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Deep-sea animals "eat" oil: One man's meat is another man's poison

Jun 19, 2017

Scientists from Germany and the USA have discovered deep-sea animals living in symbiosis with bacteria that use oil as an energy source. At asphalt volcanoes in the Gulf of Mexico that spew oil, gas and tar, mussels and sponges live in symbiosis with bacteria that use short-chained alkanes in the oil as an energy source. The researchers furthermore discovered that bacteria closely related to the symbionts, which bloomed during the Deepwater Horizon oil spill, are also able to thrive on short-chain alkanes.

Stench and heat when a road is paved, black tar clumps at the beach that stick to your feet – asphalt does not make for a homey habitat. And yet it forms the basis for a flourishing ecosystem of mussels, crabs, worms, sponges and many other animals.

 Asphalt volcanoes brimming with life

In the depths of the Gulf of Mexico, oil and tar seep from the ocean floor and form bizarre structures reminiscent of cooled lava – so-called asphalt volcanoes. Researchers from Bremen, Germany, and the USA discovered these volcanoes nearly 15 years ago. These exotic environments still have many surprises in store, such as the one shown now in a study published in Nature Microbiology by an international research group led by Maxim Rubin-Blum and Nicole Dubilier from the Max Planck Institute for Marine Microbiology in Bremen, Germany.

 Symbiotic bacteria use a novel source of energy and carbon

The Campeche Knolls asphalt volcanoes at about 3,000 meters water depth in the Gulf of Mexico are home to a thriving biological community. But what do these organisms live from?

“They can’t eat the asphalt or oil and other food sources are rare in the deep sea,” explains Rubin-Blum. 

 “However, some an­im­als have es­tab­lished a sym­bi­otic re­la­tion­ship with bac­teria, and some of these sym­bionts can ex­tract en­ergy as well as car­bon from the oil.” Mar­ine re­search­ers have long known of such bac­teria in other oil-rich en­vir­on­ments – but they are free-liv­ing mi­croor­gan­isms that do not live in sym­bi­osis.

The robotic arm of the remotely operated vehicle MARUM-Quest (MARUM)
The robotic arm of the remotely operated vehicle MARUM-Quest is shown collecting Cycloclasticus-bearing mussels and oil-rich asphalts at a site of active gas emission in 3000 meters water depth. (MARUM – Center for Marine Environmental Sciences, University of Bremen)

Spoiled ring breakers

These oil-degrading bacteria belong to the genus Cycloclasticus. Their name means “ringbreaker,” and describes their ability to degrade oil by breaking hard-to-crack ring structures in oil. These aromatic compounds (called polycyclic aromatic hydrocarbons or PAHs) are highly toxic for most organisms, and degrading them is an arduous process that costs a lot of energy.

The symbiotic Cycloclasticus that the Bremen researchers discovered in mussels and sponges from the asphalt volcanoes no longer bother with degrading PAHs. They have made life easier for themselves by specializing on the oil’s easily degradable compounds – natural gases such as butane, ethane, and propane, called short-chain alkanes. “These microorganisms no longer degrade PAH,” explains Rubin-Blum, "because they have lost the genes they need to do this .” This is the first discovery of Cycloclasticus bacteria that can no longer degrade PAH and instead gain all their energy and carbon from short-chain alkanes.

Because the short-chain alkanes are so easy to use, many microorganisms compete for them. How can these symbiotic bacteria rely on such fiercely contested compounds and why did they give up their ability to live on PAH?

“We think that they can only afford this ‘luxury’ because of their symbiosis with mussels and sponges,” explains Nicole Dubilier from the Bremen Max Planck Institute. “These hosts provide the symbiotic Cycloclasticus with a continuous supply of short-chain alkanes through their constant filtering of the surrounding seawater. By living inside animals, these symbionts are well taken care of and do not have to compete with free-living bacteria.”

“This is the first time a symbiosis based on short-chain alkanes has been described,” Rubin-Blum adds. This study thus extends the range of known substances that can power chemosynthetic symbioses.

Free-living relatives: Pleasure before business

Rubin-Blum, Dubilier and their colleagues compared the genomes of the symbiotic bacteria with closely-related free-living species of Cycloclasticus. These bloomed in large numbers in the Gulf of Mexico after the Deepwater Horizon oil catastrophe. They were excited to discover that some free-living Cycloclasticus can also degrade short-chain alkanes.

“That was surprising as until now it was thought that Cycloclasticus could only live from PAHs,” explains Dubilier. Short-chain alkanes are mainly found in the early stages of an oil spill and are quickly used up by free-living microorganisms. In contrast to the symbiotic Cycloclasticus, however, their free-living relatives are still able to use PAHs. “This allows them to remain flexible. When the short-chain morsels are gone, they can still degrade the considerably tougher PAHs,” says Dubilier.

Cycloclasticus is clearly a key player in marine oil degradation,” adds Rubin-Blum. “That is why we now plan to compare the physiology and metabolism of symbiotic and free-living Cycloclasticus in more detail to learn more about how they contribute to the degradation of hydrocarbons in the oceans.”

Colourful display of the symbiosis (Max Planck Institute for Marine Microbiology, Bremen)
Colourful display of the symbiosis: Within cells in the gills of a Bathymodiolus mussel (cell nuclei in blue), Cycloclasticus (green) reside next to larger methane-oxidizing bacteria (red). (Max Planck Institute for Marine Microbiology, Bremen)

Behind the scenes: When life gives you lemons, make lemonade

Blogpost by Maxim Rubin-Blum on Nature Microbiology Community

 

Original publication

Maxim Rubin-Blum, Chakkiath Paul Antony, Christian Borowski, Lizbeth Sayavedra, Thomas Pape, Heiko Sahling, Gerhard Bohrmann, Manuel Kleiner, Molly C. Redmond, David L. Valentine, Nicole Dubilier (2017): Short-chain alkanes fuel mussel and sponge Cycloclasticus symbionts from deep-sea gas and oil seeps. Nature Microbiology.

DOI: 10.1038/nmicrobiol.2017.93

Full-text pdf 

 

Participating institutes

Max Planck Institute for Marine Microbiology, Bremen, Germany

MARUM - Center for Marine Environmental Sciences, University of Bremen, Germany

Department of Geoscience, University of Calgary, Canada

Department of Biological Sciences, University of North Carolina at Charlotte, USA

Department of Earth Science, University of California at Santa Barbara, USA

 

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Dr. Maxim Rubin Blum

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+49 421 2028-905

Dr. Maxim Rubin Blum

Director

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Prof. Dr. Nicole Dubilier

MPI for Marine Microbiology
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Prof. Dr. Nicole Dubilier

or the press office

 

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Germany

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Fanni Aspetsberger

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Manfred Schlösser

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Manfred Schlösser
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