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A FEW years ago, as my bride and I sat finishing our wedding breakfast, I sipped my champagne, oblivious to what was sitting on the white linen-clad table in front of me. I certainly never imagined they would shape my research.

Although we were getting married in the UK, my roots lie in the Bahamas. My wife had asked my parents to bring over shells to decorate the tables. Some of them caught the eye of my PhD supervisor, Crispin Little. “Nick, these are all lucinid shells,” he said. I picked one up from the table in front of me. “Huh,” I exclaimed, “so they are.”

Lucinid clams are unusual because they get part or all of their food from symbiotic bacteria living in their gills. What’s really extraordinary, though, is how the bacteria get the energy they need to create this food: not from sunlight, as plants do, but from simple chemicals found in their surroundings – a process called chemosynthesis.

This process is what allows spectacular oases of life to thrive at hydrothermal vents deep beneath the sea’s surface. What’s less well known is that, far from being limited to the deep vents, animals that rely on chemosynthetic bacteria have turned up in all kinds of places.

Those lucinid clams are common in the shallow waters of the Bahamas, for instance – I grew up collecting their shells on the beach, but never realised what they fed on. Now I’m trying to find out what feeds on them to see how big a role they play in the local ecosystem. Recent discoveries by other researchers suggest chemosynthesis is far more important than anyone imagined.

“Chemosynthesis is far more widespread and important than we thought”

In 1977, the discovery of giant gutless worms thriving in vast numbers around hydrothermal vents stunned scientists. What did they feed on, where no light can penetrate and little food sinks down from above? It was Colleen Cavanaugh, now at Harvard University, who proposed that they get their energy from the hydrogen sulphide produced by the vents, with the help of chemosynthetic bacteria housed in special organs. In the absence of light, the bacteria use hydrogen sulphide in a reaction to produce “dark carbon”. By 1983, Cavanaugh had shown that vent worms do indeed feed on this dark carbon.

In the same year, similarly rich oases of life were discovered around methane seeps on the sea floor, again thanks to chemosynthetic bacteria. But hydrogen sulphide and methane aren’t found only in vents and seeps – they are also produced wherever organic matter decomposes in low-oxygen conditions. In other words, the raw materials for chemosynthesis can be produced by living creatures breaking down food formed by photosynthesis as well as by processes that do not involve life.

Whatever the source of these chemicals, exploiting them usually requires oxygen (see “Do aliens eat dark carbon?“). This means, Cavanaugh and others realised, that chemosynthetic microbes can thrive wherever there is a boundary between an oxygen-poor environment rich in organic matter and an oxygen-rich environment, from rotting whale carcasses in the deep sea to the mud at the bottom of garden ponds.

These microbes are common and often form partnerships with animals. From the early 1980s onwards, biologists began to discover chemosynthetic symbioses in a wide range of invertebrates, from tiny nematode worms and sponges to giant clams, living everywhere from mangrove swamps to the deep sea. These animals shelter the bacteria and help them get the chemicals they feed on and, in turn, the bacteria supply them with food. Many depend so much on the bacteria that their guts are underdeveloped or absent.

“They have been found in everything from tiny worms to sponges and giant clams”

Bivalve molluscs are particularly likely to partner with chemosynthetic bacteria. John Taylor, a mollusc specialist at the Natural History Museum in London, estimates that there are hundreds of chemosymbiotic bivalve species, from at least six families. They have evolved symbioses with various kinds of chemosynthetic bacteria on many occasions.

While there has been much interest in how these symbioses work, the assumption has been that chemosynthesis plays only a very minor role in shallow marine ecosystems. That assumption is turning out to be wrong.

