Free-Living Tube Worm Endosymbionts Found at Deep-Sea Vents

Harmer, Tara L.; Rotjan, Randi D.; Nussbaumer, Andrea D.; Bright, Monika; NG, A; DeChaine, Eric G.; Cavanaugh, Colleen M.

doi:10.1128/aem.02470-07

Cited by 65 publications

(67 citation statements)

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“…Free-living "Ca. Endoriftia persephone" symbionts have been detected in biofilms and seawater surrounding R. pachyptila aggregations (4), and it has been demonstrated recently that the Riftia symbionts can return to their free-living stage upon the death of the worm (6), thereby maintaining/sustaining environmental populations.…”

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confidence: 99%

“…In return, the endosymbionts provide the tubeworm with the organic molecules necessary for growth and metabolism, either by excreting those molecules or by being digested directly (2,3). The symbiotic bacteria are transmitted horizontally, that is to say, acquired de novo from the environment at each generation (4). The symbionts penetrate the worm tissues through the epidermis and migrate to a region between the dorsal blood vessel and the foregut to form the prototrophosome.…”

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confidence: 99%

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Insights into Symbiont Population Structure among Three Vestimentiferan Tubeworm Host Species at Eastern Pacific Spreading Centers

Perez

Juniper

2016

Appl Environ Microbiol

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The symbiotic relationship between vestimentiferan tubeworms and their intracellular chemosynthetic bacteria is one of the more noteworthy examples of adaptation to deep-sea hydrothermal vent environments. The tubeworm symbionts have never been cultured in the laboratory. Nucleotide sequences from the small subunit rRNA gene suggest that the intracellular symbionts of the eastern Pacific vent tubeworms Oasisia alvinae, Riftia pachyptila, Tevnia jerichonana, and Ridgeia piscesae belong to the same phylotype of gammaproteobacteria, "Candidatus Endoriftia persephone." Comparisons of symbiont genomes between the East Pacific Rise tubeworms R. pachyptila and T. jerichonana confirmed that these two hosts share the same symbionts. Two Ridgeia symbiont genomes were assembled from trophosome metagenomes from worms collected from the Juan de Fuca Ridge (one and five individuals, respectively). We compared these assemblies to those of the sequenced Riftia and Tevnia symbionts. Pangenome composition, genome-wide comparisons of the nucleotide sequences, and pairwise comparisons of 2,313 orthologous genes indicated that "Ca. Endoriftia persephone" symbionts are structured on large geographical scales but also on smaller scales and possibly through host specificity. IMPORTANCERemarkably, the intracellular symbionts of four to six species of eastern Pacific vent tubeworms all belong to the same phylotype of gammaproteobacteria, "Candidatus Endoriftia persephone." Understanding the structure, dynamism, and interconnectivity of "Ca. Endoriftia persephone" populations is important to advancing our knowledge of the ecology and evolution of their host worms, which are often keystone species in vent communities. In this paper, we present the first genomes for symbionts associated with the species R. piscesae, from the Juan de Fuca Ridge. We then combine these genomes with published symbiont genomes from the East Pacific Rise tubeworms R. pachyptila and T. jerichonana to develop a portrait of the "Ca. Endoriftia persephone" pangenome and an initial outline of symbiont population structure in the different host species. Our study is the first to apply genome-wide comparisons of "Ca. Endoriftia persephone" assemblies in the context of population genetics and molecular evolution.A defining characteristic of hydrothermal vent ecosystems is the diversity and ubiquity of mutualistic partnerships between metazoa (multicellular organisms) and chemolithoautotrophic bacteria. Among these associations, one of the most remarkable is the well-studied model symbiosis between the giant tubeworm Riftia pachyptila and its unique sulfide-oxidizing gammaproteobacterial partner, "Candidatus Endoriftia persephone" (1). These intracellular symbionts are hosted within the specialized cells (bacteriocytes) of an organ known as the trophosome, which occupies most of the space in the coelomic cavity of the animal's trunk. In this mutualistic association, the worm supplies the bacteria with the inorganic compounds necessary for coupling sulfide oxidatio...

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Insights into Symbiont Population Structure among Three Vestimentiferan Tubeworm Host Species at Eastern Pacific Spreading Centers

Perez

Juniper

2016

Appl Environ Microbiol

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“…It is thus possible that symbionts of Spinaxinus result from a host shift from tubeworm-associated bacteria, or from free-living relatives of these bacteria. Tubeworm symbionts are indeed reported to occur free-living in the environment, making such a host shift possible (Harmer et al 2008), although this hypothesis remains to be properly tested here. The symbiont distribution as illustrated in Figure 10 shows no pattern of relationship with the thyasirid host, the environmental setting or the geographical location.…”

Section: Discussionmentioning

confidence: 99%

<i>Spinaxinus</i> (Bivalvia: Thyasiroidea) from sulfide biogenerators in the Gulf of Mexico and hydrothermal vents in the Fiji Back Arc: chemosymbiosis and taxonomy

Oliver¹,

Rodrigues²,

Carney³

et al. 2013

Sci. Mar.

