Better Together: Symbiotic Relationships in the Sea

This story begins with a giant worm that lives in one of the most inhospitable places in the planet. A giant, gutless, eyeless worm.

In a historic exploratory voyage in 1977, Dr. Robert Ballard and his team found these majestic giant tube worms (Riftia pachyptila) towering over hydrothermal vents 8,000 feet deep in the sea along the Galápagos Rift . As they approached the seafloor, they noticed it was teeming with gushing black smoker chimneys. Below were 400℃ (752℉) acidic and sulfide-rich fluids spewing from the vents. Above was the relatively oxygen-rich, cooler, ambient seawater. The chemicals the vents release are toxic and released with high pressure, and that deep in the ocean, organic nutrients are scarce.

In these conditions, with extremely high temperatures, high acidity, low oxygen, and low nutrients, the researchers were not expecting to see a lush, diverse marine ecosystem. They were perplexed when they saw, not just living things, but a large community full of creatures of all sizes! Clams and mussels the size of dinner plates were scattered along the base of six-foot high tube worms, which were decorated with bright red plumes. Strange shrimp, squat lobsters, and crabs were seen crawling seamlessly along the seafloor, while eel-like zoarcid fish swam up above, looking for their next meal. How could such a rich community thrive in such a harsh environment?

They Key to Survival in the Deep Ocean

Microbiologist Colleen Cavanaugh had the same question as a first year graduate student at Harvard University in 1980. She was attending a lecture where the curator of worms at the Smithsonian Institution, Meredith L. Jones, was discussing giant tube worms and the mystery behind their survival. Jones had mentioned sulfur crystals found in the tube worm’s specialized organ called the trophosome. She and her colleagues thought this organ helps the worm survive by either breaking down toxins or providing nutrition for its sperm.

Incidentally, Cavanaugh had also recently attended a microbiology lecture, which got her thinking about microbes. From there, she proposed that the key to the trophosome’s function lied with some of its permanent residents: sulfur-eating bacteria. After obtaining a sample of trophosome tissue from Dr. Jones, Cavanaugh went on a quest to find these microscopic beings.

Using a high-powered microscope, Cavanaugh looked inside the trophosome and found small spheres 3-5 microns (thousandths of a millimeter) in diameter that were distinct from the rest of the tissue. She later confirmed that these spheres contained DNA, which meant that they could be bacteria.

Further examining the trophosome, Cavanaugh also found key enzymes involved in digesting sulfur and extracting the carbon from carbon dioxide. This finding further supporting her hypothesis that giant tube worms stay healthy by maintaining a symbiotic relationship with bacteria (meaning they’re two very different species who live in intimate association with one another). These tube worms have a special type of symbiosis with their bacteria called a mutualism, where both organisms benefit.

So, what’s the deal with these worms? Do they really have tiny organisms living in their tissues that help them survive? Humans and other terrestrial animals rely on gut and skin microbes to survive, so why not tube worms?

Giant Tube Worms and Bacteria Depend on Each Other

Bacteria provide giant tube worms with food in exchange for shelter. The bacteria (the “symbiont”) use a process known as chemosynthesis to reap energy from hydrogen sulfide to make organic compounds that the giant worm (the “host”) can eat. Much like how plants and other organisms harness light as an energy source to make sugar through photosynthesis, these bacteria use the electrons from the hydrogen sulfide that spews from the vents (their “food”) and the oxygen from the ambient seawater to create the energy needed to convert CO₂ (inorganic carbon) into a form that the worms and other organisms can eat (organic carbon).

But the worms aren’t the only ones reaping the benefits from this partnership. The tube worms pull their weight by delivering the ingredients for its food directly to the bacteria. Specifically, they use a special type of hemoglobin to bind both oxygen and hydrogen sulfide at the same time and deliver them right to their symbiont. (Don’t try this at home: if you carried sulfur in your blood, you’d be in big trouble.)

The service these tube worms provide helps the bacteria solve a very tough conundrum they have to deal with by living around hydrothermal vents. To make organic carbon from CO₂, these bacteria need both oxygen and sulfur around. But as single-celled organisms, it can be very difficult for them to find these ingredients in the vast, open ocean. So, the tube worms find these compounds for them. These bacteria are like an adult who has cut a deal to move back in with their parents. They get to live in a cozy home (a trophos-home, if you will), and their hosts provide them with all of their groceries. But, to pay rent, these tenants have to cook their hosts’ meals with some of those groceries. Not so bad, ain’t it?

It’s all well and good until the host decides to eat some of the tenants. Indeed, giant tube worms have been found to occasionally digest their bacterial symbionts when they’re staving. But overall, it’s a great deal!

It’s an Open Relationship

Two months after discovering the symbiotic relationship between tube worms and bacteria, Cavanaugh stumbled upon a scientific paper describing another unusual class of animal that lives on the ocean floor in seemingly inhospitable waters: gutless bivalves, like clams and oysters, that thrive in the sulfide-rich muds of eelgrass beds.

To her surprise, Cavanaugh did not find any sulfur crystals leading to the bivalve’s expected sulfur-eating bacterial symbionts. So, Cavanaugh tested for another enzyme that plants and other photosynthetic organisms use to convert carbon dioxide into usable carbon. This one is called RuBisCO. By tracing this enzyme in the bivalves, she identified trillions of chemosynthetic bacteria living in their gills that are almost identical to the ones found in the giant tube worms. Scientists hypothesize that this symbiotic relationship explains how they burrow into the ocean floor: they create Y-shaped tunnels, but they primarily live in the top half of the Y. Scientists think this allows them to have access to the oxygen-rich seawater above as well as the sulfide-rich sediments below. The nutrients are then able to flow over the gills to “feed” the bacteria while the bacteria “feed” the bivalve with organic molecules produced from sulfur. Does that sound familiar?

In all, Cavanaugh found two different marine invertebrates that live in two different sulfide-rich environments, yet have the same symbiotic association with the same chemosynthetic bacteria. She believed this meant that chemosynthetic symbioses are much more common than her predecessors thought. In fact, virtually all marine animals that live around hydrothermal vents survive because of the chemosynthetic bacteria that live in or on their cells.

In fact, within sulfide-rich sediments, scientists have found the same bacteria living in association with a variety of microscopic worms and other organisms. What’s more: scientists have also discovered methane-eating bacteria that serve as symbionts to some marine invertebrates around hydrothermal vents. These bacteria get their energy from methane instead of sulfur.

The Importance of Working Together

Much like plants and other photosynthetic organisms that are the base of food chains in terrestrial and some aquatic environments, chemosynthetic bacteria form the basis of food chains in environments where light is not available. Symbiotic relationships with chemosynthetic bacteria and larger marine animals allow both the host and symbiont to thrive in habitats and live in a way that would not otherwise be possible without their symbiotic partner. They are yet another example in nature that demonstrates the importance of working together.

For more information on chemosynthetic symbioses, take a look at Colleen Cavanaugh’s 20-minute talk for iBiology here. To learn more about the research Cavanaugh’s lab performs at Harvard University, venture over to the Cavanaugh lab website.