Category: Deep-sea

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.

Two new bivalves from chemosynthetic ecosystems

In two new lead-authored publications in Venus (Journal of the Malacological Society of Japan), we described two new bivalves from chemosynthetic ecosystems of the Western Pacific. One of them is a large vesicomyid clam ‘Calyptogena‘ marissinica Chen, Okutani, Liang & Qiu, 2018 from a methane seep in the South China Sea, and the other is Thermomya sulcata Chen, Okutani, Watanabe & Kojima from a vent in southern Mariana Trough, which is the first cuspidariid found in any chemosynthetic ecosystems.

The two new species:

‘Calyptogena’ marissinica Chen, Okutani, Liang & Qiu, 2018
VESICOMYIDAE
-1372m, Taken by ROV Haima, From ‘Haima’ methane seep, Off southern Hainan Island, Northern sector of the South China Sea, 146.9mm, Paratype #1 (NSMT-Mo 79001)
Known only from the ‘Haima’ hydrocarbon seep in the South China Sea, ‘Calyptogena’ marissinica is a large vesicomyid clam with an average shell length of about 150mm and the largest specimens exceeding 210 mm. It probably relies on endosymbiotic bacteria living inside cells of its much enlarged gills like other vesicomyids, although this warrants further research to confirm. It lives in clusters or colonies and is usually positioned half-buried in mud. Like all large vesicomyid clams, the periostracum is lighter in colouration and more glossy in young individuals. Although a little-varied species, the proportional position of umbo varies slightly among individuals even from the same colony, and the radial ridge running from the umbo to the postero-ventral corner is stronger in younger individuals. It seems to be closely related to ‘Calyptogena’ similaris from the Nankai Trough, Japan, which is far more elongate and with a more concave ventral margin. Calyptogena nanshaensis Xu & Shen 1991 is the only other large vesicomyid reported from the South China Sea, but it clearly differs from ‘C.’ marissinica in hinge morphology as well as having a straight dorsal margin, a bluntly acute posterior end, and also being much smaller in size (only up to 70 mm shell length).

Thermomya sulcata Chen, Okutani, Watanabe & Kojima, 2018
CUSPIDARIIDAE
-2849m, Snail site (12°57.189’N 143°37.166’E), Southern Mariana Trough, Leg. Shigeaki Kojima during DSV Shinkai 6500 Dive #1228 on-board R/V Yokosuka cruise YK10-11, 2010/ix/14, 8.1mm, Holotype (NSMT-Mo 78997)
Thermomya sulcata is the first ever Recent cuspidariid bivalve to be recovered from deep-sea hydrothermal vents or any chemosynthetic ecosystems, and is a handsome species characterised by a compressed, blunt rostrum and sharply raised commarginal ribs on the shell discs. Such upturned and sharp commarginal ribs are unusual among cuspidariids, and the monotypic genus Thermomya was erected to house this species. Furthermore, it is also the first member of the superorder Anomalodesmata to be found at deep-sea vents. So far only known from two specimens taken by the manned submersible DSV Shinkai 6500 from the 2849 m deep Snail hydrothermal site in the Southern Mariana Trough, but it is likely more widely distributed in the periphery of western Pacific vents where small burrowing animals are easily overlooked. It is most likely a carnivorous bivalve like other cuspidariids, using internally generated suction forces to hunt small crustaceans. The two known specimens are 8.1 mm (holotype) and 5.5 mm (paratype) in shell length. Prof. Okutani gave it an elegant Japanese name: “Yume-no-syakushi-gai”, literally meaning “Ladle Shell From Dreams”. This is in reference to the Japanese name, “Yume-Hamaguri” (= “Dream Clam”), of the famously beautiful and rare deep-water venerid clam Circomphalus hiraseanus (Kuroda, 1930) which is also characterised by sharply upturned commarginal ribs and a relatively small size within its family.

