Microbe in Marine Sediments Has a High-Fiber Diet

Researchers discovered that marine microbes, Bathyarchaeota, can use inorganic carbon and obtain energy from breaking down lignin, a complex molecule found in wood.

Tiny, single-celled archaea called Bathyarchaeota live in marine sediments all over the world. Scientists know that they’re there because they can detect their DNA. But until recently, researchers could only speculate about the role they might play in the environment based on clues in their genomes.

DCO Deep Life Community members Fengping Wang (Shanghai Jiao Tong University, China), Mark Lever (Aarhus University, Denmark), and Kai-Uwe Hinrichs, (University of Bremen, Germany), and colleagues, have finally discovered a potential function for a subgroup of Bathyarchaeota in marine sediments. In a new paper in Proceedings of the National Academy of Sciences [1], the researchers report that they cultured Bathyarchaeota for the first time in the lab, using sodium bicarbonate (NaHCO3) as a carbon source and lignin, a complex organic polymer that makes up the woody parts of plants, as an energy source. All lignin originates on land, suggesting that this subgroup of Bathyarchaeota is instrumental in breaking down terrestrial carbon compounds that end up in marine sediments. 

Scientists have speculated that Bathyarchaeota, as one of the most abundant organisms on the planet and a common inhabitant of marine sediments, are important actors in the carbon cycle. Based on their genomes, researchers have proposed that they may ferment organic carbon, perform acetogenesis (producing acetate from carbon dioxide and an energy source like hydrogen), or produce or consume methane. But no one had been able to culture the microbes in the lab to confirm their metabolism.

Wang’s group set up enrichment cultures containing a mix of microbes present in marine sediments from the East China Sea and spiked them with different organic compounds to see what kinds of carbon and energy sources might instigate Bathyarchaeota growth. They tried cellulose, phenol, casein, and oleic acid, but only lignin successfully stimulated a subgroup, called Bathy-8. After a 10-month incubation period, the cells had increased tenfold. “Lignin has a very complex structure, so not many organisms can use it. This gives Bathyarchaeota a chance to outcompete the other microbes,” said Wang.

Bathyarcheota figure
The new study suggests that Bathyarchaeota in ocean sediments survive by consuming inorganic carbon and the plant molecule lignin, which washes into the ocean from terrestrial environments. Credit: Fengping Wang

To add further evidence that Bathyarchaeota use lignin, Wang’s group grew their lignin-spiked enrichments with sodium bicarbonate carrying the carbon-13 isotope. This isotope has an extra neutron in the nucleus that can be used as a flag, to track the carbon as it moves through cells in the enrichment experiment. They collaborated with members of Hinrichs’ team, who isolated and analyzed lipids from cell membranes of Bathyarchaeota. Potential bathyarchaeotal lipids contained carbon-13, suggesting that Bathyarchaeota had consumed the flagged inorganic carbon and incorporated it into their cells. The experiment also showed that the microbes perform acetogenesis, transforming inorganic carbon into acetate, as indicated by the buildup of acetate containing carbon-13 in the enrichments.

Along coastlines, terrestrial carbon can account for up to 45% of the carbon in marine sediments, with lignin, which comes from wood and bark, as the main component. The discovery that Bathyarchaeota uses lignin adds another angle to our understanding of terrestrial carbon cycling. As far as Wang is aware, this is the first report of an archaea that can metabolize lignin in marine sediments depleted of oxygen, and there are no known bacteria in this environment that use lignin anaerobically either.
    
Lignin is one of the most abundant biopolymers on Earth, second only to cellulose, and many researchers are exploring ways to transform it into bioenergy. Wang hopes that in the future, the enzymes Bathyarchaeota uses to degrade lignin may help in bioenergy production.

The researchers do not yet have a pure culture of Bathy-8. Next, they hope to refine their cultivation techniques so that they can isolate Bathyarchaeota and further investigate its lignin degradation pathways.

“Right now, the bottleneck is cultivation,” said Wang. “We are in the genomic era. We have so many genomes from different cells and we can assume so many things from the genomes but we need to go beyond that and grow the cells in the lab.”

Ultimately, Wang also wants to recruit modeling experts to incorporate genomic, microbial, and geochemical data from marine sediments to understand how these microbes function within their home environment. “I know there are a lot of challenges,” said Wang, “but I want to push the limits of our understanding of Bathyarchaeota, and perhaps other unknown microbes.” 
 

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