A new metamorphosis revealed using synchrotron CT

A new lead-authored paper published in Proceedings of the Royal Society B: Biological Sciences reveals a previously undocumented type of metamorphosis exhibited by the deep-sea vent snail Gigantopelta using synchrotron micro-CT.

Press coverage by the New York Times: This Snail Goes Through Metamorphosis. Then It Never Has to Eat Again. by JoAnna Klein.

Metamorphosis, such as the transformation from caterpillar to butterfly or tadpole to frog, is one of the most exquisite phenomena in animal life history, and has been thought to always involve a clearly correlated transformation in both external and internal morphology. We used state-of-the-art 3D reconstruction with synchrotron CT data to reveal that the snail Gigantopelta chessoia from deep-sea hydrothermal vents goes through a further internal transformation in anatomy after settlement, which is not apparent from external morphology. Termed ‘cryptometamorphosis’, this newly discovered phenomenon allows Gigantopelta to switch from ingesting food to relying entirely on symbionts. The possibility of an additional, ‘hidden’, metamorphosis as adults also have a profound impact on understanding the energy flow in ecosystems, as it means we may not be able to tell the trophic role of an animal without detailed anatomical observations. Modelling food webs and the energetic flow in ecosystems is crucial in their conservation, especially in a time of rapid environmental changes, and our results highlight the importance of in-depth knowledge on the life history of animal species in order to model ecosystems accurately.

3D reconstructions of the digestive system in Gigantopelta chessoia, at body lengths (a) 2.2 mm, (b) 3.5 mm, (c)5.1 mm, (d) 7.8 mm, (e) 12.2 mm, and (f ) 23.0 mm. The ‘trophosome’ is indicated by yellow, shades of blue indicate other parts of the digestive system, including buccalmass, oesophagus, stomach, digestive gland, and intestine. Scale bars = 1 mm for all parts.

Using mitogenomes to reveal phylogeny and evolution of scale worms

A paper I co-authored has been published in Molecular Phylogenetics and Evolution! In this work led by Yanjie Zhang, we sequenced mitochondrial genomes from deep-sea scale worms (Annelida: Aphroditiformia) to study their phylogeny and evolution. Here’s a link that gives you free access to the full paper for the next 50 days: https://authors.elsevier.com/c/1Wt5g3m3nMqWNm

Highlights

  • We recovered 15 mitochondrial genomes and 16 18S and 28S genes from 16 scale worms
  • Eulepethidae and Aphroditidae are sister to the other families
  • Branchinotogluminae and Macellicephalinae are paraphyletic
  • Mitochondrial gene orders of deep-sea species have two novel arrangement patterns
  • Mitochondrial genomes of deep-sea species show relaxed purifying selection

 

Zhang Y, Sun J, Rouse GW, Wiklund H, Pleijel F, Watanabe HK, Chen C, Qian P-Y, Qiu J-W* (2018). Phylogeny, evolution and mitochondrial gene order rearrangement in scale worms (Aphroditiformia, Annelida): Insights from low-coverage genome sequencing. Molecular Phylogenetics and Evolution, 125: 220-231. DOI: 10.1016/j.ympev.2018.04.002

Strange ‘stacking’ behaviour seen in vent snails

A short paper describing the strange behaviour of forming hanging ‘stacks’ exhibited by the vent snail genus Gigantopelta has been published in the journal Plankton and Benthos Research! This behaviour is probably related to reproduction. The paper is open access and available for view here: https://doi.org/10.3800/pbr.13.25“Mating stacks” have been widely documented in calyptraeid slipper limpets, which are protandric and exhibit sequential hermaphroditism. Gigantopelta is a genus of peltospirid snails endemic to deep-sea hydrothermal vents containing two species, one distributed on the East Scotia Ridge in the Southern Ocean and another on the Southwest Indian Ridge in the Indian Ocean. Here, we report the observation that both species form extensive (often >15 individuals) “snail chains”. These chains are potentially analogous to ‘mating stacks’ of calyptraeids, or alternatively, maybe a behaviour to facilitate spermatophore transfer. Both Gigantopelta species apparently have separate sexes and are sexually mature at a small size. However, it remains unclear whether they undergo sex change during their life.

Snail chains formed by Gigantopelta chessoia (left) and G. aegis (right)

  • Chen C*, Marsh L, Copley JT (2018). Is it sex in chains? Potential mating stacks in deep-sea hydrothermal vent snails. Plankton and Benthos Research, 13(1): 25-27.

New paper characterises microbes associated with Antarctic vent snail

New co-authored paper published in the peer-reviewed journal “Polar Biology“! The article can be read for free via the following link: http://rdcu.be/tWBe .

