Aquifer Microbes Survive on Hydrogen and Carbon Dioxide Diet

Bacteria living on the surface of the mineral olivine inside a deep, subseafloor aquifer rely on the Wood-Ljungdahl pathway, an ancient type of metabolism that uses hydrogen and carbon dioxide to yield energy and organic compounds.

Based on what we know of early Earth and the origin of life, scientists think that the first cells lived in a warm environment fueled by water-rock reactions, such as a hydrothermal vent system, hot spring, or aquifer. The cells likely would have used hydrogen for energy and dissolved carbon dioxide for carbon to build their cells. Similar environments still exist on Earth today, and new research shows that the organisms that inhabit them probably make a living in the same way.

In a new paper in The ISME Journal, DCO researchers report that microbes living on grains of the mineral olivine in a deep, subseafloor aquifer rely on an ancient type of metabolism called the Wood-Ljungdahl pathway, which uses hydrogen and carbon dioxide. Deep Life Community members Amy Smith (Woods Hole Oceanographic Institution, USA), Martin Fisk, Rick Colwell (both at Oregon State University, USA), Olivia Mason (Florida State University, USA), Radu Popa (University of Southern California, Los Angeles, USA), and colleagues, sequenced the DNA from the community of microbes living on the grains and separated them into genomes representing 11 microbial species. The metabolic pathways revealed by the genomes yield insight into carbon cycling in the vast subseafloor aquifer environment, and give hints for what to look for to find life on other watery worlds.

microbes on basalt
Novel microbes grow on a grain of olivine submerged inside a subseafloor aquifer. Credit: Amy Smith

“This one ancient carbon fixation pathway, which we believe was present at the origin of life, was found in most of the organisms in this community, which was really cool,” said Smith.

Smith first encountered these aquifer communities as a masters student at Portland State University, USA. The aquifer in question lies beneath the floor of the Pacific ocean, near the Juan de Fuca Ridge, off the coast of Washington state. It is isolated from the seawater above, and its depth and a thick blanket of overlying sediment keep the aquifer at a toasty 64 degrees Celsius. One of Smith’s committee members, Fisk, invited her to be part of a research cruise to retrieve a flow cell inserted into a borehole in the aquifer four years earlier. The flow cell is a container with individual chambers holding grains of various minerals found in ocean crust, which allows the fluids to flow through the chambers. 

Smith Juan de Fuca
During a 2008 cruise to the Juan de Fuca Ridge, Smith collected microbes that had incubated for four years inside a flow cell inserted up to 287 meters below the seafloor. Credit: Image courtesy of Smith

After bringing the flow cell up to the surface, Smith extracted DNA from the biofilms growing on the different minerals and attempted to grow the organisms in the lab. With support from the Census of Deep Life, she sequenced DNA from the community attached to olivine, a common mineral in basalt rock that erupts to make new ocean crust. Olivine also contains iron, which participates in the water-rock reaction that yields hydrogen. This is one of the first studies to examine the community of organisms on the mineral surfaces, instead of in the fluids, which may be a better reflection of the organisms living in subsurface basalt.

Smith grouped DNA sequences from the whole olivine community into 11 individual genomes, representing eight bacterial and three archaeal species. To see how they lived, she reconstructed the metabolic pathways they could use based on which genes were present in the genomes.

All but one of the bacteria were acetogens, a group that uses the Wood-Ljungdahl pathway to gain energy and organic carbon, while making acetate. Some of the bacterial species also use sulfate to generate energy or consume organic compounds, and one could convert nitrogen into a form usable by the cells. “There were only a handful of acetogens from the seafloor known at all up until this point and now we have seven novel genomes that we’ve obtained from just this one olivine community,” said Smith. “None of the bacteria are closely related to anything we’ve ever seen before.”

Smith acknowledges that the results represent one sample from a single location, but if deep subseafloor aquifers worldwide host similar communities, then these organisms dominate a huge part of the planet. “Since 70 percent of Earth’s surface is ocean crust, we really need to investigate how these organisms are getting energy – not just to understand the carbon cycle, but to understand how life arose on Earth, how organisms use rocks for energy, and how life might exist on other ocean worlds, like Saturn’s moon Enceladus,” said Smith. Finding traces of acetate elsewhere could indicate that life forms are using a pathway similar to the Wood-Ljungdahl pathway.

To learn more about how these acetogens survive now and how they might have lived in the past, Smith is doing a detailed analysis of a single acetogen genome that has no other energy-generating pathways apart from the Wood-Ljungdahl pathway. Eventually she hopes to culture the microbe as well. Smith thinks this organism could be the closest we’ve come to finding a microbe that represents the earliest cells, as well as life that could exist on other planets.

Smith in shipboard lab
Smith processes samples aboard the 2008 cruise to the Juan de Fuca Ridge. Credit: Image courtesy of Smith


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