The first metazoa living in permanently anoxic conditions

Abstract

BackgroundSeveral 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.ResultsDuring 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.ConclusionsThis 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.

Key bioactive reaction products of the NO/H2S interaction are S/N-hybrid species, polysulfides, and nitroxyl

“…Indeed, sulfide may have supported life long before the emergence of O 2 and NO (2,3). * This notion is consistent with a number of observations: H 2 S is essential for efficient abiotic amino acid generation as evidenced by the recent reanalysis of samples of Stanley Miller's original spark discharge experiments (4), sulfide is an efficient reductant in protometabolic reactions forming RNA, protein, and lipid precursors (5), and sulfide is both a bacterial and mitochondrial substrate (6), enabling even multicellular lifeforms to exist and reproduce under conditions of permanent anoxia (7). Thus, although eukaryotic cells may have originated from the symbiosis of sulfurreducing and -oxidizing lifeforms within a self-contained sulfur redox metabolome (8), sulfide may have been essential even earlier by providing the basic building blocks of life.…”

Inter-comparison of the potentially active prokaryotic communities in the halocline sediments of Mediterranean deep-sea hypersaline basins

“…Explorations of biological diversity in DHAB water--columns led to the discovery of microorganisms with novel structures and metabolic/physiological capabilities, and to an increased understanding of the adaptability of different taxonomic groups and of the physico--chemical limits for life on Earth. Although there is some evidence that living metazoa occur in the DHABs (Danovaro et al 2010), only unicellular organisms are expected to endure in these habitats, as more complex organisms are not likely to cope with these harsh conditions for more than short periods of exposure (e.g., during feeding excursions into haloclines). Indeed, microbial life from all three domains has been shown to occur in such aquatic systems (e.g.…”

Requirements and limits for life in the context of exoplanets

“…There are interesting exceptions to the connection between oxygen and multicellular life (52,53) and the link to O 2 may be in need of further scrutiny (54). Nonetheless, levels of O 2 over a few percent on an exoplanet would be consistent with, and possibly indicative of, the presence of multicellular organisms.…”