DOCSLIB.ORG

The Ubiquitous Mussel: Bathymodiolus Aff. Brevior Symbiosis at the Central Indian Ridge Hydrothermal Vents

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
The Ubiquitous Mussel: Bathymodiolus Aff. Brevior Symbiosis at the Central Indian Ridge Hydrothermal Vents MARINE ECOLOGY PROGRESS SERIES Vol. 295: 183–190, 2005 Published June 23 Mar Ecol Prog Ser The ubiquitous mussel: Bathymodiolus aff. brevior symbiosis at the Central Indian Ridge hydrothermal vents Z. P. McKiness1, 2, C. M. Cavanaugh1,* 1Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA 2Present address: National Animal Disease Center, United States Department of Agriculture, Agricultural Research Service, 2300 Dayton Avenue, Ames, Iowa 50010, USA ABSTRACT: The discovery and exploration of hydrothermal vents on the Central Indian Ridge (CIR) yielded invaluable samples for further resolution of the biogeography of chemoautotrophic sym- bioses. Mytilid mussels were collected from 2 CIR hydrothermal vent fields and preliminary molecu- lar analyses suggested phylogenetic affinity with the western Pacific vent mussel Bathymodiolus brevior. Resolving whether this mussel, designated B. aff. brevior, hosts a dual symbiosis, as charac- terized for the 2 Mid-Atlantic Ridge hydrothermal vent mussel species, or a single chemoautotrophic symbiosis, as seen in the Pacific vent mussel species, will provide insight into the evolutionary history of mytilid symbioses. Ultrastructural, physiological, and molecular evidence are reported herein which support the presence of a single endosymbiont phylotype with chemoautotrophic metabolism. Phylogenetic analyses placed this symbiont in the same clade as the vesicomyid clam symbionts, prompting discussion regarding the evolutionary origin of chemoautotrophic symbioses in vent bivalves. KEY WORDS: Chemoautotrophic endosymbiosis · Central Indian Ridge · Hydrothermal vent · Bathymodiolus spp. Resale or republication not permitted without written consent of the publisher INTRODUCTION son & Fisher 1995). The bacterial symbionts harness energy from reduced inorganic sulfur compounds to Research at deep-sea hydrothermal vents (discov- drive carbon fixation and, ultimately, either directly or ered only 25 yr ago) has resulted in a radically altered indirectly provide their host with organic carbon. The perception of life in the aphotic zone of the world’s host organism is able to use a combination of traits to oceans. Unrivaled biomass, coupled with extreme geo- sequester and transport necessary substrates to the logical and chemical stochasticity, has redefined ideas aerobic chemoautotrophic bacteria. regarding not only deep-sea biology, but the nature As hydrothermal vent exploration has progressed, and function of ecosystems. Completely removed from and additional locales have been identified and sam- sunlight, primary productivity at hydrothermal vents is pled, many key evolutionary questions regarding the driven by chemical energy. Life in these novel habitats widespread nature of chemoautotrophic symbioses is characterized by an astounding array of physiologi- have arisen. In particular, biogeographic ‘provinces’ cal, morphological and behavioral adaptations. The are under continuous evaluation as more sites are hallmark of hydrothermal vent biology is the recurring explored (e.g. Tunnicliffe et al. 1998). The recent dis- theme of chemoautotrophic bacterial symbioses, which coveries of the Kairei and Edmond hydrothermal vent have been described for the majority of the dominant fields on the Central Indian Ridge (CIR) were of pro- vent macrofauna (Fisher 1990, Cavanaugh 1994, Nel- found importance in the context of further resolving *Corresponding author. Email: [email protected] © Inter-Research 2005 · www.int-res.com 184 Mar Ecol Prog Ser 295: 183–190, 2005 biogeographic patterns in the world’s hydrothermal species from B. brevior, this mussel will be referred to as vent ecosystems (Hashimoto