New paper on deep-sea fish transcriptomics

A new co-authored paper in BMC Genomics uses transcriptomics to look at molecular adaptation in the deep-sea fish Aldrovandia affinis (Günther, 1877) (Actinopterygii: Halosauridae). Open Access: https://doi.org/10.1186/s12864-018-4720-z 

Abstract

Background

High hydrostatic pressure and low temperatures make the deep sea a harsh environment for life forms. Actin organization and microtubules assembly, which are essential for intracellular transport and cell motility, can be disrupted by high hydrostatic pressure. High hydrostatic pressure can also damage DNA. Nucleic acids exposed to low temperatures can form secondary structures that hinder genetic information processing. To study how deep-sea creatures adapt to such a hostile environment, one of the most straightforward ways is to sequence and compare their genes with those of their shallow-water relatives.

Results

We captured an individual of the fish species Aldrovandia affinis, which is a typical deep-sea inhabitant, from the Okinawa Trough at a depth of 1550 m using a remotely operated vehicle (ROV). We sequenced its transcriptome and analyzed its molecular adaptation. We obtained 27,633 protein coding sequences using an Illumina platform and compared them with those of several shallow-water fish species. Analysis of 4918 single-copy orthologs identified 138 positively selected genes in A. affinis, including genes involved in microtubule regulation. Particularly, functional domains related to cold shock as well as DNA repair are exposed to positive selection pressure in both deep-sea fish and hadal amphipod.

Conclusions

Overall, we have identified a set of positively selected genes related to cytoskeleton structures, DNA repair and genetic information processing, which shed light on molecular adaptation to the deep sea. These results suggest that amino acid substitutions of these positively selected genes may contribute crucially to the adaptation of deep-sea animals. Additionally, we provide a high-quality transcriptome of a deep-sea fish for future deep-sea studies.

  • Lan Y, Sun J, Xu T, Chen C, Tian R, Qiu J-W, Qian P-Y* (2018). De novo transcriptome assembly and positive selection analysis of an individual deep-sea fish. BMC Genomics, 19: 394. DOI: 10.1186/s12864-018-4720-z

Indian Ocean vent stalked barnacle gets a name

A new co-authored paper published in Royal Society Open Science led by Hiromi Kayama Watanabe describes a new species of deep-sea stalked barnacle from Indian Ocean hydrothermal vents: Neolepas marisindica Watanabe, Chen & Chan in Watanabe et al., 2018. Furthermore, we also carried out phylogeographic investigation of deep-sea eolepadid stalked barnacles, leading to a better understanding of their evolution and biogeography. The paper is Open Access and available here: http://rsos.royalsocietypublishing.org/content/5/4/172408

 Abstract
Phylogeography of animals provides clues to processes governing their evolution and diversification. The Indian Ocean has been hypothesized as a ‘dispersal corridor’ connecting hydrothermal vent fauna of Atlantic and Pacific oceans. Stalked barnacles of the family Eolepadidae are common associates of deep-sea vents in Southern, Pacific and Indian oceans, and the family is an ideal group for testing this hypothesis. Here, we describe Neolepas marisindica sp. nov. from the Indian Ocean, distinguished from N. zevinae and N. rapanuii by having a tridentoid mandible in which the second tooth lacks small elongated teeth. Morphological variations suggest that environmental differences result in phenotypic plasticity in the capitulum and scales on the peduncle in eolepadids. We suggest that diagnostic characters in Eolepadidae should be based mainly on more reliable arthropodal characters and DNA barcoding, while the plate arrangement should be used carefully with their intraspecific variation in mind. We show morphologically that Neolepas specimens collected from the South West Indian Ridge, the South East Indian Ridge and the Central Indian Ridge belong to the new species. Molecular phylogeny and fossil evidence indicated that Neolepas migrated from the southern Pacific to the Indian Ocean through the Southern Ocean, providing key evidence against the ‘dispersal corridor’ hypothesis. Exploration of the South East Indian Ridge is urgently required to understand vent biogeography in the Indian Ocean.

