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Dr. Chong CHEN

Dr. Chong CHEN

Deep-sea biologist. Malacologist. Evolutionary biologist. "Mollusc collector", photographer.

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Gallery of Publications

A co-authored paper published in the Journal of Eukaryotic Microbiology reports an abundance of chitinous structures in Chilostomella ovoidea, a deep-sea benthic foraminifera. Such structures have not been found in any other foraminifera. We revealed the distribution of these structures within an entire individual using 3D reconstruction (over 400 slices at 500 nm thick each!), and discussed their potential functions. The paper is OPEN ACCESS: https://onlinelibrary.wiley.com/doi/10.1111/jeu.12828 <br />
Thanks to all co-authors, including Masashi Tsuchiya!<br />
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Abstract<br />
Benthic foraminifera, members of Rhizaria, inhabit a broad range of marine environments and are particularly common in hypoxic sediments. The biology of benthic foraminifera is key to understanding benthic ecosystems and relevant biogeochemical cycles, especially in hypoxic environments. Chilostomella is a foraminiferal genus commonly found in hypoxic deep‐sea sediments and has poorly understood ecological characteristics. For example, the carbon isotopic compositions of their lipids are substantially different from other co‐occurring genera, probably reflecting unique features of its metabolism. Here, we investigated the cytoplasmic and ultrastructural features of Chilostomella ovoidea from bathyal sediments of Sagami Bay, Japan, based on serial semi‐thin sections examined using an optical microscope followed by a three‐dimensional reconstruction, combined with TEM observations of ultra‐thin sections. Observations by TEM revealed the presence of abundant electron‐dense structures dividing the cytoplasm. Based on histochemical staining, these structures are shown to be composed of chitin. Our 3D reconstruction revealed chitinous structures in the final seven chambers. These exhibited a plate‐like morphology in the final chambers but became rolled up in earlier chambers (toward the proloculus). These chitinous, plate‐like structures may function to partition the cytoplasm in a chamber to increase the surface/volume ratio and/or act as a reactive site for some metabolic functions.<br />
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Nomaki H*, Chen C, Oda K, Tsuchiya M, Tame A, Uematsu K, Isobe N (2020). Abundant chitinous structures in Chilostomella (Foraminifera, Rhizaria) and their potential functions. Journal of Eukaryotic Microbiology, Early View. DOI: 10.1111/jeu.12828
The first vesicomyid clam genome! We present a high-quality, chromosome-level genome assembly of the chemosymbiotic deep-sea cold seep clam Archivesica marissinica, as well as the genome of its endosymbiont. Analysing the two genomes together provided new insights on the co-evolution and genomic integration in this holobiont. This co-authored paper is now published online in Molecular Biology and Evolution and it is Open Access: https://academic.oup.com/mbe/advance-article/doi/10.1093/molbev/msaa241/5909661<br />
Thanks to all collaborators, including Ting Xu and Jin Sun! <br />
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Abstract: <br />
Endosymbiosis with chemosynthetic bacteria has enabled many deep-sea invertebrates to thrive at hydrothermal vents and cold seeps, but most previous studies on this mutualism have focused on the bacteria only. Vesicomyid clams dominate global deep-sea chemosynthesis-based ecosystems. They differ from most deep-sea symbiotic animals in passing their symbionts from parent to offspring, enabling intricate coevolution between the host and the symbiont. Here, we sequenced the genomes of the clam Archivesica marissinica (Bivalvia: Vesicomyidae) and its bacterial symbiont to understand the genomic/metabolic integration behind this symbiosis. At 1.52 Gb, the clam genome encodes 28 genes horizontally transferred from bacteria, a large number of pseudogenes and transposable elements whose massive expansion corresponded to the timing of the rise and subsequent divergence of symbiont-bearing vesicomyids. The genome exhibits gene family expansion in cellular processes that likely facilitate chemoautotrophy, including gas delivery to support energy and carbon production, metabolite exchange with the symbiont, and regulation of the bacteriocyte population. Contraction in cellulase genes is likely adaptive to the shift from phytoplankton-derived to bacteria-based food. It also shows contraction in bacterial recognition gene families, indicative of suppressed immune response to the endosymbiont. The gammaproteobacterium endosymbiont has a reduced genome of 1.03 Mb but retains complete pathways for sulfur oxidation, carbon fixation, and biosynthesis of 20 common amino acids, indicating the host’s high dependence on the symbiont for nutrition. Overall, the host–symbiont genomes show not only tight metabolic complementarity but also distinct signatures of coevolution allowing the vesicomyids to thrive in chemosynthesis-based ecosystems.<br />
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Ip JC-H, Xu T, Sun J, Li R, Chen C, Lan Y, Han Z, Zhang H, Wei J, Wang H, Tao J, Cai Z, Qian P-Y, Qiu J-W* (2020). Host-endosymbiont genome integration in a deep-sea chemosymbiotic clam. Molecular Biology and Evolution, msaa241. DOI: 10.1093/molbev/msaa241
Paper documenting a case of extreme shell morphology variation in a vetigastropod limpet has been published in Marine Biodiversity! We found a new deep-sea hot vent site in the Okinawa Trough where Lepetodrilus nux (Vetigastropoda: Lepetodrilidae) lived on three substrate types, the shell morphology shifting according to the substrate shape. Previously, this level of intraspecific variation was well-known from true limpets, but this example adds to the existing evidence that any of the 54 independently-evolved limpet lineages may exhibit similar variation. The new vent site, “Ghibli Site”, is named after Studio Ghibli and includes structures such as “Laputa Chimney” and “Howl’s Castle”. Read the paper for free here: https://rdcu.be/caNYQ<br />
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Abstract: <br />
Having a non-coiled, limpet-like shell is a characteristic shared by numerous gastropod molluscs, including many lineages outside the true limpets (Patellogastropoda) where it has evolved convergently. The shell shape of limpet-formed gastropods has often been used as a key taxonomic character, and although studies have shown that it can vary depending on the substrate morphology these have mostly been examples from true limpets. Over a dozen origins of limpet-form are known in Vetigastropoda, and these limpets are still generally assumed to have rather stable shell forms that are useful for taxonomy and species identification. Here, we show that the vetigastropod limpet Lepetodrilus nux (Okutani, Fujikura & Sasaki, 1993) from a deep-sea hot vent in the Okinawa Trough develop distinct shell forms when living on different substrate types. Sequences of the barcoding region of the mitochondrial cytochrome c oxidase subunit I gene among the three forms only differed by 0.31–0.63% (K2P distance) in a 637 bp alignment, in line with the differences in shell morphology being intraspecific. The extent of shell form shift seen in this species is likely the largest reported for a vetigastropod limpet and provide further evidence that such plasticity is not phylogenetically constrained but is an intrinsic part of having a limpet-like shell. <br />
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Chen C, Watanabe-Kayama H (2020). Substrate-dependent shell morphology in a deep-sea vetigastropod limpet. Marine Biodiversity, 50(6): 104. DOI: 10.1007/s12526-020-01135-y
Co-authored paper examining genetic connectivity and differences in gene expression patterns between a hot vent and a cold seep population of deep-sea squat lobster Shinkaia crosnieri now published in Frontiers in Marine Science! A collaboration with colleagues including Ting Xu and Jin Sun. The paper is Open Access and can be freely accessed here: https://www.frontiersin.org/articles/10.3389/fmars.2020.587686<br />
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Abstract: <br />
Shinkaia crosnieri (Decapoda: Munidopsidae) is a squat lobster that dominates both deep-sea hydrothermal vent and methane seep communities in the Western Pacific. Previous studies comparing S. crosnieri living in these two types of habitats have suffered from methodological and/or sample size limits. Here, using transcriptome-wide single nucleotide polymorphisms (SNPs) markers from 44 individuals of S. crosnieri, we reveal the extent of genetic connectivity between a methane seep population in the South China Sea and a hydrothermal vent population in the Okinawa Trough, as well as their signatures of local adaptation. Analysis of differentially expressed genes (DEGs) between these two populations and population-specific genes (PSGs) revealed that a large number of unigenes, such as cytochrome P450 (CYP), glutathione S-transferase (GST) and peroxiredoxin 6 (Prdx6) related to oxidoreductase, and sulfur dioxygenase (ETHE1) and chondroitin 4-sulfotransferase 11 (CHST11) related to sulfur metabolism, showed opposite expression patterns in these two populations. Data subsampling in this study revealed that at least five individuals of S. crosnieri per site are required to generate reliable results from the differential gene expression analysis. Population genetic analyses based on 32,452 SNPs revealed clear genetic differentiation between these two populations with an FST value of 0.07 (p < 0.0005), and physical oceanographic modeling of the ocean currents in middle and deep layers also suggests a weak connection between these two sites. Analysis of outlier SNPs revealed 345 unigenes potentially under positive selection, such as sarcosine oxidase/L-pipecolate oxidase (PIPOX), alanineglyoxylate transaminase/serine-glyoxylate transaminase/serine-pyruvate transaminase (AGXT), and Cu-Zn superoxide dismutase (SOD1). Among the differentially expressed genes and genes with amino acid substitutions between the two sites are those related to oxidation resistance and xenobiotic detoxification, indicating local adaptation to the specific environmental conditions of each site. Overall, exploring the population structure of S. crosnieri using transcriptome-wide SNP markers resulted in an improved understanding of its molecular adaptation and expression plasticity in vent and seep ecosystems.<br />
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Xiao Y# / Xu T#, Sun J, Wong WC, Kwan YH, Chen C, Qiu J-W*, Qian P-Y* (2020). Population genetic structure and gene expression plasticity of the deep-sea vent and seep squat lobster Shinkaia crosnieri. Frontiers in Marine Science, 7: 587686. DOI: 10.3389/fmars.2020.587686
A co-authored paper describing two deep-sea polychaete worms in the genus Hesiolyra has been published online in Deep-Sea Research Part I! Previously, only one species was recognised in Hesiolyra and it was thought to be cosmopolitan, but our results show that this genus is in fact more diverse. The two newly named worms are from Indian Ocean hot vents, with H. longqiensis from the Southwest Indian Ridge and H. heteropoda n. sp. from Central Indian and Carlsberg ridges. Many thanks to collaborators including Ting Xu, Yanjie Zhang, Hiromi Watanabe-Kayama, among others! Link: https://doi.org/10.1016/j.dsr.2020.103401<br />
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Abstract:<br />
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Although many deep-sea species are considered to have transoceanic distribution, this assumption has rarely been critically tested. Using Hesiolyra (Hesionidae) as a case study, we show that careful molecular and morphological analyses are required for refuting/accepting claims about such wide distribution. Hesiolyra is a genus of polychaetes commonly found in hydrothermal vents of the Eastern Pacific, Atlantic and Indian Ocean. Nevertheless, H. bergi Blake, 1985, a species originally described from the Eastern Pacific Rise (EPR), is the only recognized species in this genus. Phylogenetic analyses based on the COI and 16 S rRNA genes revealed two monophyletic clades that were distinct from a clade consisting of H. bergi sequences. We erected two new species of Hesiolyra, herein named as H. longqiensis n. sp. from the Southwest Indian Ridge (SWIR) and H. heteropoda n. sp. from the Central Indian Ridge (CIR) and the Carlsberg Ridge (CR). Among them, H. longqiensis n. sp. is more closely related to H. bergi than to H. heteropoda n. sp. . Morphologically, the two newly described species can be easily distinguished from H. bergi. The notopodia and neuropodia of H. bergi and H. longqiensis n. sp., are of similar sizes, but the morphology of their lyrate chaetae and their dorsal cirri alternation patterns are different. In H. heteropoda n. sp., the notopodia are remarkably slimmer than the neuropodia, and it lacks lyrate chaetae. Overall, in this report two new species of Hesiolyra from the Indian Ocean ridges and show that the distribution of H. bergi is restricted to the Eastern Pacific Rise. Future exploration of other mid-ocean ridges is required to discover the true diversity of this genus of polychaetes inhabiting hydrothermal vent fields.<br />
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Wang Z, Xu T, Zhang Y, Zhou Y, Liu Z, Chen C, Watanabe HK, Qiu J-W* (2020). Molecular phylogenetics and morphological analyses of the ‘monospecific’ Hesiolyra (Annelida: Hesionidae) reveal two new species. Deep-Sea Research Part I: Oceanographic Research Papers, 103401. DOI: 10.1016/j.dsr.2020.103401
Co-authored paper led by Hiromi Watanabe-Kayama has been published in Journal of Crustacean Biology! We show that the deep-sea hot vent crab Gandalfus yunohana has high genetic connectivity across its known range with the gene-flow on the Izu-Bonin-Mariana Arc being predominantly southwards. For the first time we confirm that the Gandalfus from Okinawa Trough is indeed G. yunohana, as previously speculated. The article is OPEN ACCESS: https://doi.org/10.1093/jcbiol/ruaa045<br />
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Abstract: <br />
Genetic connectivity provides a basis for evaluating the resilience of animal communities by elucidating gene flow and serves as a proxy for realized dispersal through planktonic larval dispersal, settlement, and reproductive success. Gandalfus yunohana (Takeda, Hashimoto & Ohta, 2000) is a brachyuran crab endemic to deep-sea hydrothermal vents in the northwestern Pacific. Although an iconic and often dominant species, the connectivity among its populations is yet to be examined. We obtained barcoding sequences of the mitochondrial COI gene of G. yunohana from four vent fields including two on the Izu Arc, one on the northern Mariana Arc, and one in the Okinawa Trough. Genetic diversity of populations on the Izu and northern Mariana arcs were similar and shared the dominant haplotypes, showing no genetic subdivision regardless of the habitat depth. The Okinawa Trough population, for which only one specimen was available, was not genetically different from specimens from the Izu/Mariana arc populations. Estimation of the number of immigrants among populations suggests that the migration from north to south is higher than in the reverse direction. Our results resonate with previous laboratory-culture experiments, suggesting a high dispersal capability for G. yunohana. Visual observations and sampling, however, suggest that G. yunohana is exceedingly rare in the Okinawa Trough. This perhaps results from a lack of sufficient larval supply from the Izu-Bonin-Mariana Arc vents, and there may not be a reproductive population in the Okinawa Trough.<br />
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Watanabe HK*, Chen C, Kojima S, Kato S, Yamamoto H (2020). Population connectivity of the crab Gandalfus yunohana (Takeda, Hashimoto & Ohta, 2000) (Decapoda, Brachyura: Bythograeidae) from deep-sea hydrothermal vents in the northwestern Pacific. Journal of Crustacean Biology, Advance Access. DOI: 10.1093/jcbiol/ruaa045
Our paper on an endosymbiont-hosting vesicomyid clam from Antarctica has been published in Polar Biology! We show that all live pliocardiine clams so far found in vents and seeps around Antarctica are Archivesica puertodeseadoi, which was previously only known from off Argentina. We show using in situ observations and experimental respirometry that these clams are quite flexible in their ecophysiology, allowing them to thrive in a range of chemosynthesis-based ecosystems. The paper is OPEN ACCESS: https://link.springer.com/article/10.1007/s00300-020-02717-z<br />
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Abstract: <br />
Geothermal energy provides an important resource in Antarctic marine ecosystems, exemplified by the recent discovery of large-sized chemosymbiotic vesicomyid bivalves (subfamily Pliocardiinae) in the Southern Ocean. These clams, which we identified as Archivesica s.l. puertodeseadoi, have been reported as dead shells in areas previously covered by Larsen A and B ice shelves (eastern Antarctic Peninsula) and as live animals from active hydrothermal sites in the Kemp Caldera (South Sandwich Arc) at depths of 852–1487 m. Before, A. puertodeseadoi was known only from its type locality in the Argentine Sea, so we considerably extend the range of the species. Observations taken by remotely operated vehicle (ROV) footage show that the clams can live buried in sediment, or epilithically on the surface of rocks in diffuse geothermal flow. Experimental respirometry was conducted at surface pressure on individual bivalves acclimated to either their habitat temperature (4 °C) or elevated temperature (10 °C). The range of standard metabolic rates, from 3.13 to 6.59 (MO2, μmol O2 h−1 g−1 dry tissue mass), is similar to rates measured ex situ for other species in this clade, and rates did not differ significantly between temperature groups. Taken together, these data indicate a range of ecophysiological flexibility for A. puertodeseadoi. Although adapted to a specialist mode of life, this bivalve exploits a relatively broad range of habitats in the Southern Ocean: within sulphidic sediments, epilithically in the presence of diffuse sulphidic flow, or in deep methane-enriched seawater trapped under ice. <br />
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Linse K, Sigwart JD*, Chen C, Krylova EM (2020). Ecophysiology and ecological limits of symbiotrophic vesicomyid bivalves (Pliocardiinae) in the Southern Ocean. Polar Biology, Online First. DOI: 10.1007/s00300-020-02717-z
Our paper just published in Marine Biology finds shell microstructure to be a useful taxonomic character in deep-sea vent/seep pectinodontid limpets, in which shell form and radula are extremely variable intraspecifically and cannot reliably separate species. This provides a basis for taxonomy and species identification in future studies on this group. Furthermore, the limpets seem to shift their aragonite:calcite ratio in response to the environment. The paper: https://link.springer.com/article/10.1007/s00227-020-03692-z<br />