et al. 2001, Van Dover et B. aff. brevior herein, since the molecular results indicate al. 2002). The biology of CIR vents was a great mystery, high genetic identity with B. brevior. given the disparate communities inhabiting the At- While the CIR vents lack the well-studied vesicomyid lantic and Pacific vents. Forming a key physical link clam and vestimentiferan tubeworm symbioses, the between the Mid-Atlantic Ridge (MAR) hydrothermal presence of mytilid mussels at this locale is significant vents and the western Pacific back arc basins, the CIR given their ubiquity in the Atlantic and Pacific Oceans. hydrothermal vents were found to be characterized by Among symbiont-hosting vent fauna, only mussels a blend of Atlantic and Pacific faunas (Van Dover et al. have been described from all known hydrothermal vent 2001). Massive swarms of shrimp dominated the vent biogeographic provinces (Table 1): Juan de Fuca (un- fields, visually reminiscent of MAR vents. However, named new species), East Pacific Rise, EPR, (Bathy- much like western Pacific vent sites, sea anemones, modiolus thermophilus), MAR (B. azoricus and B. interspersed with clumps of mussels and snails, domi- puteoserpentis), western Pacific (B. brevior and B. elon- nated the benthic environment. gatus), and Okinawa Trough (B. japonicus, B. pla- The CIR mussels, designated Bathymodiolus aff. bre- tifrons, and B. septemdierum). Thus, finding mytilid vior, are more closely related to the western Pacific mus- mussels at the CIR vents, although not unexpected, fur- sel B. brevior than to the MAR mussels B. azoricus and B. ther establishes their global distribution. In addition to puteoserpentis, as revealed by molecular studies based their ubiquity, Bathymodiolus spp. mussels are unique on NADH dehydrogenase subunit 4 (ND4) (Van Dover et in the range of symbiont composition observed in the al. 2001, Won et al. 2002). Yamanaka et al. (2003) re- gills of different species (Table 1). To date, mussels are ported transmission electron microscope (TEM) and sul- known from hydrothermal vents and cold seeps that fur-isotope data that indicate the presence of bacterial host either sulfur-oxidizing chemoautotrophic sym- symbionts in this species. This mussel has also been de- bionts (Cavanaugh 1983, Nelson et al. 1995, Dubilier et scribed as B. marisindicus based on morphological data al. 1998) or methane-oxidizing (methanotrophic) sym- (Hashimoto 2001); however, because morphological bionts (Childress et al. 1986). Furthermore, mussels that characters may reflect phenotypic plasticity, a new spe- host ‘dual symbioses’ involving both types of bacteria cies designation may not be warranted. Pending addi- are known from the Gulf of Mexico cold seeps (Ca- tional data indicating that the CIR mussel is a separate vanaugh et al. 1987, Cavanaugh 1993, Fisher et al. Table 1. Bathymodiolus spp. Symbiont composition and geographic distribution of mussels from deep-sea hydrothermal vents. Presence of symbiont type demonstrated by ultrastructural, physiological/immunological, isotopic, and/or molecular evidence. C: chemoautotrophic symbionts; M: methanotrophic symbionts; ?: symbiont type has not been investigated Species Symbiont Location Depth Source type (m) Indian Ocean Bathymodiolus aff. brevior C Central Indian Ridge 2450–3300 This study Pacific Ocean B. brevior C North Fiji Basin 2200 Von Cosel & Metivier (1994), Lau Basin 1850 Dubilier et al. (1998) B. elongatus ? North Fiji Basin 2200 Von Cosel & Metivier (1994) B. japonicus ?, M Okinawa Trough 1200 Hashimoto & Okutani (1994), Fujiwara et al. (2000) B. platifrons M Okinawa Trough 1200 Hashimoto & Okutani (1994), Fujiwara et al. (2000), Barry et al. (2002) B. septemdierum C, ? Okinawa Trough 1200 Hashimoto & Okutani (1994), Fujiwara et al. (2000) B. thermophilus C East Pacific Rise 2000–2600 Cavanaugh (1983), Kenk & Wilson (1985), Galapagos Rift 2500 Nelson et al. (1995) Bathymodiolus n. sp.a C Juan de