Identification and characterization of endosymbiosis-related immune genes in deep-sea mussels <italic style="font-style: italic">Gigantidas platifrons</italic>

Mengna LI; Hao CHEN; Minxiao WANG; Zhaoshan ZHONG; Li ZHOU; Chaolun LI

doi:10.1007/s00343-020-0040-7

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Identification and characterization of endosymbiosis-related immune genes in deep-sea mussels Gigantidas platifrons

Biology | Updated：2023-04-27

- Identification and characterization of endosymbiosis-related immune genes in deep-sea mussels Gigantidas platifrons
- Identification and characterization of endosymbiosis-related immune genes in deep-sea mussels Gigantidas platifrons
- 海洋湖沼学报（英文） 2020年38卷第4期页码：1292-1303
- Affiliations：
  
  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 266071, China
  2.Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China
  3.Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China
  4.University of Chinese Academy of Sciences, Beijing 100049, China
- Author bio：
  
  LI Chaolun, lcl@qdio.ac.cn
- Funds：
  
  the Strategic Priority Research Program of the Chinese Academy of Sciences(XDA22050303);the Key Research Program of Frontier Sciences, CAS(ZDBS-LY-DQC032);the National Key Research and Development Program of China(No. 2018YFC0310800);the National Natural Science Foundation of China(41906103);the Taishan Scholars Project to SUN Song;© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2020
- DOI：10.1007/s00343-020-0040-7
  中图分类号：
- 收稿：2020-01-17，
  
  录用：2020-3-27，
  
  网络首发：2020-05-18，
  
  纸质出版：2020-07
- Accepted：
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Identification and characterization of endosymbiosis-related immune genes in deep-sea mussels Gigantidas platifrons[J]. 海洋湖沼学报（英文）, 2020,38(4):1292-1303.

Mengna LI, Hao CHEN, Minxiao WANG, et al. Identification and characterization of endosymbiosis-related immune genes in deep-sea mussels Gigantidas platifrons[J]. Journal of Oceanology and Limnology, 2020, 38(4): 1292-1303.
Identification and characterization of endosymbiosis-related immune genes in deep-sea mussels Gigantidas platifrons[J]. 海洋湖沼学报（英文）, 2020,38(4):1292-1303. DOI： 10.1007/s00343-020-0040-7.

Mengna LI, Hao CHEN, Minxiao WANG, et al. Identification and characterization of endosymbiosis-related immune genes in deep-sea mussels Gigantidas platifrons[J]. Journal of Oceanology and Limnology, 2020, 38(4): 1292-1303. DOI： 10.1007/s00343-020-0040-7.

摘要

Abstract

Deep-sea mussels of the subfamily Bathymodiolinae are common and numerically dominant species widely distributed in cold seeps and hydrothermal vents. During long-time evolution

deep-sea mussels have evolved to be well adapted to the local environment of cold seeps and hydrothermal vents by various ways

especially by establishing endosymbiosis with chemotrophic bacteria. However

biological processes underlying the establishment and maintenance of symbiosis between host mussels and symbionts are largely unclear. In the present study

Gigantidas platifrons

genes possibly involved in the symbiosis with methane oxidation symbionts were identified and characterized by Lipopolysaccharide (LPS) pull-down and

in situ

hybridization. Five immune related proteins including Toll-like receptor 2 (TLR2)

integrin

vacuolar sorting protein (VSP)

matrix metalloproteinase 1 (MMP1)

and leucine-rich repeat (LRR-1) were identified by LPS pull-down assay. These five proteins were all conserved in either molecular sequences or functional domains and known to be key molecules in host immune recognition

phagocytosis

and lysosome-mediated digestion. Furthermore

in situ

hybridization of LRR-1

TLR2 and VSP genes was conducted to investigate their expression patterns in gill tissues of

platifrons

. Consequently

LRR-1

TLR2

and VSP genes were found expressed exclusively in the bacteriocytes of

platifrons

. Therefore

it was suggested that TLR2

integrin

VSP

MMP1

and LRR-1 might be crucial molecules in the symbiosis between

platifrons

and methane oxidation bacteria by participating in symbiosis-related immune processes.

