Dataset Information

By more ways than one: Rapid convergence at hydrothermal vents shown by 3D anatomical reconstruction of Gigantopelta (Mollusca: Neomphalina).

ABSTRACT: Extreme environments prompt the evolution of characteristic adaptations. Yet questions remain about whether radiations in extreme environments originate from a single lineage that masters a key adaptive pathway, or if the same features can arise in parallel through convergence. Species endemic to deep-sea hydrothermal vents must accommodate high temperature and low pH. The most successful vent species share a constrained pathway to successful energy exploitation: hosting symbionts. The vent-endemic gastropod genus Gigantopelta, from the Southern and Indian Oceans, shares unusual features with a co-occurring peltospirid, the 'scaly-foot gastropod' Chrysomallon squamiferum. Both are unusually large for the clade and share other adaptive features such as a prominent enlarged trophosome-like oesophageal gland, not found in any other vent molluscs.Transmission electron microscopy confirmed endosymbiont bacteria in the oesophageal gland of Gigantopelta, as also seen in Chrysomallon. They are the only known members of their phylum in vent ecosystems hosting internal endosymbionts; other vent molluscs host endosymbionts in or on their gills, or in the mantle cavity. A five-gene phylogenetic reconstruction demonstrated that Gigantopelta and Chrysomallon are not phylogenetically sister-taxa, despite their superficial similarity. Both genera have specialist adaptations to accommodate internalised endosymbionts, but with anatomical differences that indicate separate evolutionary origins. Hosting endosymbionts in an internal organ within the host means that all resources required by the bacteria must be supplied by the animal, rather than directly by the vent fluid. Unlike Chrysomallon, which has an enlarged oesophageal gland throughout post-settlement life, the oesophageal gland in Gigantopelta is proportionally much smaller in juveniles and the animals likely undergo a trophic shift during ontogeny. The circulatory system is hypertrophied in both but the overall size is smaller in Gigantopelta. In contrast with Chrysomallon, Gigantopelta possesses true ganglia and is gonochoristic.Key anatomical differences between Gigantopelta and Chrysomallon demonstrate these two genera acquired a similar way of life through independent and convergent adaptive pathways. What appear to be the holobiont's adaptations to an extreme environment, are driven by optimising bacteria's access to vent nutrients. By comparing Gigantopelta and Chrysomallon, we show that metazoans are capable of rapidly and repeatedly evolving equivalent anatomical adaptations and close-knit relationships with chemoautotrophic bacteria, achieving the same end-product through parallel evolutionary trajectories.

SUBMITTER: Chen C

PROVIDER: S-EPMC5333402 | biostudies-literature | 2017 Mar

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

By more ways than one: Rapid convergence at hydrothermal vents shown by 3D anatomical reconstruction of Gigantopelta (Mollusca: Neomphalina).

Chen Chong C Uematsu Katsuyuki K Linse Katrin K Sigwart Julia D JD

BMC evolutionary biology 20170301 1

<h4>Background</h4>Extreme environments prompt the evolution of characteristic adaptations. Yet questions remain about whether radiations in extreme environments originate from a single lineage that masters a key adaptive pathway, or if the same features can arise in parallel through convergence. Species endemic to deep-sea hydrothermal vents must accommodate high temperature and low pH. The most successful vent species share a constrained pathway to successful energy exploitation: hosting symbi ...[more]

PMID: 28249568

Similar Datasets

Project description:The chemosymbiotic gastropod Alviniconcha (Provannidae), first described in 1988, is one of the most emblematic hydrothermal-vent taxa described from the Central Indian Ridge and the Southwest (SW) Pacific. Symbiotic bacteria found in the gill of Alviniconcha are thought to be their principal source of nutrition. In the SW Pacific, species distributions for A. kojimai, A. boucheti - and to a lesser extent A. strummeri - overlap. While Alviniconcha species do not appear to truly co-exist in these highly energetic but spatially limited habitats, certain species regularly co-occur within a single vent field and in rare instances, the same edifice. Past research suggests that SW-Pacific Alviniconcha species might aggregate around fluids with distinct geothermal profiles. These small-scale distribution patterns have been attributed to differences in their symbiont assemblages or host physiologies. However, little is known about the anatomy of most Alviniconcha species, beyond that detailed for the type species Alviniconcha hessleri, whose geographic range does not overlap with other congeners. In fact, species within this genus are currently described as cryptic, despite the absence of any comparative morphological studies to assess this. To test whether the genus is genuinely cryptic and identify any functional differences in host anatomy that might also mediate habitat partitioning in SW Pacific species, the current study examined the morphoanatomy of A. kojimai, A. boucheti and A. strummeri from the Fatu Kapa vent field, an area of hydrothermal activity recently discovered north of the Lau Basin near the Wallis and Futuna Islands and the only known example where all three species occur within adjacent vent fields. A combination of detailed dissections, histology and X-ray computed tomography demonstrate that A. kojimai, A. strummeri and A. boucheti are readily identifiable based on shell morphology and ornamentation alone, and therefore not truly cryptic. These traits provide a rapid and reliable means for species identification. However, aside from some subtle differences in radular morphology, these species of Alviniconcha exhibit conserved anatomical features, providing no evidence that functional host anatomy is implicated in habitat partitioning. This provides support for the current belief that host-species distributions are probably governed by symbiont-mediated physiological factors.

Project description:In this study, sediments were collected from two different sites in the deep-sea hydrothermal region of the South Atlantic Ocean. Two microbial enrichment cultures (H7S and H11S), which were enriched from the sediments collected at two sample sites, could effectively degrade petroleum hydrocarbons. The bacterial diversity was analyzed by high-throughput sequencing method. The petroleum degradation ability were evaluated by gas chromatography-mass spectrometry and gravimetric analysis. We found that the dominant oil-degrading bacteria of enrichment cultures from the deep-sea hydrothermal area belonged to the genera Pseudomonas, Nitratireductor, Acinetobacter, and Brevundimonas. After a 14-day degradation experiment, the enrichment culture H11S, which was obtained near a hydrothermal vent, exhibited a higher degradation efficiency for alkanes (95%) and polycyclic aromatic hydrocarbons (88%) than the enrichment culture H7S. Interestingly, pristane and phytane as biomarkers were degraded up to 90% and 91% respectively by the enrichment culture H11S, and six culturable oil-degrading bacterial strains were isolated. Acinetobacter junii strain H11S-25, Nitratireductor sp. strain H11S-31 and Pseudomonas sp. strain H11S-28 were used at a density ratio of 95:4:1 to construct high-efficiency oil-degrading consortium H. After a three-day biodegradation experiment, consortium H showed high degradation efficiencies of 74.2% and 65.7% for total alkanes and PAHs, respectively. The degradation efficiency of biomarkers such as pristane and high-molecular-weight polycyclic aromatic hydrocarbons (such as CHR) reached 84.5% and 80.48%, respectively. The findings of this study indicate that the microorganisms in the deep-sea hydrothermal area are potential resources for degrading petroleum hydrocarbons. Consortium H, which was artificially constructed, showed a highly efficient oil-degrading capacity and has significant application prospects in oil pollution bioremediation.

Dataset Information

By more ways than one: Rapid convergence at hydrothermal vents shown by 3D anatomical reconstruction of Gigantopelta (Mollusca: Neomphalina).

Publications

By more ways than one: Rapid convergence at hydrothermal vents shown by 3D anatomical reconstruction of Gigantopelta (Mollusca: Neomphalina).

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets