Dataset Information

Structure of an extracellular giant hemoglobin of the gutless beard worm Oligobrachia mashikoi.

ABSTRACT: Mouthless and gutless marine animals, pogonophorans and vestimentiferans, obtain their nutrition solely from their symbiotic chemoautotrophic sulfur-oxidizing bacteria. These animals have sulfide-binding 400-kDa and/or 3,500-kDa Hb, which transports oxygen and sulfide simultaneously. The symbiotic bacteria are supplied with sulfide by Hb of the host animal and use it to provide carbon compounds. Here, we report the crystal structure of a 400-kDa Hb from pogonophoran Oligobrachia mashikoi at 2.85-A resolution. The structure is hollow-spherical, composed of a total of 24 globins as a dimer of dodecamer. This dodecameric assemblage would be a fundamental structural unit of both 400-kDa and 3,500-kDa Hbs. The structure of the mercury derivative used for phasing provides insights into the sulfide-binding mechanism. The mercury compounds bound to all free Cys residues that have been expected as sulfide-binding sites. Some of the free Cys residues are surrounded by Phe aromatic rings, and mercury atoms come into contact with these residues in the derivative structure. It is strongly suggested that sulfur atoms bound to these sites could be stabilized by aromatic-electrostatic interactions by the surrounding Phe residues.

SUBMITTER: Numoto N

PROVIDER: S-EPMC1253539 | biostudies-literature | 2005 Oct

REPOSITORIES: biostudies-literature

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Publications

Structure of an extracellular giant hemoglobin of the gutless beard worm Oligobrachia mashikoi.

Numoto Nobutaka N Nakagawa Taro T Kita Akiko A Sasayama Yuichi Y Fukumori Yoshihiro Y Miki Kunio K

Proceedings of the National Academy of Sciences of the United States of America 20051003 41

Mouthless and gutless marine animals, pogonophorans and vestimentiferans, obtain their nutrition solely from their symbiotic chemoautotrophic sulfur-oxidizing bacteria. These animals have sulfide-binding 400-kDa and/or 3,500-kDa Hb, which transports oxygen and sulfide simultaneously. The symbiotic bacteria are supplied with sulfide by Hb of the host animal and use it to provide carbon compounds. Here, we report the crystal structure of a 400-kDa Hb from pogonophoran Oligobrachia mashikoi at 2.85 ...[more]

PMID: 16204001

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Project description:Gutless phallodrilines are marine annelid worms without a mouth or gut, which 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 phallodriline Inanidrilus exumae that differs markedly from the microbiomes of all 22 of the other host species examined. Comparative 16S rRNA gene sequence analysis and fluorescence in situ hybridization revealed that I. exumae harbors cooccurring gamma-, alpha-, and deltaproteobacterial symbionts, while all other known host species harbor gamma- and either alpha- or deltaproteobacterial symbionts. Surprisingly, the primary chemoautotrophic sulfur oxidizer "Candidatus Thiosymbion" that occurs in all other gutless phallodriline hosts does not appear to be present in I. exumae Instead, I. exumae harbors a bacterial endosymbiont that resembles "Ca Thiosymbion" morphologically and metabolically but originates from a novel lineage within the class Gammaproteobacteria This endosymbiont, named Gamma 4 symbiont here, had a 16S rRNA gene sequence that differed by at least 7% from those of other free-living and symbiotic bacteria and by 10% from that of "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), indicate that this symbiont is a chemoautotrophic sulfur oxidizer. Our results suggest that a novel lineage of free-living bacteria was able to establish a stable and specific association with I. exumae and appears to have displaced the "Ca Thiosymbion" symbionts originally associated with these hosts.IMPORTANCE All 22 gutless marine phallodriline species examined to date live in a highly specific association with endosymbiotic, chemoautotrophic sulfur oxidizers called "Ca Thiosymbion." These symbionts evolved from a single common ancestor and represent the ancestral trait for this host group. They are transmitted vertically and assumed to be in transition to becoming obligate endosymbionts. It is therefore surprising that despite this ancient, evolutionary relationship between phallodriline hosts and "Ca Thiosymbion," these symbionts are apparently no longer present in Inanidrilus exumae They appear to have been displaced by a novel lineage of sulfur-oxidizing bacteria only very distantly related to "Ca Thiosymbion." Thus, this study highlights the remarkable plasticity of both animals and bacteria in establishing beneficial associations: the phallodriline hosts were able to acquire and maintain symbionts from two very different lineages of bacteria, while sulfur-oxidizing bacteria from two very distantly related lineages were able to independently establish symbiotic relationships with phallodriline hosts.

Dataset Information

Structure of an extracellular giant hemoglobin of the gutless beard worm Oligobrachia mashikoi.

Publications

Structure of an extracellular giant hemoglobin of the gutless beard worm Oligobrachia mashikoi.

Similar Datasets

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