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Abstract: <br />
Pectinodontid limpets of the genus Bathyacmaea are endemic to hot vents and cold seeps and exhibit greatly variable shell and radular macro-morphologies, rendering reliable species-level identification challenging. Here, we analyzed shell microstructures of western Pacific vent/seep Bathyacmaea limpets using scanning electron microscopy and Raman spectrophotometry to test its usefulness in providing phylogenetic signals. Bathyacmaea shells comprised of two forms of calcitic microstructure including irregular spherulitic prismatic type-A (ISP type-A) and semi-foliated (SF), as well as the aragonitic crossed lamellar (CL) microstructure. Despite marked differences in macroscopic shell morphologies once leading them to be classified into different species or even genera, six morphotypes of Bathyacmaea nipponica from different chemosynthetic localities and substrates shared an outermost ISP-A layer and alternating layers of SF and CL structures in their outer and inner shell layers. A genetically divergent lineage recovered from the South Chamorro Seamount, however, differed in having a simple three-layered shell composition consisting of ISP-A, SF, and CL structures, in that order, from the outside, and an unusually thin inner shell layer consisting of only CL structure. Moreover, the ratio of aragonite and calcite varied with habitat conditions, with calcite dominating in vents and aragonite dominating in seeps. These results suggest that the shell microstructure of pectinodontids is under phylogenetic constraints and provides useful taxonomic signals, while the mineral polymorphism in aragonite/calcite ratio varies according to environmental factors. Furthermore, microstructures of two ‘species’ from Cretaceous seeps confirmed the same patterns in fossil lineages. <br />
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Sato K*, Watanabe HK, Jenkins RG, Chen C (2020). Phylogenetic constraint and phenotypic plasticity in the shell microstructure of vent and seep pectinodontid limpets. Marine Biology, 167: 79. DOI: 10.1007/s00227-020-03692-z
Paper just published in Antarctic Science describes Cocculina enigmadonta Chen & Linse, 2020 from deep-sea hot vent and whale fall in the Southern Ocean! This is the first vent-inhabiting species from not just family Cocculinidae but also the entire order Cocculinida, which normally occurs on wood falls. Paper: https://doi.org/10.1017/S095410202000022X<br />
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Abstract: <br />
Lush ‘oases’ of life seen in chemosynthetic ecosystems such as hot vents and cold seeps represent rare, localised exceptions to the generally oligotrophic deep ocean floor. Organic falls, best known from sunken wood and whale carcasses, are additional sources of such oases. The Kemp Caldera (59°42’S 28°20’W) in the Weddell Sea exhibits active hydrothermal vents and a natural whale fall in close proximity, where an undescribed cocculinid limpet was found living in both types of chemosynthetic habitats. This represents the first member of the gastropod order Cocculinida discovered from hot vents, and also the first record from the Southern Ocean. Here, we applied an integrative taxonomy framework incorporating traditional dissection, electron microscopy, genetic sequencing, and 3D anatomical reconstruction through synchrotron CT in order to characterise this species. Together, our data revealed an unusual member of the genus Cocculina with a highly modified radula for feeding on bacterial film, described herein as Cocculina enigmadonta n. sp. Its phylogenetically derived position within the largely wood-inhabiting Cocculina indicates that it likely evolved from an ancestor adapted to living on sunken wood, providing a compelling case of the ‘stepping stone’ evolutionary trajectory from organic falls to seeps and vents. <br />
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Chen C*, Linse K (2020). From wood to vent: first cocculinid limpet associated with hydrothermal activity discovered in the Weddell Sea. Antarctic Science, First View. DOI: 10.1017/S095410202000022X
A co-authored paper led by Masanori Okanishi is now published in Raffles Bulletin of Zoology! We described two new species of ophiuroids (brittle stars) in the genus Ophiambix from deep-sea chemosynthesis-based ecosystems around Japan (hot vents, cold seeps, wood falls), and provided two new records of known species. The paper is OPEN ACCESS: https://lkcnhm.nus.edu.sg/app/uploads/2020/01/RBZ-2020-0017.pdf<br />
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Abstract: <br />
Two new species and two new occurrence records of the genus Ophiambix Lyman, 1880 (Echinodermata: Ophiuroidea), were found on hydrothermal vents at the Pacific coast of Japan. Ophiambix kagutsuchi, new species, is distinguished from other congeners in having small granules separated from each other on aboral surface of disc, flat teeth, second from oral-most arm spines being cylindrical and spiniform in shape, and one small and spiniform tentacle scale on each tentacle pore. Ophiambix macrodonta, new species, is distinguished from the other congeners in having small granules circularly arranged surrounding the periphery of disc scales on aboral surface of disc, flat teeth, second from oral-most arm spines being flat and leaf-like in shape, and one small and spiniform tentacle scale on each tentacle pore. Furthermore, Ophiambix epicopus Paterson & Baker, 1988, was recorded from Japan for the first time and another congener, Ophiambix aculeatus Lyman, 1880, was also collected. Ophiambix kagutsuchi, new species, and Ophiambix macrodonta, new species, were collected from deep-sea chemosynthetic environments. A tabular key to all six species of the genus Ophiambix is provided.<br />
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Okanishi M*, Kato M, Watanabe HK, Chen C, Fujita T (2020). Large populations of two new species of Ophiambix (Echinodermata, Ophiuroidea) discovered on Japanese hot vents and cold seeps. Raffles Bulletin of Zoology, 68: 196-213. DOI: 10.26107/RBZ-2020-0017