Fuca 2500 McKiness et al. (2005) Atlantic Ocean B. azoricus C, M Mid Atlantic Ridge 800–2300 Trask & Van Dover (1999), Von Cosel et al. (1999), Fiala-Médioni et al. (2002) B. puteoserpentis C, M Mid Atlantic Ridge 2200–3600 Cavanaugh et al. (1992), Distel et al. (1995), Robinson et al. (1998) aSingle specimen was collected from Juan de Fuca in August 1999; host taxonomy is unresolved McKiness & Cavanaugh: Chemoautotrophic symbiosis in Bathymodiolus 185 1993) and the MAR hydrothermal vents (Cavanaugh et methylotrophy (methanol dehydrogenase). RubisCO ac- al. 1987,1992, Cavanaugh 1993, Fisher et al. 1993, Dis- tivity was assayed using the 14C incorporation method as tel et al. 1995, Robinson et al. 1998, Fiala-Médioni et al. described in Robinson et al. (1998), with fresh spinach 2002). Remarkably, the dual symbioses in these mytilids used as the positive control. Methanol dehydrogenase represent the only known example of the stable coexis- activity was tested using the spectrophotometric tence of 2 physiologically and phylogenetically distinct method of Anthony & Zatman (1964). Gill tissue of the bacteria within the same eukaryotic host cell. Thus, the MAR mussel B. azoricus, which is known to host discovery of a new species of mussel provides potential methanotrophic symbionts (Fiala-Médioni et al. 2002), evolutionary clues to the evolution of the neighboring was used as the positive control. For both assays, boiled MAR dual symbiosis species. cell free extracts and samples lacking substrate, ribu- Here, the presence and nature of symbionts in the lose 1,5-bisphosphate and methanol, respectively, CIR mussel, Bathymodiolus aff. brevior, are evaluated were used as negative controls. using ultrastructural, enzymatic and molecular meth- PCR, cloning, and sequencing of 16S rRNA. DNA ods. The phylogenetic affinities of the putative sym- was extracted
Load more

Recommended publications
  • Adaptation to Deep-Sea Chemosynthetic Environments As Revealed by Mussel Genomes
    ARTICLES PUBLISHED: 3 APRIL 2017 | VOLUME: 1 | ARTICLE NUMBER: 0121 Adaptation to deep-sea chemosynthetic environments as revealed by mussel genomes Jin Sun1, 2, Yu Zhang3, Ting Xu2, Yang Zhang4, Huawei Mu2, Yanjie Zhang2, Yi Lan1, Christopher J. Fields5, Jerome Ho Lam Hui6, Weipeng Zhang1, Runsheng Li2, Wenyan Nong6, Fiona Ka Man Cheung6, Jian-Wen Qiu2* and Pei-Yuan Qian1, 7* Hydrothermal vents and methane seeps are extreme deep-sea ecosystems that support dense populations of specialized macro benthos such as mussels. But the lack of genome information hinders the understanding of the adaptation of these ani- mals to such inhospitable environments. Here we report the genomes of a deep-sea vent/seep mussel (Bathymodiolus plati- frons) and a shallow-water mussel (Modiolus philippinarum). Phylogenetic analysis shows that these mussel species diverged approximately 110.4 million years ago. Many gene families, especially those for stabilizing protein structures and removing toxic substances from cells, are highly expanded in B. platifrons, indicating adaptation to extreme environmental conditions. The innate immune system of B. platifrons is considerably more complex than that of other lophotrochozoan species, including M. philippinarum, with substantial expansion and high expression levels of gene families that are related to immune recognition, endocytosis and caspase-mediated apoptosis in the gill, revealing presumed genetic adaptation of the deep-sea mussel to the presence of its chemoautotrophic endosymbionts. A follow-up metaproteomic analysis of the gill of B. platifrons shows metha- notrophy, assimilatory sulfate reduction and ammonia metabolic pathways in the symbionts, providing energy and nutrients, which allow the host to thrive. Our study of the genomic composition allowing symbiosis in extremophile molluscs gives wider insights into the mechanisms of symbiosis in other organisms such as deep-sea tubeworms and giant clams.
    [Show full text]
  • New Records of Three Deep-Sea Bathymodiolus Mussels (Bivalvia: Mytilida: Mytilidae) from Hydrothermal Vent and Cold Seeps in Taiwan
    352 Journal of Marine Science and Technology, Vol. 27, No. 4, pp. 352-358 (2019) DOI: 10.6119/JMST.201908_27(4).0006 NEW RECORDS OF THREE DEEP-SEA BATHYMODIOLUS MUSSELS (BIVALVIA: MYTILIDA: MYTILIDAE) FROM HYDROTHERMAL VENT AND COLD SEEPS IN TAIWAN Meng-Ying Kuo1, Dun- Ru Kang1, Chih-Hsien Chang2, Chia-Hsien Chao1, Chau-Chang Wang3, Hsin-Hung Chen3, Chih-Chieh Su4, Hsuan-Wien Chen5, Mei-Chin Lai6, Saulwood Lin4, and Li-Lian Liu1 Key words: new record, Bathymodiolus, deep-sea, hydrothermal vent, taiwanesis (von Cosel, 2008) is the only reported species of cold seep, Taiwan. this genus from Taiwan. It was collected from hydrothermal vents near Kueishan Islet off the northeast coast of Taiwan at depths of 200-355 m. ABSTRACT Along with traditional morphological classification, mo- The deep sea mussel genus, Bathymodiolus Kenk & Wilson, lecular techniques are commonly used to study the taxonomy 1985, contains 31 species, worldwide. Of which, one endemic and phylogenetic relationships of deep sea mussels. Recently, species (Bathymodiolus taiwanesis) was reported from Taiwan the complete mitochondrial genomes have been sequenced (MolluscaBase, 2018). Herein, based on the mitochondrial COI from mussels of Bathymodiolus japonicus, B. platifrons and results, we present 3 new records of the Bathymodiolus species B. septemdierum (Ozawa et al., 2017). Even more, the whole from Taiwan, namely Bathymodiolus platifrons, Bathymodiolus genome of B. platifrons was reported with sequence length of securiformis, and Sissano Bathymodiolus sp.1 which were collected 1.64 Gb nucleotides (Sun et al., 2017). from vent or seep environments at depth ranges of 1080-1380 Since 2013, under the Phase II National energy program of m.
    [Show full text]
  • M208p147.Pdf
    MARINE ECOLOGY PROGRESS SERIES Vol. 208: 147–155, 2000 Published December 8 Mar Ecol Prog Ser Phylogenetic characterization of endosymbionts in three hydrothermal vent mussels: influence on host distributions Yoshihiro Fujiwara1,*, Ken Takai2, Katsuyuki Uematsu3, Shinji Tsuchida1, James C. Hunt1, Jun Hashimoto1 1Marine Ecosystems Research Department, Japan Marine Science and Technology Center (JAMSTEC), 2-15 Natsushima, Yokosuka 237-0061, Japan 2Frontier Research Program for Deep-Sea Environment, Japan Marine Science and Technology Center (JAMSTEC), 2-15 Natsushima, Yokosuka 237-0061, Japan 3Marine Work Japan Co., 2-15 Natsushima, Yokosuka 237-0061, Japan ABSTRACT: The bacterial endosymbionts of 3 hydrothermal vent mussels from Japanese waters were characterized by transmission electron microscopic (TEM) observation and phylogenetic analy- ses of 16S ribosomal RNA gene sequences. Endosymbionts of Bathymodiolus septemdierum were related to sulfur-oxidizing bacteria (thioautotrophs), while endosymbionts of B. platifrons and B. japonicus were related to methane-oxidizing bacteria (methanotrophs). This is the first report of deep-sea mussels containing only methanotrophs (lacking thioautotrophs) from hydrothermal vents. Comparison of methane and hydrogen sulfide concentrations in end-member fluids from deep-sea hydrothermal vents indicated that methane concentrations were much higher in habitats containing Bathymodiolus spp. which harbored only methanotrophs than in other habitats of hydrothermal vent mussels. The known distribution of other
    [Show full text]
  • Dispersal and Differentiation of Deep-Sea Mussels of the Genus Bathymodiolus (Mytilidae, Bathymodiolinae)
    Hindawi Publishing Corporation Journal of Marine Biology Volume 2009, Article ID 625672, 15 pages doi:10.1155/2009/625672 Research Article Dispersal and Differentiation of Deep-Sea Mussels of the Genus Bathymodiolus (Mytilidae, Bathymodiolinae) Akiko Kyuno,1 Mifue Shintaku,1 Yuko Fujita,1 Hiroto Matsumoto,1 Motoo Utsumi,2 Hiromi Watanabe,3 Yoshihiro Fujiwara,3 and Jun-Ichi Miyazaki4 1 Institute of Biological Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan 2 Institute of Agricultural and Forest Engineering, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan 3 Research Program for Marine Biology and Ecology, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Natsushima, Yokosuka, Kanagawa 237-0061, Japan 4 Faculty of Education and Human Sciences, University of Yamanashi, Kofu, Yamanashi 400-8510, Japan Correspondence should be addressed to Jun-Ichi Miyazaki, [email protected] Received 22 February 2009; Revised 27 May 2009; Accepted 30 July 2009 Recommended by Horst Felbeck We sequenced the mitochondrial ND4 gene to elucidate the evolutionary processes of Bathymodiolus mussels and mytilid relatives. Mussels of the subfamily Bathymodiolinae from vents and seeps belonged to 3 groups and mytilid relatives from sunken wood and whale carcasses assumed the outgroup positions to bathymodioline mussels. Shallow water mytilid mussels were positioned more distantly relative to the vent/seep mussels, indicating an evolutionary transition from shallow to deep sea via sunken wood and whale carcasses. Bathymodiolus platifrons is distributed in the seeps and vents, which are approximately 1500 km away. There was no significant genetic differentiation between the populations. There existed high gene flow between B. septemdierum and B.
    [Show full text]
  • Genomics and Transcriptomics of the Green Mussel Explain the Durability
    www.nature.com/scientificreports OPEN Genomics and transcriptomics of the green mussel explain the durability of its byssus Koji Inoue1*, Yuki Yoshioka1,2, Hiroyuki Tanaka3, Azusa Kinjo1, Mieko Sassa1,2, Ikuo Ueda4,5, Chuya Shinzato1, Atsushi Toyoda6 & Takehiko Itoh3 Mussels, which occupy important positions in marine ecosystems, attach tightly to underwater substrates using a proteinaceous holdfast known as the byssus, which is tough, durable, and resistant to enzymatic degradation. Although various byssal proteins have been identifed, the mechanisms by which it achieves such durability are unknown. Here we report comprehensive identifcation of genes involved in byssus formation through whole-genome and foot-specifc transcriptomic analyses of the green mussel, Perna viridis. Interestingly, proteins encoded by highly expressed genes include proteinase inhibitors and defense proteins, including lysozyme and lectins, in addition to structural proteins and protein modifcation enzymes that probably catalyze polymerization and insolubilization. This assemblage of structural and protective molecules constitutes a multi-pronged strategy to render the byssus highly resistant to environmental insults. Mussels of the bivalve family Mytilidae occur in a variety of environments from freshwater to deep-sea. Te family incudes ecologically important taxa such as coastal species of the genera Mytilus and Perna, the freshwa- ter mussel, Limnoperna fortuneri, and deep-sea species of the genus Bathymodiolus, which constitute keystone species in their respective ecosystems 1. One of the most important characteristics of mussels is their capacity to attach to underwater substrates using a structure known as the byssus, a proteinous holdfast consisting of threads and adhesive plaques (Fig. 1)2. Using the byssus, mussels ofen form dense clusters called “mussel beds.” Te piled-up structure of mussel beds enables mussels to support large biomass per unit area, and also creates habitat for other species in these communities 3,4.
