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The First Metazoa Living in Permanently Anoxic Conditions

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The First Metazoa Living in Permanently Anoxic Conditions

Roberto Danovaro et al. BMC Biol.

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.

Figures

Figure 1
Figure 1
Metazoans retrieved from the deep hypersaline anoxic L'Atalante basin. (a) Light microscopy (LM) image of a Copepod exuvium (stained with Rose Bengal); (b) LM image of dead nematode (stained with Rose Bengal); (c) LM image of the undescribed species of Spinoloricus (Loricifera; stained with Rose Bengal); (d) LM image of the undescribed species of Spinoloricus stained with Rose Bengal showing the presence of an oocyte; (e) LM image of the undescribed species of Rugiloricus (Loricifera, stained with Rose Bengal) with an oocyte; (f) LM image of the undescribed species of Pliciloricus (Loricifera, non stained with Rose Bengal); (g) LM image of moulting exuvium of the undescribed species of Spinoloricus. Note the strong staining of the internal structures in the stained loriciferans (c and d) vs. the pale colouration of the copepod and nematode (a, b). The loriciferan illustrated in Figure 1e was repeatedly washed to highlight the presence of the internal oocyte. Scale bars, 50 μm.
Figure 2
Figure 2
Morphological details of the undescribed species of Spinoloricus (Loricifera). Scanning electron microscopy (SEM) image of (a) ventral side of a whole animal with the introvert out (note the loricated abdomen with eight plates); (b-c) anterior edge of the lorica showing the genus character of the genus Spinoloricus (additional spikes); and (d) posterior lorica with honey-comb structure. No prokaryotes are evident on the surface of the bodies of the loriciferans. Scale bars, as indicated.
Figure 3
Figure 3
Incorporation of Cell-Tracker™ Green CMFDA by loriciferans from the anoxic sediments of the L'Atalante basin. Series of confocal laser microscopy images across different sections of the body volume of the loriciferans. Sections 1-21 represent the progressive scanning of the loriciferans (undescribed species of Spinoloricus) from the outer to the inner part of the body. (a) Cell-Tracker™ Green CMFDA treated loriciferans; and (b) Loriciferans killed by freezing prior to Cell-Tracker™ Green CMFDA treatment and used as a control.
Figure 4
Figure 4
Electron micrographs of the internal body of loriciferans from the deep hypersaline anoxic L'Atalante basin. Illustrated are: (a) a hydrogenosome-like organelle; (b) hydrogenosome-like organelle with evidence of the marginal plate; (c) a field of hydrogenosome-like organelles; (d) the proximity between a possible endosymbiotic prokaryote and hydrogenosome-like organelles; (e-f) the presence of possible endosymbiotic prokaryotes; H = Hydrogenosome-like organelles, P = possible endosymbiotic prokaryotes, m = marginal plate. Scale bars, 0.2 μm.

Comment in

  • Anaerobic Metazoans: No Longer an Oxymoron
    LA Levin. BMC Biol 8, 31. PMID 20370909.
    The sediments of a deep-sea hypersaline and sulfidic Mediterranean basin have yielded an unexpected discovery, the first multicellular animals living entirely without oxy …
  • Anaerobic Animals From an Ancient, Anoxic Ecological Niche
    M Mentel et al. BMC Biol 8, 32. PMID 20370917.
    Tiny marine animals that complete their life cycle in the total absence of light and oxygen are reported by Roberto Danovaro and colleagues in this issue of BMC Biology. …
  • Animals, Anoxic Environments, and Reasons to Go Deep
    M Mentel et al. BMC Biol 14, 44. PMID 27267982.
    One of the classic questions in the early evolution of eukaryotic life concerns the role of oxygen. Many unicellular eukaryotes are strict anaerobes and many animals have …

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