In this paper, we characterised microbes associated with the recently discovered Antarctic vent snail Gigantopelta chessoia Chen et al., 2015. It has been known that this snail hosts endosymbionts in an much enlarged oesophageal gland, but the details about the symbiont’s phylogenetic position has not been published. We show that the endosymbiont is a Gammaproteobacteria related to sulfur-oxidising bacteria from cold seeps and other animals living in chemosynthetic ecosystems. Also revealed is a more diverse epibiont community on the gill surface, including members belonging to Gamma, Epsilon and Deltaproteobacteria. Interestingly, the endosymbiont Gammaproteobacteria strain was also found on the gill surface but not in the surrounding water column. Given that juveniles of this species is regularly recovered from within the adults’ mantle cavity, this suggests they may acquire the symbionts directly from the gills of adult snails.

Gigantopelta chessoia and its associated microbial community

New paper shows a vent squat lobster actively cultivates its epibionts!

A co-authored paper about the mechanism of symbiosis in a deep-sea vent crustacean is now published in the journal “Deep Sea Research Part I”: https://authors.elsevier.com/c/1Vm3k3RueHIHRB . Shinkaia crosnieri Baba & Williams, 1998 is a vent-endemic squat lobster with dense setae / hair on its ventral surface. Much like its distant (convergently evolved) cousin, the “yeti-crab” Kiwa, these setae are full of epibiotic bacteria. Recently, S. crosnieri became the first vent animal where the nutritional reliance on epibiotic bacteria was experimentally demonstrated. In this study, we take a step further and show that S. crosnieri actively utilises and produces water current that significantly increases the productivity (chemosynthetic activity) of its epibionts. This means the squat lobster is actively cultivating / farming its own food — the first example of such behavioural adaptation demonstrated among epibiont-hosting animals inhabiting chemosynthetic ecosystems.

Dense ventral setae of S. crosnieri (left) and epibionts on the setae (right)

Through a series of experiments measuring the rate of chemosynthesis (sulfide consumption rate), it was revealed that the rate in epibionts significantly increased when water current was produced. Then, living S. crosnieri individuals were shown to produce an endogenous water flow to the ventral setae through elegant current visualisation using fluorescent particles. Finally, behavioral experiment indicated that S. crosnieri likely exhibit rheotaxis in its natural habitat, meaning it uses existing water current in addition to self-generated ones to increase the productivity of its epibionts = food.

Endogenous water flow generated by S. crosnieri, left: artist’s impression (by Emi Hada) and right: visualisation of the actual current speed generated

Watsuji T, Tsubaki R, Chen C, Nagai Y, Nakagawa S, Yamamoto M, Nishiura D, Toyofuku T, Takai K (2017). Cultivation mutualism between a deep-sea vent galatheid crab and chemosynthetic epibionts. Deep-Sea Research Part I: Oceanographic Research Papers, 127: 13-20. DOI: 10.1016/j.dsr.2017.04.012

New paper on adaptation of vent/seep scale worms published!

New co-authored paper on the adaptation and evolution of vent scale worms (polynoid polychaetes) published in Scientific Reports! The article is open access and free to read here: http://www.nature.com/articles/srep46205

Scale worms inhabit a great variety of environments ranging from very shallow water down to kilometres deep and are often an important member of chemosynthetic ecosystems such as vents, often living in close proximity to hot black smokers. In this study, we sequenced the transcriptomes of two deep-sea scale worms inhabiting hydrothermal vents and hydrocarbon seeps and one shallow water counterpart that was rather closely related. By comparing the three transcriptomes, we were able to elucidate selective amino acid usage, positively selected genes, highly expressed genes, and potentially duplicated genes, thereby shedding light on how the scale worms evolved to become successful members of deep-sea chemosynthetic communities. These are the first deep-sea scale worm transcriptomes ever reported.

Highly expressed genes in B. pettiboneae (vent/seep), Lepidonotopodium sp. (vent) and H. imbricata (shallow water relative).(a) Percentage of genes participated in different cellular processes. (b) Expression level for gene groups participated in different cellular processes.

Most significant among our findings was the significance of genes related to haemoglobin. The two deep-sea polynoids chosen for this study, in the genera Branchipolynoe and Lepidonotopodium, are shown to have adopted different yet equally effective ways to cope with the oxygen-poor chemosynthetic ecosystems. Branchipolynoe rapidly evolved a novel tetra-domain haemoglobin which is highly effective in oxygen transport, whereas Lepidonotopodium increased the expression levels of standard single-domain haemoglobin to four times as high as Branchipolynoe. These results indicate that dealing with hypoxic environment is a key element in becoming successful in deep-sea vents and seeps.

Zhang Y [Yanjie], Sun J, Chen C, Watanabe HK, Feng D, Zhang Y [Yu], Chiu JMY, Qian P-Y, Qiu J-W (2017). Adaptation and evolution of polynoid scale-worms (Annelida: Polynoidae): insights from transcriptome comparison among two deep-sea and a shallow-water species. Scientific Reports, 7: 46205. http://doi.org/10.1038/srep46205