    [Show full text]
  • Mytilidae: Bathymodiolinae)
    Open Journal of Marine Science, 2013, 3, 31-39 http://dx.doi.org/10.4236/ojms.2013.31003 Published Online January 2013 (http://www.scirp.org/journal/ojms) Dispersal Ability and Environmental Adaptability of Deep-Sea Mussels Bathymodiolus (Mytilidae: Bathymodiolinae) Jun-Ichi Miyazaki1*, Saori Beppu1, Satoshi Kajio1, Aya Dobashi1, Masaru Kawato2, Yoshihiro Fujiwara2, Hisako Hirayama2 1Faculty of Education and Human Sciences, University of Yamanashi, Kofu, Japan 2Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology, Yokosuka, Japan Email: *[email protected] Received October 12, 2012; revised November 17, 2012; accepted November 29, 2012 ABSTRACT Dispersal ability and environmental adaptability are profoundly associated with colonization and habitat segregation of deep-sea animals in chemosynthesis-based communities, because deep-sea seeps and vents are patchily distributed and ephemeral. Since these environments are seemingly highly different, it is likely that vent and seep populations must be genetically differentiated by adapting to their respective environments. In order to elucidate dispersal ability and envi- ronmental adaptability of deep-sea mussels, we determined mitochondrial ND4 sequences of Bathymodiolus platifrons and B. japonicus obtained from seeps in the Sagami Bay and vents in the Okinawa Trough. Among more than 20 spe- cies of deep-sea mussels, only three species in the Japanese waters including the above species can inhabit both vents and seeps. We examined phylogenetic relationships, genetic divergences (Fst), gene flow (Nm), and genetic population structures to compare the seep and vent populations. Our results showed no genetic differentiation and extensive gene flow between the seep and vent populations, indicating high dispersal ability of the two species, which favors coloniza- tion in patchy and ephemeral habitats.
    [Show full text]
  • Gill Symbionts of the Cold-Seep Mussel Bathymodiolus Platifrons
    Fish and Shellfish Immunology 86 (2019) 246–252 Contents lists available at ScienceDirect Fish and Shellfish Immunology journal homepage: www.elsevier.com/locate/fsi Full length article Gill symbionts of the cold-seep mussel Bathymodiolus platifrons: Composition, environmental dependency and immune control T ∗ ∗∗ Jiajia Yua,c, Minxiao Wanga,b, Baozhong Liua,b, Xin Yuea, , Chaolun Lia,b, a CAS Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Center for Ocean Mega-Science, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao, 266071, China b Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, 1 Wenhai Road, Qingdao, 266000, China c University of Chinese Academy of Sciences, Beijing, 100049, China ARTICLE INFO ABSTRACT Keywords: Deep-sea Bathymodiolus mussels depend on the organic carbon supplied by symbionts inside their gills. In this Bathymodiolus platifrons study, optimized methods of quantitative real-time PCR and fluorescence in situ hybridization targeted to both Methanotrophs mRNA and 16S rRNA were used to investigate the gill symbionts of the cold-seep mussel Bathymodiolus platifrons, FISH including species composition, environmental dependency and immune control by the host. Our results showed qRT-PCR that methanotrophs were the major symbiotic bacteria in the gills of B. platifrons, while thiotrophs were scarce. Lysosomal system In the mussels freshly collected from the deep sea, methanotrophs were housed in bacteriocytes in a unique circular pattern, and a lysosome-related gene (VAMP) encoding a vesicle-associated membrane protein was expressed at a high level and presented exactly where the methanotrophs occurred. After the mussels were reared for three months in aquaria without methane supply, the abundance of methanotrophs decreased sig- nificantly and their circle-shaped distribution pattern disappeared; in addition, the expression of VAMP de- creased significantly.
    [Show full text]
  • Sea Mussel Bathymodiolus Platifrons (Bivalvia: Mytilidae) in the Northwest Pacific
    View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Woods Hole Open Access Server Received: 13 September 2017 | Revised: 26 July 2018 | Accepted: 13 August 2018 DOI: 10.1111/eva.12696 ORIGINAL ARTICLE Population genetic structure of the deep- sea mussel Bathymodiolus platifrons (Bivalvia: Mytilidae) in the Northwest Pacific Ting Xu1 | Jin Sun2 | Hiromi K. Watanabe3 | Chong Chen3 | Masako Nakamura4 | Rubao Ji5 | Dong Feng6 | Jia Lv7 | Shi Wang7,8 | Zhenmin Bao7,9 | Pei-Yuan Qian2 | Jian-Wen Qiu1 1Department of Biology, Hong Kong Baptist University, Hong Kong, China Abstract 2Department of Ocean Science, Hong Kong Studying population genetics of deep- sea animals helps us understand their history University of Science and Technology, Hong of habitat colonization and population divergence. Here, we report a population ge- Kong, China netic study of the deep- sea mussel Bathymodiolus platifrons (Bivalvia: Mytilidae) 3Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan widely distributed in chemosynthesis- based ecosystems in the Northwest Pacific. 4School of Marine Science and Technology, Three mitochondrial genes (i.e., atp6, cox1, and nad4) and 6,398 genomewide single Tokai University, Shizuoka, Japan nucleotide polymorphisms (SNPs) were obtained from 110 individuals from four hy- 5Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, drothermal vents and two methane seeps. When using the three mitochondrial Massachusetts genes, nearly no genetic differentiation was detected for B. platifrons in the Nor thwest 6 CAS Key Laboratory of Ocean and Marginal Pacific. Nevertheless, when using SNP datasets, all individuals in the South China Sea Sea Geology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, (SCS) and three individuals in Sagami Bay (SB) together formed one genetic cluster Guangzhou, China that was distinct from the remaining individuals.