Neolepas marisindica, Paratype specimens and in situ photographs

  • Watanabe HK*, Chen C, Marie DP, Takai K, Fujikura K, Chan BKK* (2018). Phylogeography of hydrothermal vent stalked barnacles: a new species fills a gap in the Indian Ocean ‘dispersal corridor’ hypothesis. Royal Society Open Science, 5: 172408. DOI: 10.1098/rsos.172408

New shrimps from hydrothermal vents

A co-author paper of mine, led by Dr. Tomoyuki Komai from Chiba Natural History Museum and Institute, has been published in the journal Zootaxa. In this paper, we described two new species of shrimps in the genus Metacrangon (Caridea: Crangonidae) from hydrothermally influenced areas in Okinawa Trough, Japan.  http://www.mapress.com/j/zt/article/view/zootaxa.4410.1.5

Abstract

Two new species of the crangonid shrimp genus Metacrangon Zarenkov, 1965, are described and illustrated on the basis of materials collected from the Okinawa Trough, Ryukyu Islands, southern Japan, during diving operations of remotely operated vehicles (ROVs): M. ryukyu n. sp. from off Iheya Island, at depth of 986 m; and Metacrangon kaiko n. sp. from NE of Yonaguni Island, at depth of 2205 m. The two new species resemble members of the M. munita (Dana, 1852) species group, but are both characteristic in having setose dactyli on pereopods 4 and 5. Some minor differences in morphology and genetic analysis using partial sequences of the barcoding mitochondrial COI gene support the recognition of the two new species. Holotypes of the two new species were collected from hydrothermally influenced areas, representing a previously unknown habitat for species of Metacrangon.

  • Komai T*, Chen C, Watanabe HK (2018). Two new species of the crangonid genus Metacrangon Zarenkov, 1965 (Crustacea: Decapoda: Caridea) from the Okinawa Trough, Japan. Zootaxa, 4410(1): 97-112. DOI: 10.11646/zootaxa.4410.1.5

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

New scale worms from hydrothermal vents named

Co-authored paper describing hydrothermal vent scale worms (Polychaeta: Polynoidae) has been just published in Frontiers in Marine Science (sorry its not molluscs this time)! It is Open Access and free for all to read here: http://www.frontiersin.org/articles/10.3389/fmars.2018.00112/

In this paper, we described two new vent polynoides including Levensteiniella undomarginata Zhang, Chen & Qiu, 2018 and Branchinotogluma elytropapillata Zhang, Chen & Qiu, 2018; and also redescribed Lepidonotopodium okinawae Sui & Li, 2017 and Branchinotogluma japonicus Miura & Hashimoto, 1991 to include both sex forms. These scale worms are highly sexually dimorphic and in many cases the two sexes have been described as separate species or even genera, highlighting the importance of describing morphological characteristics of both sexes.

  • Zhang Y, Chen C, Qiu J-W* (2018). Sexually dimorphic scale worms (Annelida: Polynoidae) from deep-sea hydrothermal vents in the Okinawa Trough: Two new species and two new sex morphs. Frontiers in Marine Science, 5: 112. DOI: 10.3389/fmars.2018.00112

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.

Three new muricids from Western Pacific

A co-authored paper describing three new muricid gastropods from the western Pacific, has been published in the peer-reviewed journal The Nautilus!

Of the three muricids described in this paper, one is a Chicomurex from the Philippines and Kwajalein Atoll – Chicomurex excelsus Houart, Moe & Chen, 2017. With live-taken specimens known from 150~200 m deep (dead shells have been collected as shallow as 60 m), this species is characterised by a long siphonal canal which carries intricately webbed fronds but lacks in strong recurved spines. This unique siphonal canal sculpture, as well as a lower spire and a more angular final teleoconch whorl, separate it from C. gloriosus (Shikama, 1977), the closest congener which it co-occurs with.

