Nicole Dubilier, from the Max-Planck Institute for Marine Microbiology, has spent much of her career studying chemosynthetic microbes and their animal hosts. She has now visited Chapopote and the asphalt volcanoes twice. “When the submersible comes up, it reeks of petroleum, and it’s filthy. We have to clean it with WD-40; it’s the only thing that works,” she says. “It’s shocking that animals can tolerate these conditions.”
In 2006, Dubilier collected two of the yellow mussels that grow on the vents. In their gills, she found not just the usual chemosynthetic microbes, but also a group of bacteria called Cycloclasticus. These are oil-eaters. When the Deepwater Horizon rig exploded in 2010, releasing 750 million liters of crude oil into the Gulf, Cycloclasticus were among the microbes that showed up to digest the slick. Their presence suggested that the mussels could indirectly be digesting the oil and gas that regularly seep out of the volcano fields.
To confirm this idea, Dubilier returned to the site in 2015 and collected more mussels. Her colleague Maxim Rubin-Blum exposed them to naphthalene—a petroleum-derived chemical. And the mussels, to his surprise, did nothing. They were not digesting the naphthalene at all. “Max nearly knocked himself out trying to get the experiments to work,” Dubilier says.
Rubin-Blum worked out what was going on by sequencing the genomes of the mussels’ microbes. When Cycloclasticus grows on oil, independent of the asphalt-volcano mussels, it attacks a group of chemicals called polycyclic aromatic hydrocarbons (PAHs), of which naphthalene is a member. These are usually very hard to break down because they contain tough ring-shaped chemical bonds, but Cycloclasticus has a large toolbox of genes that can tear these bonds apart. (Their name comes from the Greek for “ring” and the Latin for “breaker”.)
But Rubin-Blum found that the Cycloclasticus strains in the mussels have lost these PAH-breaking genes. Instead, they dine on chemicals in oil like ethane, propane, and other alkanes, which are simpler in structure, and take less energy to digest.
“It’s a jaw-dropping finding,” says Mandy Joye from the University of Georgia, who studies the microbes that bloom at oil spills. Those strains were thought to focus on PAHs. But Dubilier found that several of the genes that the mussel-bound microbes use to digest alkanes were also present in the Cycloclasticus strains that showed up at Deepwater Horizon. This suggests that free-living microbes have much broader range of oil-digesting strategies than previously assumed.
In open water, Dubilier thinks that microbes break down alkanes very quickly, forcing Cycloclasticus to focus on the tougher PAHs. But the mussels provide the microbes with a constant supply of alkanes, by continuously pumping oil-contaminated water over their gills. In this cossetted world, with a conveyor belt of snacks and no competitors, Cycloclasticus has effectively become domesticated. It lost the ability to digest PAHs and adapted to a more abundant and considerably easier source of food. “It’s like they’ve evolved to live off cake,” says Dubilier.