    [Show full text]
  • Does the Symbiotic Scale-Worm Feed on the Host Mussel in Deep-Sea Vent fi Elds?
    Res. Org. Geochem. 28, 23-26 (2012) Short Article Does the symbiotic scale-worm feed on the host mussel in deep-sea vent fi elds? Yoshimi Takahashi*,**, Yoko Sasaki**, Yoshito Chikaraishi**, Masashi Tsuchiya**, Hiromi Watanabe**, Takashi Asahida*, Tadashi Maruyama** and Katsunori Fujikura**,a （Received October 15, 2012; Accepted December 14, 2012） Abstract The scale-worm Branchipolynoe pettiboneae is frequently found in the mantle cavity of Bathymodiolus mussels living in hydrothermal vents and seeps around Japan. To investigate its feeding habits and symbiotic relationship with the host mussels, we determined the stable nitrogen isotopic composition of glutamic acid and phenylalanine for representative scale-worms including a symbiotic juvenile and a symbiotic adult, both with their host mussels, and a free-living adult, collected from hydrothermal vents of the Hatoma Knoll (～1532 m in depth) in the Okinawa Trough, Japan. The isotopic data suggested the feeding habits that Bathymodiolus platifrons is a major source of amino acids for symbiotic adult scale-worm but not for free-living adult and symbiotic juvenile scale-worms. Key words: Branchipolynoe pettiboneae, Bathymodiolus platifrons, feeding habits, nitrogen isotopic composition, symbiosis japonicus on hydrothermal vents and seeps in Japanese 1. Introduction waters (e.g., Miura and Hashimoto, 1991). Highly productive chemosynthetic communities are So far, however, few studies of Branchipolynoe associated with deep-sea hydrothermal vents and seeps, scale-worms have examined their biological and which are characterized by symbiotic interactions in- ecological behaviors including feeding habits and cluding primary chemosynthetic bacteria-animal (e.g., symbiotic relationship with the host mussels (e.g., bivalve and tubeworm) and secondary animal-animal Jollivet et al., 2000).
    [Show full text]
  • High Rates of Apoptosis Visualized in The
    High rates of apoptosis visualized in the symbiont-bearing gills of deep-sea Bathymodiolus mussels Bérénice Piquet, Bruce Shillito, François Lallier, Sébastien Duperron, Ann Andersen To cite this version: Bérénice Piquet, Bruce Shillito, François Lallier, Sébastien Duperron, Ann Andersen. High rates of apoptosis visualized in the symbiont-bearing gills of deep-sea Bathymodiolus mussels. PLoS ONE, Public Library of Science, 2019, 14 (2), pp.e0211499. 10.1371/journal.pone.0211499. hal-02042415 HAL Id: hal-02042415 https://hal.sorbonne-universite.fr/hal-02042415 Submitted on 20 Feb 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. RESEARCH ARTICLE High rates of apoptosis visualized in the symbiont-bearing gills of deep-sea Bathymodiolus mussels 1,2 2 1 2,3,4 BeÂreÂnice Piquet , Bruce Shillito , FrancËois H. LallierID , SeÂbastien Duperron *, Ann C. Andersen1* 1 Sorbonne UniversiteÂ, CNRS, Lab. Adaptation et Diversite en Milieu Marin, AD2M, Team: Adaptation et Biologie des InverteÂbreÂs marins en Conditions Extrêmes (UMR 7144), ABICE, Station Biologique de Roscoff, SBR, Roscoff, France, 2 Sorbonne UniversiteÂ, MNHN, CNRS, IRD, UCN, UA, Lab. Biologie des Organismes a1111111111 et Ecosystèmes Aquatiques BOREA (UMR 7208), Team: Adaptation aux Milieux Extrêmes, AMEX, 7 Quai a1111111111 Saint-Bernard, Paris, France, 3 MuseÂum National d'Histoire Naturelle, CNRS, Lab.
