Enrichment of intracellular sulphur cycle –associated bacteria in intertidal benthic foraminifera revealed by 16S and aprA gene analysis

Benthic foraminifera are known to play an important role in marine carbon and nitrogen cycles. Here, we report an enrichment of sulphur cycle -associated bacteria inside intertidal benthic foraminifera (Ammonia sp. (T6), Haynesina sp. (S16) and Elphidium sp. (S5)), using a meta barcoding approach targeting the 16S rRNA and aprA -genes. The most abundant intracellular bacterial groups included the genus Sulfurovum and the order Desulfobacterales. The bacterial 16S OTUs are likely to originate from the sediment bacterial communities, as the taxa found inside the foraminifera were also present in the sediment. The fact that 16S rRNA and aprA -gene derived intracellular bacterial OTUs were species-specific and significantly different from the ambient sediment community implies that bacterivory is an unlikely scenario, as benthic foraminifera are known to digest bacteria only randomly. Furthermore, these foraminiferal species are known to prefer other food sources than bacteria. The detection of sulphur-cycle related bacterial genes in this study suggests a putative role for these bacteria in the metabolism of the foraminiferal host. Future investigation into environmental conditions under which transcription of S-cycle genes are activated would enable assessment of their role and the potential foraminiferal/endobiont contribution to the sulphur-cycle.Peer reviewe

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

Symbioses between bacteria and gutless marine oligochaetes

The first description of a gutless marine oligochaete was published in 1977 (Jamieson 1977), but it was not until 1979 that the reduction of a mouth and gut in this species and several other marine tubificid worms was recognized (Erséus 1979a,b; Giere 1979). At the time, the only other free-living worms known to lack a mouth or gut were pogonophores (now called Frenulata) that were most commonly found buried deep in the reducing sediments of continental slopes. Extensive studies on these very long and thin pogonophore worms indicated that their high surface areas enabled them to gain their nutrition from the uptake of dissolved organic compounds from the environment (Southward and Southward 1980). It was therefore assumed that the gutless oligochaetes that are also quite thin (0.1–0.2 mm) and relatively long (up to 2–3 cm), also gain their nutrition through the diffusive uptake of organic compounds from the sediment pore waters

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