High genetic similarity between two geographically distinct strains of the sulfur-oxidizing symbiont ‘Candidatus Thiobios zoothamnicoli’

Abstract

The giant marine ciliate Zoothamnium niveum (Ciliophora, Oligohymenophora) is obligatorily covered by a monolayer of putative chemoautotrophic sulfur-oxidizing (thiotrophic) bacteria. For Z. niveum specimens from the Caribbean Sea it has been demonstrated that this ectosymbiotic population consists of only a single pleomorphic phylotype described as Candidatus Thiobios zoothamnicoli. The goal of our study was to identify and phylogenetically analyse the ectosymbiont(s) of a recently discovered Z. niveum population from the Mediterranean Sea, and to compare marker genes encoding key enzymes of the carbon and sulfur metabolism between the two symbiont populations. We identified a single bacterial phylotype representing the ectosymbiont of Z. niveum from the Mediterranean population showing 99.7% 16S rRNA gene (99.2% intergenic spacer region) similarity to the Caribbean Z. niveum ectosymbiont. Genes encoding enzymes typical for an inorganic carbon metabolism [ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCO)] and for sulfur metabolism (5'-adenylylsulfate reductase, dissimilatory sulfite reductase) were detected in both symbiotic populations. The very high amino acid sequence identity (97-100%) and the high nucleic acid sequence identity (90-98%) of these marker enzymes in two geographically distant symbiont populations suggests that the association of Z. niveum with Cand. Thiobios zoothamnicoli is very specific as well as temporally and spatially stable.

Allying with armored snails: the complete genome of gammaproteobacterial endosymbiont

“…Previous studies also reported slow rates of nucleotide substitution in the 16S rRNA gene of various environmentally acquired symbionts, reflecting efficient purifying selection (Peek et al, 1998). Likewise, highly clonal population has also been reported for the environmentally transmitted, symbiotic sulfur-oxidizing gammaproteobacterium of ciliate Zoothamnium (Rinke et al, 2009).…”

“Candidatus Sonnebornia yantaiensis”, a member of candidate division OD1, as intracellular bacteria of the ciliated protist Paramecium bursaria (Ciliophora, Oligohymenophorea)

“…More recently, our knowledge of the diversity of bacteria associated with ciliates has increased significantly, primarily as a result of extensive molecular investigations of some commonly occurring species of the genera Paramecium and Euplotes. These studies have demonstrated that most bacterial symbionts belong to one of four classes of the phylum Proteobacteria, namely Alphaproteobacteria (including pathogenic Rickettsia) [2,8,9,18,19,21,22,51,59,60,62,64,67,69], Betaproteobacteria [58,63,66,68], Gammaproteobacteria [4,10,48,53] and Deltaproteobacteria [15]. Associations between ciliates and bacteria of other phyla seem to be infrequent, for example, Verrucomicrobia [42] and Firmicutes [54].…”

The giant ciliate Zoothamnium niveum and its thiotrophic epibiont Candidatus Thiobios zoothamnicoli: a model system to study interspecies cooperation

“…Thiobios zoothamnicoli (Rinke et al, 2006). The similarity between this and another population from Calvi, Corsica, was 99.7% (Rinke et al, 2009) and 99.2% to a Pacific population, termed “ectosymbiont of Zoothamnium niveum ” (Kawato et al, 2010). The internal transcribed spacer (ITS) was also highly similar between the Twin Cays and Calvi population (Rinke et al, 2009).…”

“…The similarity between this and another population from Calvi, Corsica, was 99.7% (Rinke et al, 2009) and 99.2% to a Pacific population, termed “ectosymbiont of Zoothamnium niveum ” (Kawato et al, 2010). The internal transcribed spacer (ITS) was also highly similar between the Twin Cays and Calvi population (Rinke et al, 2009). Genes for the key enzyme in the Calvin Benson cycle for carbon fixation (ribulose 1,5-bisphosphate carboxylase/oxygenase) and for sulfur metabolism (APS reductase, dissimilatory sulfite reductase) were discovered (Rinke et al, 2009).…”

“…The internal transcribed spacer (ITS) was also highly similar between the Twin Cays and Calvi population (Rinke et al, 2009). Genes for the key enzyme in the Calvin Benson cycle for carbon fixation (ribulose 1,5-bisphosphate carboxylase/oxygenase) and for sulfur metabolism (APS reductase, dissimilatory sulfite reductase) were discovered (Rinke et al, 2009). …”