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

Background 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. Results 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. Conclusions 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

Cryptic niche switching in a chemosymbiotic gastropod

Life stages of some animals, including amphibians and insects, are so different that they have historically been seen as different species. ‘Metamorphosis’ broadly encompasses major changes in organism bodies and, importantly, concomitant shifts in trophic strategies. Many marine animals have a biphasic lifestyle, with small pelagic larvae undergoing one or more metamorphic transformations before settling into a permanent, adult morphology on the benthos. Post-settlement, the hydrothermal vent gastropod Gigantopelta chessoia experiences a further, cryptic metamorphosis at body sizes around 5–7 mm. The terminal adult stage is entirely dependent on chemoautotrophic symbionts; smaller individuals do not house symbionts and presumably depend on grazing. Using high-resolution X-ray microtomography to reconstruct the internal organs in a growth series, we show that this sudden transition in small but sexually mature individuals dramatically reconfigures the organs, but is in no way apparent from external morphology. We introduce the term ‘cryptometamorphosis’ to identify this novel phenomenon of a major body change and trophic shift, not related to sexual maturity, transforming only the internal anatomy. Understanding energy flow in ecosystems depends on the feeding ecology of species; the present study highlights the possibility for adult animals to make profound shifts in biology that influence energy dynamics

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

http://www.godac.jamstec.go.jp/darwin/cruise/natsushima/nt05-12/

Intracellular isotope localization in Ammonia sp. (Foraminifera) of oxygen-depleted environments : results of nitrate and sulfate labeling experiments

© The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Microbiology 7 (2016): 163, doi:10.3389/fmicb.2016.00163.Some benthic foraminiferal species are reportedly capable of nitrate storage and denitrification, however, little is known about nitrate incorporation and subsequent utilization of nitrate within their cell. In this study, we investigated where and how much 15N or 34S were assimilated into foraminiferal cells or possible endobionts after incubation with isotopically labeled nitrate and sulfate in dysoxic or anoxic conditions. After 2 weeks of incubation, foraminiferal specimens were fixed and prepared for Transmission Electron Microscopy (TEM) and correlative nanometer-scale secondary ion mass spectrometry (NanoSIMS) analyses. TEM observations revealed that there were characteristic ultrastructural features typically near the cell periphery in the youngest two or three chambers of the foraminifera exposed to anoxic conditions. These structures, which are electron dense and ~200–500 nm in diameter and co-occurred with possible endobionts, were labeled with 15N originated from 15N-labeled nitrate under anoxia and were labeled with both 15N and 34S under dysoxia. The labeling with 15N was more apparent in specimens from the dysoxic incubation, suggesting higher foraminiferal activity or increased availability of the label during exposure to oxygen depletion than to anoxia. Our results suggest that the electron dense bodies in Ammonia sp. play a significant role in nitrate incorporation and/or subsequent nitrogen assimilation during exposure to dysoxic to anoxic conditions.This work was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan (Young Scientists B No. 22740340 and Scientific Research C No. 24540504 to HN), an Invitation Fellowship for Research in Japan to JB by Japan Society for the Promotion of Science (JSPS), the Robert W. Morse Chair for Excellence in Oceanography at WHOI to JB, and The Investment in Science Fund at WHOI to JB

Data from: Cryptic niche switching in a chemosymbiotic gastropod

Life stages of some animals, including amphibians and insects, are so different that they have historically been seen as different species. ‘Metamorphosis’ broadly encompasses major changes in organism bodies and, importantly, concomitant shifts in trophic strategies. Many marine animals have a biphasic lifestyle, with small pelagic larvae undergoing one or more metamorphic transformations before settling into a permanent, adult morphology on the benthos. Post-settlement, the hydrothermal vent gastropod Gigantopelta chessoia experiences a further, cryptic metamorphosis at body sizes around 5-7 mm. The terminal adult stage is entirely dependent on chemoautotrophic symbionts; smaller individuals do not house symbionts, and presumably depend on grazing. Using high resolution x-ray microtomography to reconstruct the internal organs in a growth series, we show this sudden transition in small but sexually mature individuals dramatically reconfigures the organs, but is in no way apparent from external morphology. We introduce the term ‘cryptometamorphosis’ to identify this novel phenomenon of a major body change and trophic shift, not related to sexual maturity, transforming only the internal anatomy. Understanding energy flow in ecosystems depends on the feeding ecology of species; the present study highlights the possibility for adult animals to make profound shifts in biology that influence energy dynamics