Prony Bay Chimneys Have Surprising First Inhabitants

At the bottom of Prony Bay by New Caledonia in the Pacific Ocean, lies a field of tall, rocky edifices called chimneys, which form from streams of warm, alkaline fluids that emerge from the seafloor.

These chimneys, and the hydrothermal vent fluids that pour out of them, offer a window into the conditions that exist in recesses in the rocks deep beneath the ocean floor, and into the microbes that survive there, in circumstances that could be close to the habitat that supported the first cells on Earth.

DCO’s Céline Pisapia, Emmanuelle Gérard, and Bénédicte Ménez (all from the Institut de Physique du Globe de Paris, France) and colleagues, examined chimneys in Prony Bay that are still in the process of forming, to identify the first organisms that colonize them. In a new paper in Frontiers in Microbiology, they report the detection of filamentous bacteria, which serve as scaffolding for the chimneys, and likely live on organic compounds present in the vent fluids.

“We were particularly interested in the very young chimneys, the ones that are newly formed,” said senior author Ménez. “There we expected to find microbes that could represent the ones that live at depth within the rocks.”

Prony Bay is a shallow lagoon, which allowed divers to access the chimneys easily and collect rocks from actively venting chimneys of different ages. Researchers used scanning electron microscopy and confocal laser scanning microscopy with probes for specific DNA sequences to see the bacteria within the chimney samples. They observed filamentous bacteria that form long chains, with minerals attaching to them. The filaments appeared to act like iron rebar in concrete, to support the chimney’s growth.

The researchers isolated individual bacterial filaments through laser microdissection. They analyzed the minerals growing on the filaments using X-ray diffraction and found brucite and some hydrotalcite had formed on filaments within the youngest chimney.

Analysis of microbial DNA extracted from the dissected rock samples suggests that the filamentous bacteria belong to the Firmicutes phylum, and are descended from organisms that inhabited an early branch on the tree of life. They also identified sequences from two other bacterial groups known to live in hydrothermal and sub-seafloor environments.

 

 

 

 

 

 

 

 

 

Brucite forms along a bacterial filament. Credit: Provided by Céline Pisapia.

Researchers were surprised to find that these colonizing microbes came from groups that may consume organic carbon compounds for energy, rather than synthesizing their own food from inorganic sources – a process called autotrophy. The fluids that discharge from the hydrothermal vents come from serpentinization reactions that occur between seawater and minerals in the surrounding mantle rocks and are rich in H2. In the presence of CO2, these compounds are the perfect energy and carbon sources for methanogens. But the serpentinization reaction can also produce abiotic organic compounds, whose diversity scientists have not fully explored.

“We expected to find autotrophic microbes that can use inorganic carbon, such as CO2,” said Pisapia. “But in Prony Bay, methanogens, which have this capability, were not the first colonizers. They were only detected once the chimneys matured.”

With their IPGP colleague Emmanuelle Gérard, researchers are now sequencing the genome of single bacterial cells dissected from the chimneys. They hope that the genome will illuminate the metabolic processes that the microbes use to thrive in the Prony Bay chimneys and within pores in rock beneath the bay.

“Maybe autotrophy is not the main or the only way to survive in mantle-derived rocks, because there could be a lot of organic compounds that derive from purely chemical reactions and are available for life,” said Ménez. “We still have to describe the diversity of those compounds and the way they form and that will be one of the goals of our DCO project in the upcoming year.”

Mature and young chimneys forming in the Prony Bay hydrothermal vent field and sampled by divers. Credit:  Courtesy of US IMAGO team at IRD research center in Nouméa (New Caledonia) and Frontiers in Microbiology. 

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