Chicomurex excelsus Houart, Moe & Chen, 2017, Holotype (7-9) and Paratype CM (10-11)

The other two species described are from Fiji and in the genus Chicoreus (Triplex) – Chicoreus kaitomoei Houart, Moe & Chen, 2017 and Chicoreus aquilus Houart, Moe & Chen, 2017, both being small-sized (<40 mm) for the genus. Although C. kaitomoei has been confused with C. aculeatus (Lamarck, 1822) and C. nobilis Shikama, 1977, these two species have multispiral protoconchs implying planktotrophic development unlike C. kaitomoei which has a pausispiral protoconch implying lecithotrophic development. The teleoconch of C. kaitomoei is by very short variceal spines (except those from P1-3) and a siphonal canal with three abapically bent spines concentrated on the anterior half. This species inhabit shallow waters around 9~30 m deep and is named after Kaito Moe, son of Chris Moe.

Chicomurex kaitomoei Houart, Moe & Chen, 2017, Holotype (21-23) and Paratype CM (24-25)

Finally, C. aquilus which is only known from the holotype taken from 31~40 m deep in Fiji, is a highly distinctive species closest to C. rubescens (Broderip, 1833) and a few other species belonging to Chicoreus “group 2” (sensu Houart, 1992) but easily distinguished by differences in varice and aperture characteristics.

Chicoreus aquilus Houart, Moe & Chen, 2017, Holotype

Houart R*, Moe C, Chen C (2017). Description of three new muricids (Gastropoda: Muricidae: Muricinae) from the Philippines and Fiji. The Nautilus, 131(4): 207-216.

Unveiling the “Yokosuka” hydrothermal vent site

A new paper on the discovery of a new hydrothermal vent field has been published in the peer-reviewed Open Access journal Royal Society Open Science! I acted as the corresponding author. Read for free here: http://rsos.royalsocietypublishing.org/content/4/12/171570

We report, in this paper, the discovery of the “Yokosuka” site – the deepest and hottest hydrothermal vent field in the Okinawa Trough, Japan. At 2190 m deep, this new vent field is highly active and exhibit vigorous focused venting from ‘black smoker’ chimneys, the highest temperature recorded being 364°C.

Vent chimneys in the “Yokosuka site”

Fauna and microbiota in the new site were generally similar to other Okinawa Trough vents, although with some different characteristics. For fauna, the dominance of the deep-sea mussel Bathymodiolus aduloides is surprising given other nearby vent sites are usually dominated by B. platifrons and/or B. japonicus, and a sponge field in the periphery dominated by Poecilosclerida is unusual for vents in this region. In terms of microbiota, the H2-rich vent fluids in one of the chimneys resulted in the dominance of hydrogenotrophic chemolithoautotrophs such as Thioreductor and Desulfobacterium. In terms of vent fluid, notable Cl depletion (130 mM) and high concentrations of both H2 and CH4 (~10 mM) probably result from subcritical phase separation and thermal decomposition of sedimentary organic matter. Our insights from the Yokosuka site implies that although the distribution of vent animal species may be linked to depth, the constraint is perhaps not water pressure and resulting chemical properties of the vent fluid but instead physical properties of the surrounding seawater.

Overview of the “Yokosuka site”

We named the new vent site after R/V Yokosuka, the supporting vessel of DSV Shinkai6500 and AUV URASHIMA.

R/V Yokosuka, which caught the first signs of the “Yokosuka site” using a Multi-Beam Echo Sounder

  • Miyazaki J, Kawagucci S, Makabe A, Takahashi A, Kitada K, Torimoto J, Matsui Y, Tasumi E, Shibuya T, Nakamura K, Horai S, Sato S, Ishibashi J, Kanzaki H, Nakagawa S, Hirai M, Takaki Y, Okino K, Watanabe HK, Kumagai H, Chen C* (2017). Deepest and hottest hydrothermal activity in the Okinawa Trough: Yokosuka site at Yaeyama knoll. Royal Society Open Science, 4: 171570. http://dx.doi.org/10.1098/rsos.171570