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Open Access Highly Accessed Research article

The first metazoa living in permanently anoxic conditions

Roberto Danovaro1*, Antonio Dell'Anno1, Antonio Pusceddu1, Cristina Gambi1, Iben Heiner2 and Reinhardt Møbjerg Kristensen2

Author affiliations

1 Department of Marine Science, Faculty of Science, Polytechnic University of Marche, Via Brecce Bianche, 60131 Ancona, Italy

2 Natural History Museum of Denmark, Zoological Museum, Invertebrate Department, Universitetsparken 15, DK-2100 Copenhagen, Denmark

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Citation and License

BMC Biology 2010, 8:30  doi:10.1186/1741-7007-8-30

Published: 6 April 2010

Abstract

Background

Several unicellular organisms (prokaryotes and protozoa) can live under permanently anoxic conditions. Although a few metazoans can survive temporarily in the absence of oxygen, it is believed that multi-cellular organisms cannot spend their entire life cycle without free oxygen. Deep seas include some of the most extreme ecosystems on Earth, such as the deep hypersaline anoxic basins of the Mediterranean Sea. These are permanently anoxic systems inhabited by a huge and partly unexplored microbial biodiversity.

Results

During the last ten years three oceanographic expeditions were conducted to search for the presence of living fauna in the sediments of the deep anoxic hypersaline L'Atalante basin (Mediterranean Sea). We report here that the sediments of the L'Atalante basin are inhabited by three species of the animal phylum Loricifera (Spinoloricus nov. sp., Rugiloricus nov. sp. and Pliciloricus nov. sp.) new to science. Using radioactive tracers, biochemical analyses, quantitative X-ray microanalysis and infrared spectroscopy, scanning and transmission electron microscopy observations on ultra-sections, we provide evidence that these organisms are metabolically active and show specific adaptations to the extreme conditions of the deep basin, such as the lack of mitochondria, and a large number of hydrogenosome-like organelles, associated with endosymbiotic prokaryotes.

Conclusions

This is the first evidence of a metazoan life cycle that is spent entirely in permanently anoxic sediments. Our findings allow us also to conclude that these metazoans live under anoxic conditions through an obligate anaerobic metabolism that is similar to that demonstrated so far only for unicellular eukaryotes. The discovery of these life forms opens new perspectives for the study of metazoan life in habitats lacking molecular oxygen.