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SUMMARY: Two new species of the thyasirid genus Spinaxinus (S. emicatus Oliver n. sp. and S. phrixicus Oliver n. sp.) are described from the Gulf of Mexico and the southwest Pacific, respectively. Both are compared with the type species of the genus, the eastern Atlantic S. sentosus . Living specimens from the Gulf of Mexico were retrieved from artificial sulfide bio-generators on the upper Louisiana Slope. Gill morphology and molecular markers from the symbiotic bacteria confirm that Spinaxinus is chemosynthetic and that the chemoautotrophic bacteria are related to sulfide oxidizing Gammaproteobacteria. Living specimens from the southwest Pacific were retrieved from hydrothermal vent sites in the Fiji and Lau Back Arc Basins. In the Atlantic Spinaxinus is now recorded from two anthropogenic situations and appears to be generally absent from natural cold seep sites and not yet recorded at any hydrothermal sites. The primarily anthropogenic distribution of Spinaxinus in the Atlantic is discussed with reference to the natural hydrothermal vent habitat of the Pacific S. phrixicus.Keywords: Thyasiroidea, taxonomy, chemosymbiosis, anthropogenic settings, hydrothermal vents. RESUMEN: SpinaxinuS (Bivalvia: Thyasiroidea) de bio-generadores artificiales de sulfuro situados en el Golfo de Méjico y en fuentes hidrotermales de las Islas Fiji: quimiosimbiosis y taxonomía. -En este trabajo se describen dos especies nuevas de tisárido del género Spinaxinus (S. emcatus Oliver n. sp. y S. phrixicus Oliver n. sp.) encontradas respectivamente en el Golfo de Méjico y en el sureste del Pacífico. Se comparan estas dos especies nuevas con la especie tipo del género, S. sentous Oliver y Holmes, 2006 descrita en el Este del Atlántico. Para describir estas dos especies, se observaron ejemplares vivos recolectados sobre bio-generadores artificiales de sulfuro situados en la parte alta de la plataforma continental de Louisiana, en el Golfo de Méjico. Las observaciones realizadas de las branquias de Spinaxinus y la caracterización genética de las bacterias simbiontes en estos ejemplares confirmaron que Spinaxinus es un género quimiosintético que contiene bacterias quimioautótrofas cercanas a las Gammaproteobacterias responsables de la oxidación del sulfuro. También se recolectaron ejemplares vivos de fuentes hidrotermales situadas en las Islas Fiji y en 'Lau Back Arc Basins' ambas localizadas en el Pacífico suroccidental. La especie atlántica de Spinaxinus se encontró en dos tipos de sustratos artificiales mientras que parece que esta especie no se encuentra en ambientes naturales equivalentes como serían las surgencias frías y las fuentes hidrotermales. La distribución aparentemente limitada de la especie atlántica se discute en relación con la distribución de S. phrixicus en las fuentes hidrotermales del Pacífico.

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“…In deep-sea vestimentiferan tubeworms, for example, the adults depend entirely on intracellular chemoautotrophic bacterial symbionts for nutrition; during metamorphosis the worms lose their functioning digestive tract altogether. However, these bacteria appear to be acquired environmentally during development, not from a host parent, and also are found free-living (21,22). In this case and others, a multispecies metabolic collective recurs in each generation, but the collectives do not reproduce as a unit.…”

Section: Conceptual Frameworkmentioning

confidence: 99%

Reproduction, symbiosis, and the eukaryotic cell

Godfrey‐Smith

2015

Proc. Natl. Acad. Sci. U.S.A.

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This paper develops a conceptual framework for addressing questions about reproduction, individuality, and the units of selection in symbiotic associations, with special attention to the origin of the eukaryotic cell. Three kinds of reproduction are distinguished, and a possible evolutionary sequence giving rise to a mitochondrion-containing eukaryotic cell from an endosymbiotic partnership is analyzed as a series of transitions between each of the three forms of reproduction. The sequence of changes seen in this "egalitarian" evolutionary transition is compared with those that apply in "fraternal" transitions, such as the evolution of multicellularity in animals.symbiosis | evolution | reproduction | eukaryote S ymbiosis raises general questions about evolution, cooperation, and "individuality" in living systems. These issues arise in especially important forms in the context of endosymbiotic theories of the evolution of the eukaryotic cell. This family of theories holds that the origins of the mitochondrion lie in a transition that began with the engulfing of a bacterium by an archaeon. The bacterium became first an endosymbiont and eventually an organelle, often playing an essential role in the metabolism of the larger cell. A similar sequence occurred in the history of plastids in photosynthetic eukaryotes, including the lineage leading to land plants (1-4). The endosymbiotic theory holds that the evolutionary transition that produced the eukaryotic cell was one in which a new kind of biological individual arose from the combination and integration of others (5).This paper develops a conceptual framework for addressing questions about individuality as they arise in symbiotic associations, with the eukaryotic cell as a central case. It does so by focusing especially on reproduction, an evolutionary phenomenon that is reshaped repeatedly in evolutionary transitions. Existing frameworks used in this area often treat reproduction and evolution in purely genetic terms (6). However, all objects that can form parentoffspring lineages can evolve in a Darwinian manner if further conditions are met. Symbiotic associations and the transitions they undergo motivate the development of a general treatment of reproduction, covering diverse kinds of parent-offspring lineages and distinguishing between biological objects that do form such lineages and those that do not. Although this paper is informal, the treatment of reproduction is intended to complement abstract multilevel models of Darwinian evolution, especially those based on the Price equation (7). The paper's framework embraces the importance of intermediate cases and movement between categories.

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Free-Living Tube Worm Endosymbionts Found at Deep-Sea Vents

Cited by 65 publications

References 22 publications

Insights into Symbiont Population Structure among Three Vestimentiferan Tubeworm Host Species at Eastern Pacific Spreading Centers

Insights into Symbiont Population Structure among Three Vestimentiferan Tubeworm Host Species at Eastern Pacific Spreading Centers

<i>Spinaxinus</i> (Bivalvia: Thyasiroidea) from sulfide biogenerators in the Gulf of Mexico and hydrothermal vents in the Fiji Back Arc: chemosymbiosis and taxonomy

Reproduction, symbiosis, and the eukaryotic cell

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