Anaerobic animals from an ancient, anoxic ecological niche

Abstract

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. These fascinating animals are new members of the phylum Loricifera and possess mitochondria that in electron micrographs look very much like hydrogenosomes, the H2-producing mitochondria found among several unicellular eukaryotic lineages. The discovery of metazoan life in a permanently anoxic and sulphidic environment provides a glimpse of what a good part of Earth's past ecology might have been like in 'Canfield oceans', before the rise of deep marine oxygen levels and the appearance of the first large animals in the fossil record roughly 550-600 million years ago. The findings underscore the evolutionary significance of anaerobic deep sea environments and the anaerobic lifestyle among mitochondrion-bearing cells. They also testify that a fuller understanding of eukaryotic and metazoan evolution will come from the study of modern anoxic and hypoxic habitats.

Figure 1

Schematic phylogeny of animals based on the report by Dunn et al [48] which, however, did not include the phylum Loricifera [1] (highlighted in red). It was placed here (dotted line) as branching with Priapulida and Kinorhyncha as reported elsewhere [49,50]. Higher taxon designations are those used in references [48-50]. The Cycloneuralia, where Loricifera belong, are currently grouped within the Ecdysozoa, which also includes nematodes and insects. To the right of the phylogeny, several species are listed whose facultatively anaerobic mitochondria have been studied [10-14]; in no way does this imply the absence of anaerobic mitochondira in other groups. No biochemical data are yet available for the Loriciferan mitochondria [1].

Figure 2

Protistan schematic phylogeny representing current view about eukaryotes phylogeny grouping all known eukaryotic life to six major clades or supergroups [20], together with information about the mitochondria from some anaerobic, facultatively anaerobic or parasitic representatives [19,21]. With greater sampling of anoxic habitats [3,4,27], additional information about anaerobic eukaryotes can be expected. The latest additions are the new species of loriciferan animals (red) from the anoxic L'Atalante basin [1]. LECA: last eukaryotic common ancestor. Note the absence of primitively amitochondriate lineages among eukaryotes [19,21].