The Archaea Are Winning in Deep-Sea, Oxic Subsurface Sediments

Highly efficient archaea, called Thaumarchaea, out-survive bacteria in the energy-poor, oxygen-containing sediments beneath the deep sea. These Thaumarchaea consume bits of proteins from dead cells to build their own biomass and also to obtain energy.

Archaea and bacteria may look very similar under the microscope, but organisms from these two different domains of life have important physiological differences that affect where and how they live. We know much more about bacteria living on the surface world, compared to archaea, but a new study finds that in deep, oxic marine sediments, a type of archaea belonging to the Thaumarchaea dominate. In these oxygen-containing layers of muck, with little food or energy, they have outnumbered bacteria for millions of years.

In a new paper in Science Advances, Aurèle Vuillemin and William Orsi (both at Ludwig-Maximilians-Universität München, Germany) with DCO Deep Life Community members Emily Estes (University of Delaware, USA), Robert Pockalny, and Steven D’Hondt (both at University of Rhode Island, USA), and additional colleagues, report that Thaumarchaea outcompete bacteria in oxic sediments, likely by using a clever metabolic trick. The researchers studied the abundance and diversity of microbes in sediments below the North Atlantic Ocean. They discovered that Thaumarchaea survive for so long by being highly efficient and by wringing more energy from the bits of dead cells that they consume, compared to bacteria. Their findings show that Thaumarchaea play important roles in cycling carbon and nitrogen in this especially large, deep ecosystem. 

“The area of the seafloor with oxic sediments is really big,” said Orsi. “Modeling suggests that between 10 and 40 percent of the ocean seafloor is oxygenated all the way through the sediments down to the underlying crust. This is a huge region of the seafloor that is essentially unknown in terms of the deep biosphere.” 

ammonia-oxidizing Thaumarchaea
The ammonia-oxidizing Thaumarchaea take in pieces of proteins from necromass to build their cells and obtain energy. The dual benefit they gain from the necromass coupled with their highly efficient metabolic pathways help these archaea to outcompete bacteria in oxic sediments. Credit: Vuillemin et al.

In seafloor sediments near continents, runoff from land delivers a major payload of organic carbon. Microbes in the sediments quickly devour this carbon and use up all the available oxygen in the process, resulting in sediments that are oxygen-depleted just below the surface. But under the open ocean, a sprinkling of detritus and dead cells are the only food sources that settle on the seafloor, and so oxygen persists throughout the sediments. Previous studies have shown that microbes live in oxic sediments and do consume small amounts of oxygen, but due to the difficulties of extracting sediment samples from thousands of meters beneath the sea surface, scientists know little about their identity or how they survive with so little food or energy.

To find out what is living in these vast, oxic sediments, the researchers teamed up in 2014 for Expedition KN223 on the research vessel Knorr to the Sargasso Sea in the North Atlantic. Members of the expedition, led by Richard Murray (Boston University, USA), Arthur Spivack (University of Rhode Island), and Pockalny, cored 30 meters into the seafloor, which was about 5500 meters beneath the ocean’s surface, reaching 15 million-year-old layers of sediment.  

R/V Knorr
Researchers traveled on the R/V Knorr to collect sediment samples from beneath the Sargasso Sea. Credit: Maximiliano Amenabar

 Back in the lab, the researchers quantified the number of archaea and bacteria at each depth and used DNA sequencing to identify the types of microbes present. “We made a startling discovery,” said Orsi. “Archaea were way more abundant than bacteria, specifically a group called ammonia-oxidizing Thaumarchaea.” 

The researchers learned more about what metabolic pathways these ammonia-oxidizing Thaumarchaea possess by sequencing metagenomes (that is, all of the DNA from microbes present at different sediment depths). They found that the Thaumarchaea have an incredibly efficient pathway for taking in inorganic carbon and “fixing” it into organic carbon for use in the cell.
 
These ultimate bottom feeders also take in bits of degraded proteins and dead cells, called necromass, to build their cellular structures. Additionally, they clip off ammonia (NH4+) from pieces of proteins, oxidize it, and turn it into nitrite (NO2-), which is an additional chemical reaction that provides energy for the cell. “It’s a perfect metabolism if you’re living under constant energy starvation,” said Orsi.   

The process of clipping ammonia off of proteins is called deamination and many microbes can do it, but the unique ability of the Thaumarchaeota to capture additional energy from the ammonia is what helps them outcompete bacteria for such long timescales. As D’Hondt said, “It’s a fine line between deamination and de-animation.” He suspects that their efficient carbon fixation pathway combined with the extra energy gained from oxidizing ammonia allow the Thaumarchaea to dominate in these sediments, because bacteria living there do not have this ability. 

The experiments suggest that Thaumarchaea turn inorganic carbon into biomass in these deep-sea oxic sediments. This is the first time that scientists have demonstrated the importance of this type of metabolism in this environment.

Currently, Orsi, Vuillemin, and their collaborators are studying the microbial communities from nearby sediments that are similarly food- and energy-poor, but lack oxygen. They want to compare the makeup and metabolic strategies of the two communities, and see how the lack of oxygen affects the competition between different groups of bacteria with the archaea

“We should give some credit to archaea and open our minds to the true extent of what they’re capable of, because apparently in oxic sediments they’re able to outcompete bacteria for millions of years,” said Orsi. “This may also be true of other subsurface environments.”

Group on Knorr
Researchers aboard the R/V Knorr include (left to right) Richard Murray (Boston University, USA), Arthur Spivack, Robert Pockalny (both at University of Rhode Island, USA), Steve Hovan (Indiana University of Pennsylvania, USA), and David Smith (University of Rhode Island, USA).  Credit: Christopher Griner

Main image: The crew collected sediment cores reaching 30 meters beneath the seafloor, which represents about 15 million years of sedimentation. Credit: Christopher Griner

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