关键词

Keywords

references

S Akira , K Takeda . Toll-like receptor signalling . Nature Reviews Immunology , 2004 . 4 ( 7 ): 499 - 511 . DOI: 10.1038/nri1391 http://doi.org/10.1038/nri1391 .

J P Barry , K R Buck , R K Kochevar , D C Nelson , Y Fujiwara , S K Goffredi , J Hashimoto . Methane-based symbiosis in a mussel, Bathymodiolus platifrons , from cold seeps in Sagami Bay, Japan . Invertebrate Biology , 2002 . 121 ( 1 ): 47 - 54 . DOI: 10.1111/j.1744-7410.2002.tb00128.x http://doi.org/10.1111/j.1744-7410.2002.tb00128.x .

R Bettencourt , P Dando , P Collins , V Costa , B Allam , R Serrão Santos . Innate immunity in the deep sea hydrothermal vent mussel Bathymodiolus azoricus . Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology , 2009 . 152 ( 2 ): 278 - 289 . DOI: 10.1016/j.cbpa.2008.10.022 http://doi.org/10.1016/j.cbpa.2008.10.022 .

R Bettencourt , M Pinheiro , C Egas , P Gomes , M Afonso , T Shank , R Serrão Santos . High-throughput sequencing and analysis of the gill tissue transcriptome from the deep-sea hydrothermal vent mussel Bathymodiolus azoricus . BMC Genomics , 2010 . 11 ( 1 ): 559 DOI: 10.1186/1471-2164-11-559 http://doi.org/10.1186/1471-2164-11-559 .

J M Brooks , Ⅱ M C Kennicutt , C R Fisher , S A Macko , K Cole , J J Childress , R R Bidigare , R D Vetter . Deep-sea hydrocarbon seep communities: evidence for energy and nutritional carbon sources . Science , 1987 . 238 ( 4830 ): 1 138 - 1 142 . DOI: 10.1126/science.238.4830.1138 http://doi.org/10.1126/science.238.4830.1138 .

L Cerenius , K Söderhäll . Variable immune molecules in invertebrates . Journal of Experimental Biology , 2013 . 216 ( 23 ): 4 313 - 4 319 . DOI: 10.1242/jeb.085191 http://doi.org/10.1242/jeb.085191 .

H Chen , M X Wang , H Zhang , H Wang , Z Lv , L Zhou , Z S Zhong , C Lian , L Cao , C L Li . An LRR-domain containing protein identified in Bathymodiolus platifrons serves as intracellular recognition receptor for the endosymbiotic methane-oxidation bacteria . Fish & Shellfish Immunology , 2019 . 93 354 - 360 . DOI: 10.1016/j.fsi.2019.07.032 http://doi.org/10.1016/j.fsi.2019.07.032 .

J Chow , S M Lee , Y Shen , A Khosravi , S K Mazmanian . Host-bacterial symbiosis in health and disease . Advances in Immunology , 2010 . 107 243 - 274 . DOI: 10.1016/B978-0-12-381300-8.00008-3 http://doi.org/10.1016/B978-0-12-381300-8.00008-3 .

H Chu , S K Mazmanian . Innate immune recognition of the microbiota promotes host-microbial symbiosis . Nature Immunology , 2013 . 14 ( 7 ): 668 - 675 . DOI: 10.1038/ni.2635 http://doi.org/10.1038/ni.2635 .

J B Corliss , J Dymond , L I Gordon , J M Edmond , R P von Herzen , R D Ballard , K Green , D Williams , A Bainbridge , K Crane , T H van Andel . Submarine thermal springs on the Galápagos Rift . Science , 1979 . 203 ( 4385 ): 1 073 - 1 083 . DOI: 10.1126/science.203.4385.1073 http://doi.org/10.1126/science.203.4385.1073 .

R Danovaro , C Corinaldesi , A Dell'Anno , P V R Snelgrove . The deep-sea under global change . Current Biology , 2017 . 27 ( 11 ): R461 - R465 . DOI: 10.1016/j.cub.2017.02.046 http://doi.org/10.1016/j.cub.2017.02.046 .

R Danovaro , P V R Snelgrove , P Tyler . Challenging the paradigms of deep-sea ecology . Trends in Ecology & Evolution , 2014 . 29 ( 8 ): 465 - 475 . DOI: 10.1016/j.tree.2014.06.002 http://doi.org/10.1016/j.tree.2014.06.002 .

