Symbiosis insights through metagenomic analysis of a microbial consortium.

Symbioses between bacteria and eukaryotes are ubiquitous, yet our understanding of the interactions driving these associations is hampered by our inability to cultivate most host-associated microbes. Here we use a metagenomic approach to describe four co-occurring symbionts from the marine oligochaete Olavius algarvensis, a worm lacking a mouth, gut and nephridia. Shotgun sequencing and metabolic pathway reconstruction revealed that the symbionts are sulphur-oxidizing and sulphate-reducing bacteria, all of which are capable of carbon fixation, thus providing the host with multiple sources of nutrition. Molecular evidence for the uptake and recycling of worm waste products by the symbionts suggests how the worm could eliminate its excretory system, an adaptation unique among annelid worms. We propose a model that describes how the versatile metabolism within this symbiotic consortium provides the host with an optimal energy supply as it shuttles between the upper oxic and lower anoxic coastal sediments that it inhabits.

Gamma- and epsilonproteobacterial ectosymbionts of a shallow-water marine worm are related to deep-sea hydrothermal vent ectosymbionts.

The marine oligochaete worm Tubificoides benedii is often found in high numbers in eutrophic coastal sediments with low oxygen and high sulfide concentrations. A dense biofilm of filamentous bacteria on the worm's tail end were morphologically described over 20 years ago, but no further studies of these epibiotic associations were done. In this study, we used fluorescence in situ hybridization and comparative sequence analysis of 16S rRNA and protein-coding genes to characterize the microbial community of the worm's tail ends. The presence of genes involved in chemoautotrophy (cbbL and cbbM) and sulfur metabolism (aprA) indicated the potential of the T. benedii microbial community for chemosynthesis. Two filamentous ectosymbionts were specific to the worm's tail ends: one belonged to the Leucothrix mucor clade within the Gammaproteobacteria and the other to the Thiovulgaceae within the Epsilonproteobacteria. Both T. benedii ectosymbionts belonged to clades that consisted almost exclusively of bacteria associated with invertebrates from deep-sea hydrothermal vents. Such close relationships between symbionts from shallow-water and deep-sea hosts that are not closely related to each other are unusual, and indicate that biogeography and host affiliation did not play a role in these associations. Instead, similarities between the dynamic environments of vents and organic-rich mudflats with their strong fluctuations in reductants and oxidants may have been the driving force behind the establishment and evolution of these symbioses.

Multiple bacterial symbionts in two species of co-occurring gutless oligochaete worms from Mediterranean sea grass sediments.

Gutless oligochaete worms are found worldwide in the pore waters of marine sediments and live in symbiosis with chemoautotrophic sulfur-oxidizing bacteria. In the Mediterranean, two species of gutless oligochaete worms, Olavius algarvensis and O. ilvae, co-occur in sediments around sea grass beds. These sediments have extremely low sulfide concentrations (< 1 microM), raising the question if O. ilvae, as shown previously for O. algarvensis, also harbours sulfate-reducing symbionts that provide its sulfur-oxidizing symbionts with reduced sulfur compounds. In this study, we used fluorescence in situ hybridization (FISH) and comparative sequence analysis of genes for 16S rRNA, sulfur metabolism (aprA and dsrAB), and autotrophic carbon fixation (cbbL) to examine the microbial community of O. ilvae and re-examine the O. algarvensis symbiosis. In addition to the four previously described symbionts of O. algarvensis, in this study a fifth symbiont belonging to the Spirochaetes was found in these hosts. The symbiotic community of O. ilvae was similar to that of O. algarvensis and also included two gammaproteobacterial sulfur oxidizers and two deltaproteobacterial sulfate reducers, but not a spirochete. The phylogenetic and metabolic similarity of the symbiotic communities in these two co-occurring host species that are not closely related to each other indicates that syntrophic sulfur cycling provides a strong selective advantage to these worms in their sulfide-poor environment.