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

Abstract

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.

Comparative metagenomics of bathypelagic plankton and bottom sediment from the Sea of Marmara

“…Acidobacteria, a phylum that was found to be abundant in deep-sea Mediterranean waters (Quaiser et al, 2008), was also relatively well represented in mesopelagic waters, but not in deeper waters. By contrast, Acidobacteria were one of the three dominant groups in sediment libraries, together with Gamma-and mostly sulfate-reducing Delta-proteobacteria ( Figure S5; Woyke et al, 2006), relatives of which have been found in association with other gutless oligochaete worms in the Mediterranean (Ruehland et al, 2008). This suggests that some of the sediment-associated bacteria form stable endosymbiotic associations with a variety of anaerobic eukaryotic hosts.…”

Metagenomic analysis of size-fractionated picoplankton in a marine oxygen minimum zone

“…Spirochetes, which are traditionally associated with marine sediments or microbial mats, were only detected at the core OMZ depths (110, 200 m), consistent with this group being dominated by strictly or facultatively anaerobic members (Munn, 2011). Marine spirochetes have also been found in association with eukaryotes (Ruehland et al, 2008;Demiri et al, 2009), and may therefore be enriched in the particle fraction via attachment to larger organisms or sinking fecal matter. Similarly, sequences matching Mollicutes, which here were affiliated exclusively with the Mycoplasma (data not shown), may have originated from eukaryotic material, as mycoplasmas have been found in the larval stages of marine invertebrates and in the intestinal microflora of several fish species (Zimmer and Woollacott, 1983;Bano et al, 2007).…”

Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use

“…O. algarvensis lives in coarse-grained coastal sediments off the island of Elba, Italy, and migrates between the upper oxidized and the lower reduced sediment layers (6). It hosts a stable and specific microbial consortium consisting of five bacterial endosymbionts in its body wall: two aerobic or denitrifying gammaproteobacterial sulfur oxidizers (γ1-and γ3-symbionts), two anaerobic deltaproteobacterial sulfate reducers (δ1-and δ4-symbionts), and a spirochete with an unknown metabolism (7,8). The sulfate-reducing δ-symbionts provide the sulfur-oxidizing γ-symbionts with reduced sulfur compounds as an internal energy source for autotrophic CO 2 fixation via the Calvin-Benson cycle, thus explaining how O. algarvensis can thrive in its sulfide-poor environment (6, 9).…”