The worm affair: fidelity and environmental adaptation in symbiont species that co‐occur in vestimentiferan tubeworms

Zvi-Kedem, Tal; Shemesh, Eli; Tchernov, Dan; Rubin‐Blum, Maxim

doi:10.1111/1758-2229.12994

Cited by 4 publications

(4 citation statements)

References 79 publications

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“…The presence of flagella-encoding loci could suggest that the biology of the A. adamantis symbiosis is markedly different from other gammaproteobacterial associations in Alviniconcha and has closer resemblance to Campylobacteria-dominated systems, where flagella have been implicated in host specificity, nutrient transfer and/or continuous symbiont transmission ( Sanders et al 2013 ). Host specificity might further be promoted by outer membrane porins, which have been shown to play a role in host recognition in both terrestrial and aquatic symbioses ( Weiss et al 2008 ; Nyholm et al 2009 ; Zvi-Kedem et al 2021 ). Host colonization and subsequent maintenance of the intrahost symbiont population involves a delicate interplay between host and symbiont molecular factors.…”

Section: Resultsmentioning

confidence: 99%

Genome assembly of the chemosynthetic endosymbiont of the hydrothermal vent snailAlviniconcha adamantisfrom the Mariana Arc

Breusing

Hauer

Beinart

2022

G3 Genes|Genomes|Genetics

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Chemosynthetic animal-microbe symbioses sustain hydrothermal vent communities in the global deep sea. In the Indo-Pacific Ocean, hydrothermal ecosystems are often dominated by gastropod species of the genus Alviniconcha, which live in association with chemosynthetic Gammaproteobacteria or Campylobacteria. While the symbiont genomes of most extant Alviniconcha species have been sequenced, no genome information is currently available for the gammaproteobacterial endosymbiont of A. adamantis – a comparatively shallow living species that is thought to be the ancestor to all other present Alviniconcha lineages. Here, we report the first genome sequence for the symbiont of A. adamantis from the Chamorro Seamount at the Mariana Arc. Our phylogenomic analyses show that the A. adamantis symbiont is most closely related to Chromatiaceae endosymbionts of the hydrothermal vent snails A. strummeri and Chrysomallon squamiferum, but represents a distinct bacterial species or possibly genus. Overall, functional capacity of the A. adamantis symbiont appeared to be similar to other chemosynthetic Gammaproteobacteria, though several flagella and chemotaxis genes were detected, which are absent in other gammaproteobacterial Alviniconcha symbionts. These differences might suggest potential contrasts in symbiont transmission dynamics, host recognition or nutrient transfer. Furthermore, an abundance of genes for ammonia transport and urea usage could indicate adaptations to the oligotrophic waters of the Mariana region, possibly via recycling of host- and environment-derived nitrogenous waste products. This genome assembly adds to the growing genomic resources for chemosynthetic bacteria from hydrothermal vents and will be valuable for future comparative genomic analyses assessing gene content evolution in relation to environment and symbiotic lifestyle.

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Section: Resultsmentioning

confidence: 99%

Genome assembly of the chemosynthetic endosymbiont of the hydrothermal vent snailAlviniconcha adamantisfrom the Mariana Arc

Breusing

Hauer

Beinart

2022

G3 Genes|Genomes|Genetics

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“…They can move within a single DNA molecule and among different DNA molecules [47] and are a fundamental evolutionary force shaping genome structure and driving genome evolution [15,18]. TEs are enriched in many horizontally transmitted deep-sea symbionts, including symbiotic bacteria of deep-sea mussels, worms, and snails [22][23][24][25]. The proportion of transposases annotated in G. platifrons symbionts is relatively lower than that in symbionts of deep-sea snail Gigantopelta aegis [25].…”

Section: The Function Of Tes In the Adaptive Evolution Of Endosymbiontsmentioning

confidence: 99%

“…Despite their importance in adaptive evolution, our understanding of the contributions of MGEs to deep-sea symbioses, especially those involving horizontally transmitted symbionts, remains in its infancy. However, recent studies have revealed a substantial level of TE enrichment in certain deep-sea horizontally transmitted symbionts [21][22][23][24]. For example, in the bacterial symbionts of deep-sea snails, TEs represent more than 10% of total genes [25].…”

Section: Introductionmentioning

confidence: 99%

Mosaic environment-driven evolution of the deep-sea mussel Gigantidas platifrons bacterial endosymbiont

