the rocks called fractures, contains microbes. The fracture fluid, therefore, is a snapshot of life in the deep, containing the microbes themselves as well as their food and waste products.

“As we started analyzing the samples we noticed something peculiar,” said lead author Maggie Lau (Princeton University, USA). “With the high level of methane in the fracture fluid, we expected to see lots of methanogens, microbes that feed on geologically-produced hydrogen and produce methane. But, these microbes were only about 2% of the studied community. Either they were working extremely hard to produce methane for the entire ecosystem, which seemed unlikely, or we were missing a key piece of the puzzle.”

Lau and her colleagues analyzed DNA, RNA, and protein in the fracture fluids. These biological molecules are important markers for metabolic processes, and hold information about the types of organisms in a sample and how they generate energy and biomass. In the Witwatersrand fracture fluids, Lau et al. noticed a large population of bacteria producing the enzymes necessary for getting energy from nitrate and reduced sulfur, a process that has previously gone unrecognized in the deep.

They also performed analyses to look for chemical hints of this type of metabolism in the fracture fluids. They found that while there were geochemical signs of denitrification and sulfur oxidation, nitrate and sulfide were measured at micro-molar level. This low concentration may be sufficient to support microbial life but seemingly not high enough to constitute an important energy source. Thus, observing a high percentage of bacteria that utilize nitrate and sulfide was something of a surprise.

“We realized that the microbes in this deep biosphere are working together to drive the metabolism of the community, rather than just working individually,” said Lau. “We refer to this metabolic cooperation as syntrophy. One microbe creates metabolic “wastes” that are actually the food for another, the next microbe in the chain, which not only remove these waste molecules from the system that would slow growth of the first microbe but also turn them into food for the first microbe. Thus, by working together in recycling metabolites, both microbes benefit, increasing the fitness of the community as a whole."

The authors also note the metabolic diversity present in the ecosystem’s inhabitants. They suggest that the ability of the inhabitants to shift with the availability of substrates over time is key to survival and the overall stability of the ecosystem.

“It’s exciting to find that this large portion of the deep ecosystem is flourishing indirectly through the small number of methanogens,” added Lau. “This is unexpected, and may change how we look for life, whether extinct or extant, on other planets and moons.”

Images: Top left: Maggie Lau and Olukayode Kuloyo collecting gas samples at Beatrix Gold Mine, South Africa. Credit: Maggie Lau. Middle: Maggie Lau (on the ladder) adjusting water flow while Rachel Harris sets up a filtration system for capturing cells. Credit: Rachel L. Harris. 

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