Multicelled Animals May Live Oxygen-Free

Creatures living deep in the Mediterranean without oxygen would be a remarkable first, biologists say.

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By Susan Milius, Science News

The claim is startling and the evidence indirect, but marine biologists seem open to the idea that multicellular animals can live without oxygen.

Three species of loriciferan, a creature that sounds and looks like something out of a Dr. Seuss book, appear to go their whole lives without oxygen, researchers report online April 6 in BMC Biology.

“This discovery is truly exceptional,” says invertebrate biologist Gonzalo Giribet of Harvard University, who was not part of the study.

Pulled out of a briny, sulfurous hellhole 3.5 kilometers below the surface of the Mediterranean Sea, the newfound creatures look like tiny cups with tentacles sticking out. Loriciferans are real, multicellular animals though, so different from other creatures that the tiny marine oddballs have their own phylum on a par with mollusks and arthropods.

Until now, biologists had expected only one-celled organisms such as bacteria to thrive in oxygen-depleted places. Multicellular animals were known to pass through or hunker down temporarily in environments without oxygen, but in all cases needed to have it in some way at some time.  

Following molecular tests and microscope work, the scientists who found the three species propose that the loriciferans in the muck aren’t just visiting down there.

Finding a full-time resident of oxygen-free zones “would be a watershed for how we can think about where animals live,” says Tim Shank of Woods Hole Oceanographic Institution in Massachusetts. He studies animals living in the improbably deep, harsh, hot world of ocean vents, which nonetheless still rely on oxygenated water swirling around. If an animal really can survive long-term in a totally oxygen-free place, Shank says, it would be “a step beyond” even the marvels of the vents.

The loriciferans’ home, the L’Atalante basin, turned so briny when the Mediterranean Sea was closed off from the Atlantic and salt concentrated in the basin much the way it does in the Dead Sea today. When the Mediterranean reconnected to the Atlantic, extreme brine remained trapped in the L’Atalante and other deep basins.

Three research expeditions — in 1998, 2005 and 2008 — have found loriciferans in core samples from the basin. When researchers first found the animals, “we thought they were cadavers,” says study coauthor Roberto Danovaro of Polytechnic University of Marche in Ancona, Italy. 

To see if the loriciferans had just wafted down after dying elsewhere, researchers brought up more sediment cores and tested them on ship in nitrogen-filled incubators protected from oxygen. In molecular tests, the animals appeared to be alive and metabolizing.

The presence of cast-off skins also suggests that the loriciferans are growing on location. They may be reproducing there too. Two individuals had eggs, Danovaro says. Also, the loriciferans aren’t even a millimeter long and have limited mobility, so it’s unlikely that they’d move through the 50 meters of oxygen-free water above them. Thus, the researchers argue, it’s most likely the basin is their full-time home.

The evidence may be indirect, but “I think they’re right,” says Lisa Levin of Scripps Institution of Oceanography in La Jolla, Calif.

Electron microscope images show that loriciferans’ cellular innards look adapted for a zero-oxygen life, Danovaro says. Their cells don’t appear to have mitochondria, which use oxygen to generate energy. Instead, images of loriciferan tissue reveal what look like hydrogenosomes, organelles that power some anaerobic single-celled creatures.

And near the loriciferans’ hydrogenosome-like bits lie rod-shaped structures that could be symbiotic organisms.  Some one-celled creatures depend on such organisms along with the organelles to harvest energy.

The research team may indeed have found multicelled creatures living in anoxic conditions, but the evidence for those creatures having hydrogenosomes still looks "preliminary," cautions Johannes Hackstein of Radboud University Nijmegen in the Netherlands, who studies the structures.