Localization of RubisCO and sulfur in endosymbiotic bacteria of the gutless marine oligochaete Inanidrilus leukodermatus (Annelida)

Krieger, Jens; Giere, Olav; Dubilier, Nicole

doi:10.1007/s002270000355

Cited by 26 publications

(19 citation statements)

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“…The Gamma 1 symbionts of gutless oligochaetes have been identified as chemoautotrophic sulfur oxidizers based on their close phylogenetic relationship to free-living sulfur oxidizers, the presence of sulfur in their cells, and immunohistochemical studies showing the presence of form I RubisCO in these symbionts (10,25). This study provides further evidence that these symbionts are thiotrophic, based on the presence of the cbbL gene of form I RubisCO and the aprA gene of APS reductase.…”

Section: Discussionmentioning

confidence: 70%

“…An alternative explanation, that some or all of the alphaproteobacterial symbionts of these hosts are sulfur-oxidizing chemoautotrophs and that they are the source of these genes, is unlikely. The oligochaete Alpha symbionts are not related to known alphaproteobacterial sulfur oxidizers, and it has been shown that these small bacteria in I. leukodermatus do not contain sulfur and are not labeled by a form I RubisCO antiserum (25).…”

Section: Discussionmentioning

confidence: 99%

“…They form a monophyletic group that consists of only two genera, Inanidrilus and Olavius, within the subfamily Phallodrilinae (31). All worm species described so far, 25 Inanidrilus and 56 Olavius species (12), live in an obligate association with endosymbiotic bacteria. The lack of both a digestive and an excretory system led to the assumption that the symbiotic bacteria provide their hosts with a source of nutrition (19).…”

mentioning

confidence: 99%

“…I. leukodermatus occurs in high abundance in calcareous sands of coral reefs around the island Bermuda in the northwest Atlantic Ocean, and the morphology, physiology, and ecology of this species have been studied intensively (9,16,19,20,23,25). The symbionts of this species were the first to be characterized using molecular methods, and only a single thiotrophic gammaproteobacterial phylotype was identified despite the presence of multiple bacterial morphotypes (9).…”

mentioning

confidence: 99%

“…Two distinct forms of RubisCO have been found in chemoautotrophic symbionts: form I, for which the cbbL gene is used as a functional marker, and form II, for which the cbbM gene is used (5,25,33,38,39). Form I RubisCO differs from form II structurally and is better adapted to CO 2 fixation under aerobic conditions (40,41).…”

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confidence: 99%

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Phylogeny of 16S rRNA, Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase, and Adenosine 5′-Phosphosulfate Reductase Genes from Gamma- and Alphaproteobacterial Symbionts in Gutless Marine Worms (Oligochaeta) from Bermuda and the Bahamas

Blazejak

Kuever

Erséus

et al. 2006

Appl Environ Microbiol

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Gutless oligochaetes are small marine worms that live in obligate associations with bacterial endosymbionts. While symbionts from several host species belonging to the genus Olavius have been described, little is known of the symbionts from the host genus Inanidrilus. In this study, the diversity of bacterial endosymbionts in Inanidrilus leukodermatus from Bermuda and Inanidrilus makropetalos from the Bahamas was investigated using comparative sequence analysis of the 16S rRNA gene and fluorescence in situ hybridization. As in all other gutless oligochaetes examined to date, I. leukodermatus and I. makropetalos harbor large, oval bacteria identified as Gamma 1 symbionts. The presence of genes coding for ribulose-1,5-bisphosphate carboxylase/oxygenase form I (cbbL) and adenosine 5-phosphosulfate reductase (aprA) supports earlier studies indicating that these symbionts are chemoautotrophic sulfur oxidizers. Alphaproteobacteria, previously identified only in the gutless oligochaete Olavius loisae from the southwest Pacific Ocean, coexist with the Gamma 1 symbionts in both I. leukodermatus and I. makropetalos, with the former harboring four and the latter two alphaproteobacterial phylotypes. The presence of these symbionts in hosts from such geographically distant oceans as the Atlantic and Pacific suggests that symbioses with alphaproteobacterial symbionts may be widespread in gutless oligochaetes. The high phylogenetic diversity of bacterial endosymbionts in two species of the genus Inanidrilus, previously known only from members of the genus Olavius, shows that the stable coexistence of multiple symbionts is a common feature in gutless oligochaetes.

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Section: Discussionmentioning

confidence: 70%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%