Thrilled to reveal the Scaly-foot Snail's whole genome in a paper I co-first authored with Jin Sun and Norio Miyamoto, published today in Nature Communications! The genome assembly is one of the best molluscan (and even lophotrochozoan) genomes available to date, being resolved at a chromosomal-level. By comparing available genome and tissue-specific transcriptome data from other animals, we identified an ancient ‘biomineralisation toolkit’ key to repeated evolution of hard parts in molluscs and other lophotrochozoan animals. OPEN ACCESS: https://www.nature.com/articles/s41467-020-15522-3<br />
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Abstract: <br />
The Scaly-foot Snail, Chrysomallon squamiferum, presents a combination of biomineralised features, reminiscent of enigmatic early fossil taxa with complex shells and sclerites such as sachtids, but in a recently-diverged living species which even has iron-infused hard parts. Thus the Scaly-foot Snail is an ideal model to study the genomic mechanisms underlying the evolutionary diversification of biomineralised armour. Here, we present a high-quality whole-genome assembly and tissue-specific transcriptomic data, and show that scale and shell formation in the Scaly-foot Snail employ independent subsets of 25 highly-expressed transcription factors. Comparisons with other lophotrochozoan genomes imply that this biomineralisation toolkit is ancient, though expression patterns differ across major lineages. We suggest that the ability of lophotrochozoan lineages to generate a wide range of hard parts, exemplified by the remarkable morphological disparity in Mollusca, draws on a capacity for dynamic modification of the expression and positioning of toolkit elements across the genome.<br />
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Sun J# / Chen C# / Miyamoto N#, Li R, Sigwart JD, Xu T, Sun Y, Wong WC, Ip JCH, Zhang W, Lan Y, Bissessur D, Watsuji T-o, Watanabe HK, Takaki Y, Ikeo K, Fujii N, Yoshitake K, Qiu J-W, Takai K*, Qian P-Y* (2020). The Scaly-foot Snail genome and implications for the origins of biomineralised armour. Nature Communications, 11: 1657. DOI: 10.1038/s41467-020-15522-3
Co-authored paper led by Jin Sun showcases the biodiversity of the recently discovered "Tiancheng" deep-sea hot vent field on the Southwest Indian Ridge, Indian Ocean -- including a new population of the now-Endangered Scaly-foot Snail (Chrysomallon squamiferum). Genetically, they were closer to populations on the Central Indian Ridge than another on the same ridge (but further away).  We also report the first chimney structure venting high-temeprature fluids from this particular vent field. OPEN  ACCESS: https://royalsocietypublishing.org/doi/10.1098/rsos.200110<br />
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Abstract: <br />
Biodiversity of hydrothermal vents in the Indian Ocean, particularly those on the Southwest Indian Ridge (SWIR), are still relatively poorly understood. The Tiancheng field on the SWIR was initially reported with only a low-temperature diffuse flow venting area, but here we report two new active areas, including a chimney emitting high-temperature vent fluids. Biological sampling in these new sites doubled the known megafauna and macrofauna richness reported from Tiancheng. Significantly, we found several iconic species, such as the scaly-foot snail and the first Alviniconcha population on the SWIR. Tiancheng shares a high proportion of taxa with vents on the Central Indian Ridge (CIR) and lacks a number of key taxa that characterize other vents investigated so far on the SWIR. Population genetics of the scaly-foot snail confirmed this, as the Tiancheng population was clustered with populations from the CIR, showing low connectivity with the Longqi field. Unlike the previously examined populations, scales of the Tiancheng scaly-foot snail were coated in zinc sulfide, although this results only from precipitation. The close connection between Tiancheng and CIR vents indicates that the dispersal barrier for vent endemic species is not the Rodriguez Triple Junction as previously suggested but the transformation faults between Tiancheng and Longqi, warranting further studies on deep currents in this area to resolve the key barrier, which has important implications for biological conservation.<br />
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Sun J# / Zhou Y#, Chen C, Kwan YH, Sun Y, Wang X, Yang L, Zhang R, Wei T, Yang Y, Qu L, Sun C*, Qian P-Y* (2020). Nearest vent, dearest friend: Biodiversity of Tiancheng vent field reveals cross-ridge similarities in the Indian Ocean. Royal Society Open Science, 7: 200110. DOI: 10.1098/rsos.200110
A co-authored paper with Jin Sun and others has been published in PLoS One. In this study, comparative transcriptomics was used to investigate the differences in molecular adaptation between two deep-sea vent endemic alvinocaridid shrimps -- one living right next to hot vent orifice and one living in the cooler peripheral areas. <br />
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Abstract: <br />
Diffusing fluid at a deep-sea hydrothermal vent creates rapid, acute physico-chemical gradients that correlate strongly with the distribution of the vent fauna. Two alvinocaridid shrimps, Alvinocaris longirostris and Shinkaicaris leurokolos occupy distinct microhabitats around these vents and exhibit different thermal preferences. S. leurokolos inhabits the central area closer to the active chimney, while A. longirostris inhabits the peripheral area. In this study, we screened candidate genes that might be involved in niche separation and microhabitat adaptation through comparative transcriptomics. The results showed that among the top 20% of overexpressed genes, gene families related to protein synthesis and structural components were much more abundant in S. leurokolos compared to A. longirostris. Moreover, 15 out of 25 genes involved in cellular carbohydrate metabolism were related to trehalose biosynthesis, versus 1 out of 5 in A. longirostris. Trehalose, a non-reducing disaccharide, is a multifunctional molecule and has been proven to act as a protectant responsible for thermotolerance in Saccharomyces cerevisiae. Putative positively selected genes involved in chitin metabolism and the immune system (lectin, serine protease and antimicrobial peptide) were enriched in S. leurokolos. In particular, one collagen and two serine proteases were found to have experienced strong positive selection. In addition, sulfotransferase-related genes were both overexpressed and positively selected in S. leurokolos. Finally, genes related to structural proteins, immune proteins and protectants were overexpressed or positively selected. These characteristics could represent adaptations of S. leurokolos to its microhabitat, which need to be confirmed by more evidence, such as data from large samples and different development stages of these alvinocaridid shrimps. <br />
