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 ‘Calyptogenamarissinica 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

JAMSTEC collaborates with Nintendo’s Splatoon 2!

I was live on web broadcast for a programme by Niconico as a part of collaborative project between Nintendo and JAMSTEC. The next in-game “splatfest” in the Nintendo Switch game “Splatoon 2” will be between “Mysterious Life” vs “Advanced Technology” teams. I represented “Mysterious Life” team and introduce some related researches in JAMSTEC. Live was from April 21, 13:00-15:00 (in Japanese), and is available for viewing here.

Scaly-foot x Splatoon 2!

The collaboration between JAMSTEC and Splatoon 2 will continue!! http://www.jamstec.go.jp/sp2/

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

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

First Columbellidae snail from deep-sea vent

Lead-authored paper published in Zootaxa today! This paper describes Astyris thermophilus Chen, Watanabe, Araya, 2017, the first Columbellidae species discovered from deep-sea hydrothermal vent ecosystems. Its Japanese name literally means “columbellid from the underworld”. It was found at the Natsu site, Iheya North hydrothermal field, Okinawa Trough, just shy of 1100m depth. http://www.mapress.com/j/zt/article/view/zootaxa.4363.4.13

Astyris thermophilus. A–D. Holotype (UMUT RM32644). E. Paratype #1 (NSMT Mo 78990). F. Paratype #2(UMUT RM32645), periostracum removed to show spiral striae. G. Protoconch of paratype #6, a juvenile specimen (UMUT RM32646). H. Operculum of paratype #2 (UMUT RM32645). I. Radula of paratype #2, UMUT RM32645). Scale bars = 2 mm (A–F),500 μm (G, H), 20 μm (I).

  • Chen C*, Watanabe HK, Araya JF (2017). First columbellid species (Gastropoda: Buccinoidea) from deep-sea hydrothermal vents discovered in Okinawa Trough, Japan. Zootaxa, 4363(4): 592-596. DOI: 10.11646/zootaxa.4363.4.13

Two new vent snails from 2.8km deep in the Indian Ocean!

New lead-authored paper, announcing the discovery of two new peltospirid vent snails, has been published in the peer-reviewed Open Access journal Frontiers in Marine Science! Read for free here: https://doi.org/10.3389/fmars.2017.00392

This paper describes two new species of small gastropods, belonging to the hydrothermal vent endemic family Peltospiridae, from the Longqi hydrothermal vent field (~2785 m deep) on the Southwestern Indian Ridge, Indian Ocean; a new genus was erected to house one of them. The descriptions are based on shell (protoconch, teleoconch, periostracum, shell microstructure), radula, as well as anatomical characters.

Lirapex politus Chen et al., 2017 (~4.5 mm shell height) is the first Indian Ocean representative of genus Lirapex which is also known from eastern Pacific and mid-Atalantic vents, and differs from the other known congeners by its lack of obvious axial sculpture (hence ‘politus’, smooth), as well as a narrower umbilicus and the final 0.5 whorl of the teleoconch being less detached.

Lirapex politus n. sp., scale bars = 1 mm.

Dracogyra subfuscus Chen et al., 2017 (~7 mm shell diameter) is a depressed, globular, coiled peltospirid with a dark periostracum; the genus Dracogyra Chen et al., 2017 was established for this species. It is most similar to Depressigyra globulus Warén & Bouchet, 1989 known from the eastern Pacific, but easily separated from it by a lack of basal notch in the aperture and a more depressed shell with narrower umbilicus. Furthermore, the radula of D. subfuscus is highly characteristic with the central tooth being very wide and compressed.

Dracogyra subfuscus n. gen., n. sp., scale bars = 1 mm.

A Bayesian phylogeny using the mitochondrial COI barcoding gene confirmed the placement of the two new species in clade Neomphalina and family Peltospiridae. The two new species co-occur with two giant holobiont peltospirids including the scaly-foot Chrysomallon squamiferum Chen et al., 2015 and Gigantopelta aegis Chen et al., 2015, and are sometimes found on their body surface. The two new species do not host endosymbiotic bacteria and gut contents suggest that they probably feed on microbial film on chimney surfaces, as well as epibionts of the two larger peltospirids.

  • Chen C*, Zhou Y, Wang C, Copley JT (2017). Two new hot-vent peltospirid snails (Gastropoda: Neomphalina) from Longqi hydrothermal field, Southwest Indian Ridge. Frontiers in Marine Science, 4: 392. DOI: 10.3389/fmars.2017.00392

Two rare gastropods from two new vents!

Lead-authored paper reporting the unexpected discovery of two very rare snails in two new hydrothermal vent sites is now published in the peer-reviewed Open Access journal PeerJ! Read for free at: https://peerj.com/articles/4121/

In this paper, we report the discovery of two very rare gastropods – the calliostomatid Otukaia ikukoae Sakurai, 1994 and the muricid Abyssotrophon soyoae (Okutani, 1959) in newly located hydrothermal vent sites in the Okinawa Trough, Japan. One of the two new sites is named the “Fukai” site after the poisonous forest of the same name in the Studio Ghibli film “Nausicaä of the Valley of the Wind” (1984)! The discovery of these snails represent the second record of Calliostomatidae and the third Muricidae from vents, and also represent range extensions of both species to the southwest, by about 700 km in the case of O. ikukoae. Based on radular characteristics, O. ikukoae is returned to genus Otukaia from Tristichotrochus.

Specimens of the two gastropods collected from hydrothermally influenced areas.(A–D) Tristichotrochus ikukoae from Fukai site, Higashi-Ensei. (E–J) Abyssotrophon soyoae from Crane site, Tarama Hill; (E–H) Specimen #1, (I, J) Specimen #2. Scale bars: (A–D) 1 cm, (E–J) 0.5 cm.

Although this is the first time either species are observed in their natural habitat, both are considered to be occasional invaders of vent ecosystems from surrounding regular sea bottom and not vent endemics given their other records from non-vent environment as well as the fact that they were found in weak diffuse flow venting areas and not focused venting areas. Nevertheless, it is clear that they are able to tolerate, to a certain extent, environmental stresses associated with vents (e.g., raised heavy metal and hydrogen sulfide concentrations). This enables them to access to rich food supplies supported by chemosynthesis primary production, and suggest that vent periphery likely play a key role in the evolution of biological adaptation to hydrothermal vent environment.

The Fukai site (above) and the Crane site (below).

  • Chen C*, Watanabe HK, Miyazaki J, Kawagucci S (2017). Unanticipated discovery of two rare gastropod molluscs from recently located hydrothermally influenced areas in the Okinawa Trough. PeerJ, 5: e4121. http://dx.doi.org/10.7717/peerj.4121/

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