Oxygen and Other Electron Acceptors

Gutless oligochaetes require oxygen, not only for their own respiration, but also for their sulfur-oxidizing symbionts, that use oxygen or other oxidized compounds such as nitrate as an electron acceptor. While the worms can survive short periods in the absence of oxygen, presumably by switching to an anaerobic metabolism as observed in many other marine invertebrates (Grieshaber et al. 1992; Dubilier et al. 1995b), longer periods of anoxia for several days lead to massive mortalities (Dubilier, unpubl. obs.). As all tubificids, the worms contain well developed blood vessels with a red respiratory pigment (presumably hemoglobin), enabling them to store oxygen for limited time periods.

At almost all sites investigated, gutless oligochaetes are most dominant in the deeper sediment layers at 5-15 cm below the sediment surface. In most sediments, including those of coral reefs, oxygen penetrates at most only a few cm into the sediment (Falter and Sansone 2000). At the Elba site in the Mediterranean, oxygen can penetrate as deep as 3 cm below the sediment surface (D. de Beer, unpubl. data), but not to where the worms occur at 10-15 cm sediment depth. At the up-welling site off the coast of Peru, where O. crassitunicatus was the dominant member of the infauna, oxygen concentrations were extremely low just above the sediment surface (<1 ^M) and it is very likely that such low concentrations persist for longer time periods (Levin et al. 2002, 2003). Interestingly, at this site the worms occur in the upper sediment layers between 1-5 cm sediment depth, indicating that the worms migrate upwards when oxygen becomes limiting.

In all known habitats of gutless oligochaetes there is no overlap between oxygen in the upper sediment layers and reduced sulfur compounds in the deeper sediment layers. Since the worms do not build tubes or burrows, it is assumed that they migrate between the lower sulfidic and the upper oxygenated sediments. This model implies that sulfide is taken up in the anoxic deeper sediment layers, oxidized to sulfur by either nitrate from the environment or oxygen from the worm's hemoglobin, and the sulfur stored in the bacteria until the worms migrate to upper sediment layers where the sulfur could be fully oxidized to sulfate. Experiments show that the worms can migrate actively through the sediment (Giere et al. 1991). However, nothing is known about the time periods spent by individual worms in oxygenated or sulfidic sediments, whether nitrate is used as an electron acceptor, and whether the symbiotic bacteria can oxidize sulfide using oxygen stored in the worm's hemoglobin.

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