A symbiosis or body hijack?

A symbiosis between a eukaryote and bacteria conveys a mutualistic relationship whereby an enhancement of fitness is evident in both partners. But at what stage does a symbiosis become a hijacking?

The worm Olavius algarvensis resides in shallow water sediment, migrating between the oxic and anoxic. Whether voluntarily or not, this worm has undergone an extreme body makeover; whereby it is now exists in a gutless form, without a mouth or an excretion system. O. algarvensis relies solely on it’s four bacterial symbionts for all its nutritional demands. The community of bacteria is made up of two aerobic denitrifying gammaproteobacteria, and two anaerobic sulfate reducing deltaproteobacteria. Sulfide is scare in the shallow sediment, so the sulfate reduction provides energy for the deltaproteobacteria, whilst simultaneously providing sulfide for the gammaproteobacteria, which can be used for autotrophic CO₂ fixation. 

The balance seems too perfect, and all organisms need to acquire nutrients from external sources. Kleiner et al (2012) shows that the ideal energy source for this migrating worm and its suite of microbes is carbon monoxide (CO). CO has a large redox potential and can be transferred to a number of electron acceptors, and thus provides a ubiquitous energy source for both anaerobic and aerobic bacteria. The use of CO as an energy source was supported by genes for CO dehydrogenase in all bacterial symbionts, and additionally by the unexpectedly high concentration of CO in the sediment.

As the worm did not hold on to its excretory system in its bodily cutbacks, an efficient waste management system is in place, which conserves energy by recycling waste products. The fermentative waste products produced by the worm in anaerobic conditions, is utilised by the delta-proteobacteria. Additionally the author hypothesises that one of the gammaproteobacteria may also contribute to waste management, as it produces an enzyme (3-HPB) that would allow it to fix CO₂, but also assimilate waste products. Furthermore, the gene for the 3-HPB-enzyme has been acquired through horizontal gene transfer, and may have been key in the early establishment of the symbiosis.

Consistent with the frugal nature of this symbiosis another mechanism for conserving energy is proposed.  In the first step of sulfate reduction pyrophosphate is produced, and must be removed from the cell in order to reduce sulfide. Yet the removal is energy costly and essentially wasteful. Here the bacteria are thought to store the pyrophosphate from sulfate reduction using a pyrophosphate enzyme (pryophosphatease), which is bound to the cell membrane. The pyrophosphatease acts as a proton pump creating a proton motive force, by hydrolysing pyrophosphate instead of ATP. The author infers that this might be a common feature in all sulfate reducers.

This intricate balance between the bacterial symbionts functioning together, like a well-oiled machine, leaves me questioning when does a eukaryotic organism just become a house for a bacterial community? This worm would not survive alone in this environment, so the bacteria are essential, but would the worm have dispersed elsewhere had the symbionts not moved in? Or would it have come to the end of it’s evolutionary line?

Reference:

Kleiner, M., Wentrup, C., Lott, C., Teeling, H., Wetzel, S., Young, J., ... & Dubilier, N. (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, 109(19), E1173-E1182.