Acquisition of a Novel Sulfur-Oxidizing Symbiont in the Gutless Marine Worm Inanidrilus exumae

• Gutless marine oligochaetes (Annelida, Clitellata) lack a digestive and excretory system, and live in an obligate association with multiple bacterial endosymbionts that supply them with nutrition. In this study, we discovered an unusual symbiont community in the gutless oligochaete Inanidrilus exumae that differs markedly from the microbiome of all other 22 examined host species. Comparative 16S rRNA sequence analysis and fluorescence in situ hybridization revealed that I.exumae harboured co-occurring gamma-, alpha- and deltaproteobacterial symbionts, while all other host species harbour gamma- and either alpha- or deltaproteobacterial symbionts. Surprisingly, the primary chemoautotrophic, sulfur-oxidizer, Ca. Thiosymbion, which occurs in all other gutless oligochaetes, does not appear to be present in I.exumae. Instead, I. exumae harboured a bacterial endosymbiont that resembled Ca. Thiosymbion morphologically and metabolically, but originated from a novel lineage within the Gammaproteobacteria. This endosymbiont, named Gamma 4 symbiont here, had a 16S rRNA sequence that differed by at least 7% from those of other free-living and symbiotic bacteria and by 10% from Ca. Thiosymbion. Sulfur globules in the Gamma 4 symbiont cells, as well as the presence of genes characteristic for autotrophy (cbbL) and sulfur oxidation (aprA), suggest that this symbiont is a chemoautotrophic sulfur oxidizer. Our results indicate that a novel lineage of free-living bacteria was able to establish a stable and specific association with I. exumae, and displace the Ca. Thiosymbion symbionts originally associated with these hosts.

Subject headings

NATURVETENSKAP  -- Biologi -- Evolutionsbiologi (hsv//swe)

NATURAL SCIENCES  -- Biological Sciences -- Evolutionary Biology (hsv//eng)

NATURVETENSKAP  -- Biologi -- Mikrobiologi (hsv//swe)

NATURAL SCIENCES  -- Biological Sciences -- Microbiology (hsv//eng)

Keyword

symbiosis

oligochaetes

Clitellata

chemoautotrophy

fluorescence in situ hybridization

16S rRNA

aprA

cbbL

sulfur oxidizers

sulfate reducers

symbiont replacement / displacement

symbiosis

Publication and Content Type

ref (subject category)

art (subject category)