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

Journal article
Authors Claudia Bergin
Cecilia Wentrup
Nancy Brewig
Anna Blazejak
Christer Erséus
Olav Giere
Markus Schmid
Pierre De Wit
Nicole Dubilier
Published in Applied and Environmental Microbiology
Volume 84
Issue 7
ISSN 0099-2240
Publication year 2018
Published at Department of marine sciences
Department of Biological and Environmental Sciences
Language en
Links https://doi.org/10.1128/AEM.02267-1...
Keywords symbiosis, oligochaetes, Clitellata, chemoautotrophy, fluorescence in situ hybridization, 16S rRNA, aprA, cbbL, sulfur oxidizers, sulfate reducers, symbiont replacement / displacement
Subject categories Evolutionary Biology

Abstract

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.

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