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Zhu F-C, Sun J, Yan G-Y, Huang J-M, Chen C, He L-S* (2020). Insights into the strategy of micro-environmental adaptation: Transcriptomic analysis of two alvinocaridid shrimps at a hydrothermal vent. PLoS ONE 15(1): e0227587. DOI: 10.1371/journal.pone.0227587
And the final (I think) paper of 2019 is a co-authored review (with Takuya Yahagi and Shinsuke Kawagucci) of the larval dispersal process at deep-sea chemosynthetic ecosystems, published in the journal "Oceanography in Japan". It is in Japanese with English abstract and is available via OPEN ACCESS here: http://kaiyo-gakkai.jp/jos/uminokenkyu/vol28/28-4_5_6/28-4_5_6-03-Yahagi.pdf<br />
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Abstract: <br />
The discovery of unfathomably high animal biomass inhabiting deep seafloors with geofluid input, such as hydrothermal vents, is widely recognized as one of the most extraordinary scientific achievements in recent history. Four decades since its discovery, how animals migrate between these stepping stone-like habitats remains a fascinating research topic. The concept of larval dispersal where animals migrate during their early life stages (as eggs or larvae), is generally accepted as the only viable process for this to occur. Here, we review existing studies concerning this process in three stages (emigration, migration, and colonization) and consider two different viewpoints (biological factors and seawater dynamics). Furthermore, we disentangle the obstacles and limitations related to the study of animal dispersal in hydrothermal vents, discuss new developments in the field, and provide an outlook on research in the coming decades. <br />
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Yahagi T*, Chen C, Kawagucci S* (2019). What we know, what we can know, and what we will never know about the larval dispersal process at deep-sea chemosynthetic ecosystems. Oceanography in Japan, 28: 97-125. DOI: 10.5928/kaiyou.28.4-5-6_97 [In Japanese with English abstract]
Co-authored article published in the journal Deep-Sea Research Part I presents the biogeography, systematics, and taxonomy of Amphisamytha polychaete worms from Indian Ocean hot vents. 50 days OPEN  access: https://authors.elsevier.com/c/1a8WW3RueHTjSa<br />
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This also includes the description of three new species: Amphisamytha marisindica Zhou et al., 2019, A. collaris Zhou et al., 2019, and A. wocanensis Zhou et al., 2019. <br />
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Abstract: <br />
Deep-sea polychaetes in the genus Amphisamytha are well known from numerous hydrothermal vents and hydrocarbon seeps in the Pacific and Atlantic oceans. Records from the Indian Ocean, however, have not been characterized morphologically or genetically. Here, we examined specimens taken from deep-sea vents on three mid-ocean ridges in the Indian Ocean, including Southwest Indian Ridge (SWIR), Central Indian Ridge (CIR), and Carlsberg Ridge (CR), and re-assessed phylogenetic relationships within the genus including the Indian Ocean records. Multi-gene phylogenetic analyses using a concatenated alignment of 16S rRNA, 18S rRNA, 28S rRNA, and COI genes recovered four distinct, hitherto unreported, lineages in the Indian Ocean interpreted to represent four undescribed species. One of these, formally described as Amphisamytha marisindica n. sp. herein, is characterized by relatively large body size, conspicuous nuchal organs, smooth abdominal glandular pads, and 17–19 abdominal chaetigers. It was found to span all three ridges, representing one of the most widespread species in the genus. Two further sympatric species, Amphisamytha collaris n. sp. and Amphisamytha sp. Longqi, appeared to prefer relict/inactive chimneys in the Longqi field, SWIR. Amphisamytha collaris n. sp. is unique for its V-shaped collar on the posterior lobe of prostomium. Due to the scarcity and condition of the samples available, Amphisamytha sp. Longqi was not formally described. Lastly, Amphisamytha wocanensis n. sp. was only recorded from the Wocan field, CR, and no reliable morphological characteristics could separate it from A. carldarei and A. fauchaldi, indicative of cryptic speciation. Monophyly of the genus Amphisamytha was not supported in the current phylogeny, warranting further revisions at the genus level. The four Indian Ocean species were placed into two well-supported clades: Amphisamytha sp. Longqi and A. collaris n. sp. formed sister-relationship with the Southwest Pacific A. julianeae, while A. marisindica n. sp. and A. wocanensis were recovered as crown taxa in a clade composed of their East Pacific and Atlantic congeners, indicating two separate evolutionary lineages of Amphisamytha meeting in the Indian Ocean. The sister-relationship of species from the Carlsberg Ridge and East Pacific suggests extreme long-distance dispersal of their ancestor, or points towards numerous undescribed or extinct species belonging to this clade. <br />
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Zhou Y, Chen C, Watanabe HK, Zhang R, Wang C* (2019). Amphisamytha (Annelida: Ampharetidae) from Indian Ocean hydrothermal vents: biogeographic implications. Deep-Sea Research Part I: Oceanographic Research Papers, 154: 103148. DOI: 10.1016/j.dsr.2019.103148
Co-authored paper led by Katrin Linse now published in Royal Society Open Science! This paper presents a new Antarctic hydrothermal vent field in the Kemp Caldera, South Sandwich Arc and its biology. Open access: https://royalsocietypublishing.org/doi/10.1098/rsos.191501<br />
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Abstract:<br />