Take the 2 million red knot birds that migrate from Siberia to an area of intertidal mudflats and seagrass beds in Mauritania, western Africa, called the Banc d’Arguin. Quite what all these birds feed on had been a bit of a puzzle. The answer turns out to be lucinid clams. Jan van Gils and Matthijs van der Geest, while working at the Royal Netherlands Institute for Sea Research, that the vast flocks of red knots get half of their food from lucinid clams. The bacteria in the lucinids recycle energy from rotting seagrass that would otherwise be buried in sediments, greatly increasing the population the ecosystem can support (see diagram).

Recycling energy

This isn’t the only example of plant debris being recycled by chemosynthesis. Rivers wash vast quantities of plant material into the sea, but it has been assumed that little entered marine food webs. Then, in 2009, Martin Attrill and his colleagues at Plymouth University Marine Institute in the UK showed that marine relatives of earthworms, called oligochaete worms, can consume this organic matter and pass it up the food chain to the birds and fish that feed on them.

More recently, Nicole Dubilier and her colleagues at the Max Planck Institute for Marine Microbiology in Bremen, Germany, found that these worms have . In fact, the bacteria are exactly the same as those associated with shrimps, crabs and snails at deep-sea hydrothermal vents. It still isn’t clear what the worms gain from the bacteria, but the suspicion is that they help the worms take advantage of the abundance of terrestrial matter that washes into the estuaries.

Around New Zealand, chemosynthesis plays a big role. Here, rivers wash forest litter into fjords, producing sediment very rich in organic material. Dense white mats of free-living chemosynthetic bacteria cover large patches of seabed, and chemosymbiotic clams dominate the animal community. by Stephen Wing and Rebecca McLeod at the University of Otago in Dunedin show that at depths of around 50 metres, chemosynthesis is the main food source for these communities, which in turn feed local fish such as blue cod and common wrasse, lobsters and sea urchins.

As well as providing food for innumerable marine animals, chemosymbiotic animals can be a valuable food source for us. Near Tinharé Island on Brazil’s Bahia coast, for instance, local people harvest lucinid clams from mangrove swamps to eat and to sell to restaurants. The raw flesh is apparently quite tasty, but the gills that house the chemosynthetic bacteria are bitter. Clams like the tiger lucinid are also eaten throughout the Caribbean, a tradition that goes all the way back to the indigenous peoples.

It was the tiger lucinid whose shells decorated the tables on my wedding day. And it is not just a food source. This clam burrows through the sediment housing the knotted roots of tropical seagrass. While studying seagrass in the Banc d’Arguin, a colleague of van Gils, Tjisse van der Heide, noticed that where there were more clams, there seemed to be more seagrass.

The team confirmed that this is the case with field and lab studies. They found that as leaf litter from seagrass decomposes, hydrogen sulphide forms in the sediments. This foul-smelling gas is toxic to seagrass roots so, if it builds up, it inhibits growth. When the clams are present, though, their symbiotic bacteria mop up the gas – and more gas means more food for the clams. So the clams and the seagrass each grow best when the other is present ().

Seagrass supports a wide range of animals, including manatees, turtles and seahorses. It provides nurseries for many commercially important fish and shellfish species. It even helps stabilise coastal sediments and store carbon. All of this, we now know, is thanks in part to the chemosymbiotic clams.

How many more ecosystems could be reliant in part on chemosynthesis? We are just scratching the surface when it comes to understanding the role of chemosynthesis in the ocean. And it’s not just the sea. Recent studies have shown that it plays a role in lakes and rivers too. It is amazing that a phenomenon first discovered in the dark depths of the ocean has turned out to be happening in our back yards all this time.

Speaking of back yards, it was my childhood home of the Bahamas where that wedding day comment struck me. I was snorkelling in the seagrass bed just off the beach and noticed dead lucinid shells clumped on the sandy seabed. What caught my attention was that they were all broken in the same odd way – with one shell completely intact while the other was broken off along a growth line. Something is eating these clams – but what? With help from the British Ecological Society and Natural Environment Research Council, I will be returning to the Bahamas to find the culprits and document another chemosynthesis-fuelled food chain.

This article appeared in print under the headline “Alternative lifestyle”