The Mussels That Eat Oil

In 2004, a team of geologists discovered something extraordinary while exploring the Gulf of Mexico. They were searching for sites where oil and gas seep out of the ocean floor, but instead, two miles below the ocean’s surface, they found a field of dormant black volcanoes. And unlike typical volcanoes that spew out molten rock, these had once belched asphalt. They looked like they had been fashioned from the same stuff used to pave highways, because that’s exactly what they were. The team named one of them Chapopote after the Nahuatl word for “tar.”*

Even if the volcanoes aren’t erupting any longer, a world of asphalt seems like a particularly inhospitable environment. And yet, the team found that life flourished on the volcanoes. Tubeworms, sea lilies, and corals had embedded themselves among the asphalt. Clams and mussels were thriving among sediments that were slick with oil. Crabs scuttled over them, while fish swam past. Life, as they say, finds a way, even when that way involves growing on tar.

Many of these animals likely flourished by forming partnerships with microbes, which use chemicals like hydrogen sulfide and methane to make their own food. This way of life, known as chemosynthesis, is the oldest on the planet. It allows bacteria to thrive in deep-sea habitats that are untouched by sunlight and choked by toxic chemicals. And it allows animals to colonize those same worlds by relying on the bacteria for their nutrition.  

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.

“It’s all about food,” says Colleen Cavanaugh from Harvard University, who first discovered chemosynthetic microbes in the 1980s. The microbes get a regular delivery of fast food from their hosts, and the mussels live off the byproducts of their partners’ digestive work. “This allows the partners to colonize and thrive in the deep-sea—an otherwise inhospitable environment due to the lack of food.”

Dubilier notes that the mussels she studied on volcanoes evolved from shallow-water relatives around 50 million years ago. And there are more than 50 related species that have all colonized inhospitable environments like hydrothermal vents and asphalt volcanoes by teaming up with microbes. “They’re like Darwin’s finches,” she says.

* The story originally referred to Chapopote as the Aztec word for tar; “Aztec” refers to a group of people, and the language they used was Nahuatl.  We regret the error.