C Détrée , F H Lallier , A Tanguy , J Mary . Identification and gene expression of multiple peptidoglycan recognition proteins (PGRPs) in the deep-sea mussel Bathymodiolus azoricus , involvement in symbiosis? . Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology , 2017 . 207 1 - 8 . DOI: 10.1016/j.cbpb.2017.02.002 http://doi.org/10.1016/j.cbpb.2017.02.002 .

N Dubilier , C Bergin , C Lott . Symbiotic diversity in marine animals: the art of harnessing chemosynthesis . Nature Reviews Microbiology , 2008 . 6 ( 10 ): 725 - 740 . DOI: 10.1038/nrmicro1992 http://doi.org/10.1038/nrmicro1992 .

D Feng , M Cheng , S Kiel , J W Qiu , Q H Yang , H Y Zhou , Y B Peng , D F Chen . Using Bathymodiolus tissue stable carbon, nitrogen and sulfur isotopes to infer biogeochemical process at a cold seep in the South China Sea . Deep Sea Research Part I: Oceanographic Research Papers , 2015 . 104 52 - 59 . DOI: 10.1016/j.dsr.2015.06.011 http://doi.org/10.1016/j.dsr.2015.06.011 .

A Fiala-Médioni , Z McKiness , P Dando , J Boulegue , A Mariotti , A Alayse-Danet , J Robinson , C Cavanaugh . Ultrastructural, biochemical, and immunological characterization of two populations of the mytilid mussel Bathymodiolus azoricus from the Mid-Atlantic Ridge:evidence for a dual symbiosis . Marine Biology , 2002 . 141 ( 6 ): 1 035 - 1 043 . DOI: 10.1007/s00227-002-0903-9 http://doi.org/10.1007/s00227-002-0903-9 .

K M Fontanez , C M Cavanaugh . Evidence for horizontal transmission from multilocus phylogeny of deep-sea mussel (Mytilidae) symbionts . Environmental Microbiology , 2014 . 16 ( 12 ): 3 608 - 3 621 . DOI: 10.1111/1462-2920.12379 http://doi.org/10.1111/1462-2920.12379 .

Y Fujiwara , K Takai , K Uematsu , S Tsuchida , J C Hunt , J Hashimoto . Phylogenetic characterization of endosymbionts in three hydrothermal vent mussels:influence on host distributions . Marine Ecology Progress Series , 2000 . 208 147 - 155 . DOI: 10.3354/meps208147 http://doi.org/10.3354/meps208147 .

F G Giancotti , E Ruoslahti . Integrin signaling . Science , 1999 . 285 ( 5430 ): 1 028 - 1 033 . DOI: 10.1126/science.285.5430.1028 http://doi.org/10.1126/science.285.5430.1028 .

S Halary , V Riou , F Gaill , T Boudier , S Duperron . 3D FISH for the quantification of methane- and sulphuroxidizing endosymbionts in bacteriocytes of the hydrothermal vent mussel Bathymodiolus azoricus . The ISME Journal , 2008 . 2 ( 3 ): 284 - 292 . DOI: 10.1038/ismej.2008.3 http://doi.org/10.1038/ismej.2008.3 .

M J Humphries . Integrin structure . Biochemical Society Transactions , 2000 . 28 ( 4 ): 311 - 39 . DOI: 10.1042/bst0280311 http://doi.org/10.1042/bst0280311 .

E Kádár , S A Davis , A Lobo-da-Cunha . Cytoenzymatic investigation of intracellular digestion in the symbiontbearing hydrothermal bivalve Bathymodiolus azoricus . Marine Biology , 2008 . 153 ( 5 ): 995 - 1 004 . DOI: 10.1007/s00227-007-0872-0 http://doi.org/10.1007/s00227-007-0872-0 .

T Kawai , S Akira . The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors . Nature Immunology , 2010 . 11 ( 5 ): 373 - 384 . DOI: 10.1038/ni.1863 http://doi.org/10.1038/ni.1863 .

Ⅱ M C Kennicutt , J M Brooks , R R Bidigare , R R Fay , T L Wade , T J McDonald . Vent-type taxa in a hydrocarbon seep region on the Louisiana slope . