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Extracellular and Mixotrophic Symbiosis in the Whale-Fall Mussel Adipicola pacifica: A Trend in Evolution from Extra- to Intracellular Symbiosis

BACKGROUND: Deep-sea mussels harboring chemoautotrophic symbionts from hydrothermal vents and seeps are assumed to have evolved from shallow-water asymbiotic relatives by way of biogenic reducing environments such as sunken wood and whale falls. Such symbiotic associations have been well characteriz...

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Autores principales: Fujiwara, Yoshihiro, Kawato, Masaru, Noda, Chikayo, Kinoshita, Gin, Yamanaka, Toshiro, Fujita, Yuko, Uematsu, Katsuyuki, Miyazaki, Jun-Ichi
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2910738/
https://www.ncbi.nlm.nih.gov/pubmed/20676405
http://dx.doi.org/10.1371/journal.pone.0011808
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author Fujiwara, Yoshihiro
Kawato, Masaru
Noda, Chikayo
Kinoshita, Gin
Yamanaka, Toshiro
Fujita, Yuko
Uematsu, Katsuyuki
Miyazaki, Jun-Ichi
author_facet Fujiwara, Yoshihiro
Kawato, Masaru
Noda, Chikayo
Kinoshita, Gin
Yamanaka, Toshiro
Fujita, Yuko
Uematsu, Katsuyuki
Miyazaki, Jun-Ichi
author_sort Fujiwara, Yoshihiro
collection PubMed
description BACKGROUND: Deep-sea mussels harboring chemoautotrophic symbionts from hydrothermal vents and seeps are assumed to have evolved from shallow-water asymbiotic relatives by way of biogenic reducing environments such as sunken wood and whale falls. Such symbiotic associations have been well characterized in mussels collected from vents, seeps and sunken wood but in only a few from whale falls. METHODOLOGY/PRINCIPAL FINDING: Here we report symbioses in the gill tissues of two mussels, Adipicola crypta and Adipicola pacifica, collected from whale-falls on the continental shelf in the northwestern Pacific. The molecular, morphological and stable isotopic characteristics of bacterial symbionts were analyzed. A single phylotype of thioautotrophic bacteria was found in A. crypta gill tissue and two distinct phylotypes of bacteria (referred to as Symbiont A and Symbiont C) in A. pacifica. Symbiont A and the A. crypta symbiont were affiliated with thioautotrophic symbionts of bathymodiolin mussels from deep-sea reducing environments, while Symbiont C was closely related to free-living heterotrophic bacteria. The symbionts in A. crypta were intracellular within epithelial cells of the apical region of the gills and were extracellular in A. pacifica. No spatial partitioning was observed between the two phylotypes in A. pacifica in fluorescence in situ hybridization experiments. Stable isotopic analyses of carbon and sulfur indicated the chemoautotrophic nature of A. crypta and mixotrophic nature of A. pacifica. Molecular phylogenetic analyses of the host mussels showed that A. crypta constituted a monophyletic clade with other intracellular symbiotic (endosymbiotic) mussels and that A. pacifica was the sister group of all endosymbiotic mussels. CONCLUSIONS/SIGNIFICANCE: These results strongly suggest that the symbiosis in A. pacifica is at an earlier stage in evolution than other endosymbiotic mussels. Whale falls and other modern biogenic reducing environments may act as refugia for primal chemoautotrophic symbioses between eukaryotes and prokaryotes since the extinction of ancient large marine vertebrates.
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spelling pubmed-29107382010-07-30 Extracellular and Mixotrophic Symbiosis in the Whale-Fall Mussel Adipicola pacifica: A Trend in Evolution from Extra- to Intracellular Symbiosis Fujiwara, Yoshihiro Kawato, Masaru Noda, Chikayo Kinoshita, Gin Yamanaka, Toshiro Fujita, Yuko Uematsu, Katsuyuki Miyazaki, Jun-Ichi PLoS One Research Article BACKGROUND: Deep-sea mussels harboring chemoautotrophic symbionts from hydrothermal vents and seeps are assumed to have evolved from shallow-water asymbiotic relatives by way of biogenic reducing environments such as sunken wood and whale falls. Such symbiotic associations have been well characterized in mussels collected from vents, seeps and sunken wood but in only a few from whale falls. METHODOLOGY/PRINCIPAL FINDING: Here we report symbioses in the gill tissues of two mussels, Adipicola crypta and Adipicola pacifica, collected from whale-falls on the continental shelf in the northwestern Pacific. The molecular, morphological and stable isotopic characteristics of bacterial symbionts were analyzed. A single phylotype of thioautotrophic bacteria was found in A. crypta gill tissue and two distinct phylotypes of bacteria (referred to as Symbiont A and Symbiont C) in A. pacifica. Symbiont A and the A. crypta symbiont were affiliated with thioautotrophic symbionts of bathymodiolin mussels from deep-sea reducing environments, while Symbiont C was closely related to free-living heterotrophic bacteria. The symbionts in A. crypta were intracellular within epithelial cells of the apical region of the gills and were extracellular in A. pacifica. No spatial partitioning was observed between the two phylotypes in A. pacifica in fluorescence in situ hybridization experiments. Stable isotopic analyses of carbon and sulfur indicated the chemoautotrophic nature of A. crypta and mixotrophic nature of A. pacifica. Molecular phylogenetic analyses of the host mussels showed that A. crypta constituted a monophyletic clade with other intracellular symbiotic (endosymbiotic) mussels and that A. pacifica was the sister group of all endosymbiotic mussels. CONCLUSIONS/SIGNIFICANCE: These results strongly suggest that the symbiosis in A. pacifica is at an earlier stage in evolution than other endosymbiotic mussels. Whale falls and other modern biogenic reducing environments may act as refugia for primal chemoautotrophic symbioses between eukaryotes and prokaryotes since the extinction of ancient large marine vertebrates. Public Library of Science 2010-07-27 /pmc/articles/PMC2910738/ /pubmed/20676405 http://dx.doi.org/10.1371/journal.pone.0011808 Text en Fujiwara et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Fujiwara, Yoshihiro
Kawato, Masaru
Noda, Chikayo
Kinoshita, Gin
Yamanaka, Toshiro
Fujita, Yuko
Uematsu, Katsuyuki
Miyazaki, Jun-Ichi
Extracellular and Mixotrophic Symbiosis in the Whale-Fall Mussel Adipicola pacifica: A Trend in Evolution from Extra- to Intracellular Symbiosis
title Extracellular and Mixotrophic Symbiosis in the Whale-Fall Mussel Adipicola pacifica: A Trend in Evolution from Extra- to Intracellular Symbiosis
title_full Extracellular and Mixotrophic Symbiosis in the Whale-Fall Mussel Adipicola pacifica: A Trend in Evolution from Extra- to Intracellular Symbiosis
title_fullStr Extracellular and Mixotrophic Symbiosis in the Whale-Fall Mussel Adipicola pacifica: A Trend in Evolution from Extra- to Intracellular Symbiosis
title_full_unstemmed Extracellular and Mixotrophic Symbiosis in the Whale-Fall Mussel Adipicola pacifica: A Trend in Evolution from Extra- to Intracellular Symbiosis
title_short Extracellular and Mixotrophic Symbiosis in the Whale-Fall Mussel Adipicola pacifica: A Trend in Evolution from Extra- to Intracellular Symbiosis
title_sort extracellular and mixotrophic symbiosis in the whale-fall mussel adipicola pacifica: a trend in evolution from extra- to intracellular symbiosis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2910738/
https://www.ncbi.nlm.nih.gov/pubmed/20676405
http://dx.doi.org/10.1371/journal.pone.0011808
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