Faunal assemblages at hydrothermal vents associated with island-arc volcanism are less well known than those at vents on mid-ocean ridges and back-arc spreading centres. This study characterizes chemosynthetic biotopes at active hydrothermal vents discovered at the Kemp Caldera in the South Sandwich Arc. The caldera hosts sulfur and anhydrite vent chimneys in 1375–1487 m depth, which emit sulfide-rich fluids with temperatures up to 212°C, and the microbial community of water samples in the buoyant plume rising from the vents was dominated by sulfur-oxidizing Gammaproteobacteria. A total of 12 macro- and megafaunal taxa depending on hydrothermal activity were collected in these biotopes, of which seven species were known from the East Scotia Ridge (ESR) vents and three species from vents outside the Southern Ocean. Faunal assemblages were dominated by large vesicomyid clams, actinostolid anemones, Sericosura sea spiders and lepetodrilid and cocculinid limpets, but several taxa abundant at nearby ESR hydrothermal vents were rare such as the stalked barnacle Neolepas scotiaensis. Multivariate analysis of fauna at Kemp Caldera and vents in neighbouring areas indicated that the Kemp Caldera is most similar to vent fields in the previously established Southern Ocean vent biogeographic province, showing that the species composition at island-arc hydrothermal vents can be distinct from nearby seafloor-spreading systems. δ13C and δ15N isotope values of megafaunal species analysed from the Kemp Caldera were similar to those of the same or related species at other vent fields, but none of the fauna sampled at Kemp Caldera had δ13C values, indicating nutritional dependence on Epsilonproteobacteria, unlike fauna at other island-arc hydrothermal vents.<br />
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Linse K*, Copley JT, Connelly DP, Larter RD, Pearce DA, Polunin NVC, Chen C, Clarke A, Glover A, Graham AGC, Huvenne VAI, Marsh L, Reid WDK, Roterman CN, Sweeting CJ, Zwirglmaier K, Tyler PA (2019). Fauna of the Kemp Caldera and its upper bathyal hydrothermal vents (South Sandwich Arc, Antarctica). Royal Society Open Science, 6(11): 191501. DOI: 10.1098/rsos.191501
Co-first authored article published in Trends in Ecology and Evolution! We highlight environmental sound (soundscape) as a key conservation tool to assess deep-sea mining impacts to benthic ecosystems, and urge for global effort in implementing it widely. The resilience of these ecosystems, such as hydrothermal vents, rely on larval dispersal which may be directed by habitat-specific sound. Link: https://www.cell.com/trends/ecology-evolution/fulltext/S0169-5347(19)30284-8<br />
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Abstract: <br />
Targets of deep-sea mining commonly coincide with biodiversity hotspots, such as hydrothermal vents. The resilience of these ecosystems relies on larval dispersal, which may be directed by habitat-specific soundscapes. We urge for a global effort to implement soundscape as a conservation tool to assess anthropogenic disruption to deep-sea benthic ecosystems. <br />
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Lin T-H#* / Chen C#, Watanabe HK, Kawagucci S, Yamamoto H, Akamatsu T (2019). Using soundscape to assess deep-sea benthic ecosystems. Trends in Ecology & Evolution, 34(12): 1069-1071. DOI: 10.1016/j.tree.2019.09.006
Published in Frontiers in Marine Science, a co-authored paper with Yi Lan, Jin Sun, Ting Xu, among others used transcriptome analyses to look into the host-symbiont interactions among two deep-sea vesicomyid clams and their endosymbiotic sulfur-oxidising bacteria. OPEN ACCESS: https://www.frontiersin.org/articles/10.3389/fmars.2019.00680/full<br />
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Abstract: <br />
In deep-sea hydrothermal vents and hydrocarbon seeps, chemoautotrophic bacteria use chemical substances as energy resources for primary production, ultimately supporting dense communities of megafauna, including charismatic giant vesicomyid clams. These clams inherit their endosymbionts from their parents and house them intracellularly in their gills. How these organisms maintain their unique symbiotic relationship at the cellular level, however, remains largely unclear. In the present study, transcriptomes of different organs in Phreagena okutanii collected from a hydrothermal vent and in Archivesica marissinica collected from a methane seep were sequenced in order to decipher their host–symbiont relationships. Expressional analyses of the transcriptomes showed that the tricarboxylic acid (TCA) cycle-related genes, the Rab gene family, and the lysozyme genes were highly expressed in the gills. Furthermore, genes related to vesicle trafficking, lysosomes, and mitochondrial and energy metabolism were positively selected. The endosymbiont genes involved in sulfur oxidation, oxidative phosphorylation, and adenosine triphosphate (ATP) synthesis were highly expressed. The results suggest that the vesicomyid clams provide intermediates to fulfill the metabolic needs of their endosymbionts, and in return the endosymbionts actively generate nutrients for the hosts through being digested by the lysozymes of the host. Furthermore, the positive selection of genes related to vesicle trafficking, lysosomes, and mitochondrial and energy metabolism indicates molecular adaptations of the host in order to benefit from symbiosis. Overall, the present study provides the first set of transcriptomes for deep-sea chemosymbiotic vesicomyid clams, facilitating a better understanding of the host–symbiont relationship that has allowed them to become dominant animals in deep-sea hydrothermal vents and cold seeps.<br />
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Lan Y, Sun J, Zhang W, Xu T, Zhang Y, Chen C, Feng D, Wang H, Tao J, Qiu J-W, Qian P-Y* (2019). Host-symbiont interactions in deep-sea chemosymbiotic vesicomyid clams: insights from transcriptome sequencing. Frontiers in Marine Science, 6: 680. DOI: 10.3389/fmars.2019.00680
A co-authored paper published in Applied and Environmental Microbiology presents evidences pointing to a symbiotic relationship between Haplosclerida sponges from deep-sea hydrothermal vents in the Okinawa Trough and a sulfur-oxidising bacteria dominant in its microbiome. Furthermore, metagenomic results indicate that the metabolism of the symbiotic bacteria may be supported by viruses in the same environment. <br />
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Abstract: <br />
