Toxic meal for gutless marine worm

Toxic meal for gutless marine worm

Olavius algarvensis is a marine worm which lives off the coast of Italy in the Mediterranean (Fig. 1.). The worm has no mouth or gut and lives off energy provided by five different symbiotic bacteria.  Previous metagenomic studies have shown that the bacterial symbionts enable the worm to migrate between upper oxidized layers of sediment and lower suboxic and anoxic layers to inhabit a range of different niches.

 

Figure 1. A photograph of Olavius algarvensis taken from the Max Planck Institute for Marine Microbiology website.

 

Kleiner et al. (2012) used metaproteomics and metabolomics to reveal previously unknown metabolic interactions between the symbionts and the worm host. At this point it is useful to highlight the difference between metagenomics and metaproteomics/metabolomics, the former approach can only predict the metabolic potential of an organism based on its genome, while the latter gives information on the actual physiology and metabolism occurring at the time of sampling. Both approaches are becoming increasingly important in studying non-culturable species.

The most significant findings of this study were that O. algarvensis symbionts can recycle host fermentative waste products and that they can use carbon monoxide (toxic to most animals) as an energy source. Given the oligotrophic conditions which the worm inhabits it would certainly be advantageous to recycle energy rather than excreting it. Aquatic invertebrates (without symbionts) must excrete fermentative waste products to maintain their internal pH, in doing so they lose large amounts of energy-rich organic compounds. The recycling of fermentative host waste products was detected by the high expression of enzymes for an almost complete 3-hydroxypropionate bi-cycle in one of the symbionts, in which the fermentative waste products can be heterotrophically assimilated. The discovery that symbionts can use carbon monoxide as an energy source came as quite a surprise given its toxicity to animals as it would be expected to have negative effects on the host. Furthermore researchers were surprised to find carbon monoxide in the sediment in sufficient quantities to allow such reactions to occur. This toxic compound, when coupled with carbon dioxide, is an excellent electron donor whose electrons can be transferred to a variety of terminal electron acceptors. The analysis detected the presence of aerobic and anaerobic carbon monoxide dehydrogenases. Carbon monoxide could therefore be used as an energy source for the symbionts under all redox conditions as the worm moves through the sediment layers.

Whilst reading about complex symbioses between a host animal and its microbes, I can’t help but wonder how such a relationship has evolved. Selection pressures have driven the symbiosis so far that it would appear the worm has entirely lost its ability to survive independently. We are starting to get a mechanistic understanding of the physiology of O. algarvensis’s relationship with four of its symbionts (two aerobic gammaproteobacteria who are both sulfur oxidzers and two anaerobic deltaproteobacteria who are both sulphate reducers). However there is a fifth member of the consortium, a spirochete, which we still know very little about. In the future it would be interesting to investigate the evolutionary relationship of the host and its symbionts more explicitly, rather than just speculating, which is all we have so far. Furthermore it would be interesting to explore how the host animal can survive in the presence of carbon monoxide, a known respiratory poison.

Kleiner, M., Wentrup, C., Lott, C., Teeling, H., Wetzel, S., Young, J., Chang, Y.-J., et al. (2012). Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use. Proceedings of the National Academy of Sciences of the United States of America, 109(19), 1–10.  http://www.pnas.org/content/109/19/E1173.full.pdf+html