Sun,

Wang,

Cao

et al. 2023

Microbiome

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Background The within-species diversity of symbiotic bacteria represents an important genetic resource for their environmental adaptation, especially for horizontally transmitted endosymbionts. Although strain-level intraspecies variation has recently been detected in many deep-sea endosymbionts, their ecological role in environmental adaptation, their genome evolution pattern under heterogeneous geochemical environments, and the underlying molecular forces remain unclear. Results Here, we conducted a fine-scale metagenomic analysis of the deep-sea mussel Gigantidas platifrons bacterial endosymbiont collected from distinct habitats: hydrothermal vent and methane seep. Endosymbiont genomes were assembled using a pipeline that distinguishes within-species variation and revealed highly heterogeneous compositions in mussels from different habitats. Phylogenetic analysis separated the assemblies into three distinct environment-linked clades. Their functional differentiation follows a mosaic evolutionary pattern. Core genes, essential for central metabolic function and symbiosis, were conserved across all clades. Clade-specific genes associated with heavy metal resistance, pH homeostasis, and nitrate utilization exhibited signals of accelerated evolution. Notably, transposable elements and plasmids contributed to the genetic reshuffling of the symbiont genomes and likely accelerated adaptive evolution through pseudogenization and the introduction of new genes. Conclusions The current study uncovers the environment-driven evolution of deep-sea symbionts mediated by mobile genetic elements. Its findings highlight a potentially common and critical role of within-species diversity in animal-microbiome symbioses.

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“…The vestimentiferan symbionts are endosymbionts belonging to Gammaproteobacteria with sulfuroxidizing potentials (6,13). By now, no symbiont has been cultured, but more than 10 metagenome-based assembled genomes have been obtained (14)(15)(16)(17)(18), which revealed that vestimentiferan symbionts had similar carbon and energy metabolic potentials. All symbionts harbor the Calvin-Benson-Bassham (CBB) cycle and the reductive tricarboxylic acid cycle (15)(16)(17).…”

Section: Introductionmentioning

confidence: 99%

Integrated multi-approaches reveal unique metabolic mechanisms of Vestimentifera to adapt to deep-sea hydrothermal vents

Sun

Yuan

Sun

et al. 2023

Preprint

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Vestimentiferans (Siboglinidae, Polychaeta) thrive in deep-sea hydrothermal vents and depend on chemosynthetic symbiosis for nutrition. Currently, the central carbon metabolisms, especially the sugar synthesis pathways, of vestimentiferans remain obscure. In this study, the genome of the vestimentiferan Arcovestia ivanovi was obtained. Comparative genomics revealed that, unlike other Polychaeta, vestimentiferans possessed trehaloneogenesis and lacked gluconeogenesis. Transcriptome and metabolome detected the expression of trehalose-6-phosphate synthase (TPS), the key enzyme of trehaloneogenesis, and trehalose in vestimentiferan tissues, especially trophosome, suggesting the possibility of trehalose as the main blood sugar in vestimentiferans. Vestimentiferan TPS was most closely related to arthropod TPS and may be transferred from arthropods via transposons that existed in high densities around the vestimentiferan and arthropod TPS loci. Electron microscopy observed vestimentiferan symbionts with packed glycogen granules. Consistently, glycogen biosynthesis was present in vestimentiferan symbionts but absent in other Siboglinidae symbionts. Together this study revealed that vestimentiferans have evolved unique metabolic mechanisms to adapt to hydrothermal vents by utilizing trehaloneogenesis as the major sugar-synthesizing pathway, which produces trehalose to facilitate tolerance of the stresses (such as high temperature and H2S) of the vents. This study also indicated a critical role of bacterial glycogen biosynthesis in the highly efficient symbiont-vestimentiferan cooperation.

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The worm affair: fidelity and environmental adaptation in symbiont species that co‐occur in vestimentiferan tubeworms

Cited by 4 publications

References 79 publications

Genome assembly of the chemosynthetic endosymbiont of the hydrothermal vent snailAlviniconcha adamantisfrom the Mariana Arc

Genome assembly of the chemosynthetic endosymbiont of the hydrothermal vent snailAlviniconcha adamantisfrom the Mariana Arc

Mosaic environment-driven evolution of the deep-sea mussel Gigantidas platifrons bacterial endosymbiont

Integrated multi-approaches reveal unique metabolic mechanisms of Vestimentifera to adapt to deep-sea hydrothermal vents

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