    [Show full text]
  • Metagenomic Analyses of a Deep-Sea Mussel Symbiosis Merle Ücker
    Metagenomic analyses of a deep-sea mussel symbiosis Dissertation zur Erlangung des Grades eines Doktors der Naturwissenschaften – Dr. rer. nat. – dem Fachbereich Biologie / Chemie der Universität Bremen vorgelegt von Merle Ücker Bremen März 2021 Die vorliegende Doktorarbeit wurde von Juni 2017 bis März 2021 in der Abteilung Symbiose am Max-Planck-Institut für Marine Mikrobiologie unter der Leitung von Prof. Dr. Nicole Dubilier und direkter Betreuung von Dr. Rebecca Ansorge und Dr. Yui Sato angefertigt. The research presented in this thesis was performed from June 2017 until March 2021 at the Max Planck Institute for Marine Microbiology in the Department of Symbiosis under leadership of Prof. Dr. Nicole Dubilier and direct supervision of Dr. Rebecca Ansorge and Dr. Yui Sato. Gutachter*innen | reviewers Prof. Dr. Nicole Dubilier Prof. Dr. Thorsten Reusch Assist. Prof. Dr. Roxanne Beinart Tag des Promotionskolloquiums | date of doctoral defence 21 April 2021 Diese zur Veröffentlichung erstellte Version der Dissertation enthält Korrekturen. To the ocean. Contents Contents Summary .................................................................................................................................... 1 Zusammenfassung...................................................................................................................... 2 Chapter I | Introduction .............................................................................................................. 4 Aims of this thesis ...............................................................................................................
    [Show full text]
  • A Toll-Like Receptor Identified in Gigantidas Platifrons and Its
    A Toll-like receptor identified in Gigantidas platifrons and its potential role in the immune recognition of endosymbiotic methane oxidation bacteria Mengna Li1,2,*, Hao Chen1,3,4,*, Minxiao Wang1,3,4, Zhaoshan Zhong1,3,4, Hao Wang1,3,4, Li Zhou1,3,4, Huan Zhang1,3,4 and Chaolun Li1,2,3,4 1 Center of Deep Sea Research and Key Laboratory of Marine Ecology & Environmental Sciences (CODR and KLMEES), Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China 2 University of Chinese Academy of Sciences, Beijing, China 3 CAS Key Laboratory of Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China 4 Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, China * These authors contributed equally to this work. ABSTRACT Symbiosis with chemosynthetic bacteria is an important ecological strategy for the deep-sea megafaunas including mollusks, tubeworms and crustacean to obtain nutrients in hydrothermal vents and cold seeps. How the megafaunas recognize symbionts and establish the symbiosis has attracted much attention. Bathymodiolinae mussels are endemic species in both hydrothermal vents and cold seeps while the immune recognition mechanism underlying the symbiosis is not well understood due to the nonculturable symbionts. In previous study, a lipopolysaccharide (LPS) pull-down assay was conducted in Gigantidas platifrons to screen the pattern recognition receptors potentially involved in the recognition of symbiotic methane-oxidizing bacteria (MOB). Consequently, a total of 208 proteins including GpTLR13 were identified. Here the molecular structure, expression pattern and immune function of GpTLR13 were further analyzed. It was found that Submitted 4 January 2021 GpTLR13 could bind intensively with the lipid A structure of LPS through surface 24 March 2021 Accepted plasmon resonance analysis.
    [Show full text]