Undersea plumes super-charge carbon cycling, offer potential biotech breakthroughs

The complex and dynamic microbial communities and microbially-mediated processes that occur in the ocean help stabilize the earth's climate. 

Far below the ocean's surface, along the seafloor, hydrothermal vents release heat and chemicals into the deep water that fuel vibrant, breathtaking ecosystems. The microbial communities associated with hydrothermal vents are hot spots of biological production in the deep sea. In shallow waters and terrestrial environments where sunlight is available, plants use photosynthesis to harness energy from sunlight to generate biomass. In contrast, at hydrothermal vents, where sunlight is unavailable, microbes rely on chemosynthesis, a process that relies on energy gradients generated by oxidation reactions to support biomass generation.

In a new research study published in Nature Communications, marine biogeochemists examined these metabolic processes ~2,000 meters deep in the Gulf of California, documenting elevated microbial activity that provides new insights into global biogeochemical cycles and opens up a new frontier for genomic discovery.

At hydrothermal vents, seawater circulates through cracks and fissures in the seafloor and interacts with hot magma beds, heating the seawater and chemically altering it. When these superheated fluids are discharged into the water column, they contain high concentrations of nutrients that fuel incredible biological communities in the deep, dark ocean. In the Gulf of California, high rates of phytoplankton production provide a steady rain of decaying biomass that settles on the seafloor. Through hydrothermal-heating processes, this organic matter is converted to oil, methane, and low molecular weight organic compounds. 

"Super-heated, thermally-altered seawater is discharged at the sea floor as hydrothermal fluids," said Samantha Joye, Regents' Professor and Georgia Athletic Association Distinguished Professor of Arts and Sciences and leader of the research team. "In the Gulf of California, the fluids are more than 330º centigrade, and they are loaded with labile organics, methane and oil components."

The exchange of materials and energy between the sea floor and the overlying water column, known as benthic-pelagic coupling, occurs in all aquatic systems. Typically, the fluids discharged from vents contain inorganic energy sources like ammonium, hydrogen and reduced iron, which fuel chemoautotrophic metabolisms. In the Gulf of California, hydrothermal fluids also contain all kinds of organic compounds – ranging from methanol and acetate to complex petroleum components and methane, which can support heterotrophic metabolisms. The complex cocktail of organic matter injected into the deepwater likely molds and fuels microbial communities there. 

"The idea that heterotrophy – when organisms obtain energy from the oxidation of organic matter – plays a significant role in driving microbial dynamics in plume was not really considered," said Joye. The results presented in the paper contest the widely held presumption that of chemoautotrophic processes dominating plumes. "With such high concentrations of organic metabolites, of course, the microbes are going to feast."

Hot fluids are buoyant and, as they are diluted with seawater, they mix turbulently as they rise. Water column microbes are exposed to the chemical cocktail in the plumes and respond rapidly, doubling their population in minutes. By documenting the transcriptional signature of microbes in the plume, microbiologists can "track" different organisms as they respond and grow. 

"Plume microbes must take advantage of the substrates as they are available," Joye said. "The hydrothermally-derived organic substrates are in effect super-charging carbon cycling."

Joye explained that organic carbon cycling typically happens collaboratively, with multiple microbes involved, especially in the degradation of complex organics like hydrocarbons. "Hydrothermal plumes contain complex organics like oils and low molecular weight compounds like volatile fatty acids and alcohols. Because of how rapidly the source fluids are diluted, the microbes must strike while the iron is hot and consume organic compounds rapidly."

The rapid response of heterotrophs in hydrothermal plumes shifts the thinking about ocean carbon cycling. "These are free-living microbes that are responding very fast and very efficiently to dissolved organic carbon inputs," she said. "This system is truly exceptional; the cocktail of organics that the microbes are exposed to makes plumes a prime target for isolating organisms with unique enzymes and metabolic strategies to degrade organic carbon."

With the latest tools in bioinformatics, organic-rich habitats in the deep-sea is great target for identifying and ultimately isolating microorganisms that can produce biofuels.

"There is clear potential for biotech applications –when you have complex microbial communities that are competing for substrates, you typically see expression of antibiotics and antivirals that could be unique," Joye said.

“Life exists under all sorts of extreme conditions - acidic conditions, super salty conditions, cold and hot temperatures, but we have shown that microbes can thrive in a way no one had observed before," said Andrew Montgomery, UGA doctoral candidate and co-author on the study. "This totally changes our perspective of what is possible in these unique ecosystems and opens the potential for future innovations in biotechnology, with potential to discover microbes capable of degrading oil and other contaminants in novel ways.”

Recently developed tools allow scientists to ask the right questions, pairing bioinformatics with the new findings might open up an incredible frontier in microbial discovery.

The study, "Elevated heterotrophic activity in Guaymas Basin hydrothermal plumes influences deep-sea carbon cycling," was published May 28.

Image: A discharging hydrothermal flange at 2000m water depth in the Southern rift of the Guaymas Basin (Gulf of California). Photo acquired by the remotely operated vehicle SuBastian on expedition #190211 of the Research Vessel Falkor which is operated by the Schmidt Ocean Institute. Photo credit: Schmidt Ocean Institute.