In deep-sea hydrothermal vent environments, sulfur-oxidizing bacteria belonging to the clade SUP05 are crucial symbionts of invertebrate animals. Marine viruses, as the most abundant biological entities in the ocean, play essential roles in regulating the sulfur metabolism of the SUP05 bacteria. To date, vent sponge-associated SUP05 and their phages have not been well documented. The current study analyzed microbiomes of Haplosclerida sponges from hydrothermal vents in the Okinawa Trough and recovered the dominant SUP05 genome, designated VS-SUP05. Phylogenetic analysis showed that VS-SUP05 was closely related to endosymbiotic SUP05 strains from mussels living in deep-sea hydrothermal vent fields. Homology and metabolic pathway comparisons against free-living and symbiotic SUP05 strains revealed that the VS-SUP05 genome shared many features with the deep-sea mussel symbionts. Supporting a potentially symbiotic lifestyle, the VS-SUP05 genome contained genes involved in the synthesis of essential amino acids and cofactors that are desired by the host. Analysis of sponge-associated viral sequences revealed putative VS-SUP05 phages, all of which were double-stranded viruses belonging to the families Myoviridae, Siphoviridae, Podoviridae, and Microviridae. Among the phage sequences, one contig contained metabolic genes (iscR, iscS, and iscU) involved in iron-sulfur cluster formation. Interestingly, genome sequence comparison revealed horizontal transfer of the iscS gene among phages, VS-SUP05, and other symbiotic SUP05 strains, indicating an interaction between marine phages and SUP05 symbionts. Overall, our findings confirm the presence of SUP05 bacteria and their phages in sponges from deep-sea vents and imply a beneficial interaction that allows adaptation of the host sponge to the hydrothermal vent environment. <br />
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Zhou K, Zhang R, Sun J, Zhang W, Tian R, Chen C, Kawagucci S, Xu Y* (2019). Potential interactions between clade SUP05 sulfur-oxidizing bacteria and phages in hydrothermal vent sponges. Applied and Environmental Microbiology, 85(22): e00992-19. DOI: 10.1128/AEM.00992-19
New lead-authored paper in Biology Letters reveals how deep-sea pectinodontid limpets 'shapeshifts' when growing on different substrates, shown by a three-months long live translocation experiment. These results, combined with morphology+genetic data from nearly 100 limpets, reveal many ‘species’ in two 'genera' to be just ONE variable species. Serradonta is just curvy Bathyacmaea! This also impacts interpretations of the ecology of some extinct species. Read here: https://royalsocietypublishing.org/doi/10.1098/rsbl.2019.0504<br />
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With Hiromi Watanabe-Kayama, Takashi Toyofuku, Ting Xu, Jin Sun, among others. <br />
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Abstract: <br />
Pectinodontid limpets are important members of deep-sea hot vents and cold seeps as can be seen by their conspicuous presence in both extant and extinct systems. They have traditionally been classified into different genera and species based on shell and radula characteristics; the reliability of these characters has been questioned but not tested thoroughly. Here, for the first time in taxa endemic to deep-sea chemosynthetic ecosystems, we combine substrate translocation with molecular data to assess the plasticity and variability of key phenotypic characters. Molecular data revealed that several ‘species’ of extant vent/seep pectinodontids actually represent intergrading morphotypes of a single, highly plastic, evolutionary lineage, with each morphological trait being possibly influenced differently by environmental and genetic factors. Our results challenge previous interpretations of paleoecology at fossil chemosynthetic ecosystems and highlight the importance of modern analogues in understanding fossil systems.<br />
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Chen C*, Watanabe HK, Nagai Y, Toyofuku T, Xu T, Sun J, Qiu J-W, Sasaki T (2019). Complex factors shape phenotypic variation in deep-sea limpets. Biology Letters, 15(10): 20190504. DOI: 10.1098/rsbl. 2019.0504
Just published in the Journal of Molluscan Studies of The Malacological Society of London, our new paper describes two new deep-sea abyssochrysoidean snails endemic to hot vents and gives insights on their ecology. Provanna beebei is from vents in the Caribbean Sea nearly 5000 m deep, and Provanna cooki is from the Southern Ocean including Antarctic waters at over 2000 m deep. Read here: http://bit.ly/Provanna<br />
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Abstract: <br />
The recent discovery and exploration of deep-sea hydrothermal vent fields in the Mid-Cayman Spreading Centre, Caribbean Sea (Beebe Vent Field, 4956–4972 m depth) and the East Scotia Ridge, Southern Ocean (E2 and E9 vent fields, 2394–2641 m depth) have yielded extensive collections of two new provannid species, Provanna beebei n. sp. and P. cooki n. sp. Morphological and molecular taxonomy (530 bp of the mitochondrial cytochrome c oxidase subunit I gene) confirm P. beebei n. sp. and P. cooki n. sp. as distinct species; these species are formally described, and details are provided of their distribution, habitat and species associations. Bayesian and maximum likelihood analyses support the placement of P. beebei n. sp. and P. cooki n. sp within the genus Provanna and show that these two new deep-sea species form a well-supported clade with the abyssal West Pacific P. cingulata. Provanna beebei n. sp. and P. cooki n. sp. represent the first records of Provanna from hydrothermal vents in the Caribbean Sea and Southern Ocean, respectively, and extend the known geographic range of the genus. For the first time, intraspecific phenotypic variation in size and sculpture has been reported for Provanna. At the East Scotia Ridge, shell-size frequency distributions and median shell size of P. cooki n. sp. varied significantly between the E2 and E9 vent fields, as well as between diffuse flow and high-temperature venting habitats within each field. The variation in shell sculpture in relation to habitat was also observed in P. cooki n. sp. <br />
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Linse K / Nye V, Copley JT, Chen C (2019). On the systematics and ecology of two new species of Provanna (Gastropoda: Provannidae) from deep-sea hydrothermal vents in the Caribbean Sea and Southern Ocean.  Journal of Molluscan Studies, eyz024, https://doi.org/10.1093/mollus/eyz024
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