Anaerobic Metazoans: No longer an oxymoron

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COMMENTARY

Anaerobic Metazoans: No longer an oxymoron Commentary Lisa A Levin

Abstract The sediments of a deep-sea hypersaline and sulfidic Mediterranean basin have yielded an unexpected discovery, the first multicellular animals living entirely without oxygen. Reported by Danovaro et al. in BMC Biology, these three new species of Loricifera add a new and remarkable dimension to anoxic ecosystems previously thought to support only unicellular life. Few environments on earth lack life in some form; microbes appear to be ubiquitous, with a presence from the atmosphere [1] to the deep subsurface ocean [2]. But extreme settings often lack multicelluar organisms. Some of the most extreme environments on earth can be found in the deep ocean. Excessively high salinities in brine pools, toxic sulfide levels within methane seep sediments, high metal concentrations in hydrothermal vent fluids, high pressures at the bottom of trenches, and anoxic sediments in isolated basins and midwater oxygen minimum zones are examples. Prokaryotic organisms (without nuclei) are known to inhabit all of these settings, and single-cell eukaryotic organisms (protozoa), most noticeably ciliates and foraminifera, are also recorded in most extreme deep-sea environments. Anoxic and dysoxic environments in particular host a reduced diversity of protozoans [3]. These protozoans have a range of adaptations that often involve symbioses [4] and the ability to store and respire nitrate, although most taxa that do this appear to be facultative anaerobes [5]. To date, however, no one has found metazoans capable of living and reproducing entirely in the absence of oxygen. This has changed with the discovery by Danovaro et al.[6] of viable loriciferans in a hypersaline, anoxic basin of the Mediterranean Sea. Loricifera are small (< 1 mm), exclusively marine meiofauna that belong to a relatively recently described marine phylum. Although there are only 22 described species, they have been recorded from a broad range of depths and settings ranging from shallow, coastal waters * Correspondence: [email protected] 1

Integrative Oceanography Division, Scripps Institution of Oceanography, La Jolla, CA 92093-0218, USA

Full list of author information is available at the end of the article

to methane seeps and hydrothermal vents, to the IzuOgasawara trench off Japan [7,8]. Loriciferans are an unlikely candidate for the honor of being the first anoxyphilic metazoan. Low-oxygen sediments have been studied extensively and loriciferans are rarely reported [9]. Whether they were overlooked or are exceedingly rare and thus not sampled is unclear. Perhaps scientists have been looking for them in all the wrong places. In the L'Atalante Basin the loriciferans were sampled with other metazoans (copepods and nematodes) but Danovaro et al.[6], using a protein binding stain, fluorogenic probes, and radiolabel uptake experiments, determined that only the loriciferans were alive and metabolically active at the time of collection. They found not one, but three new sp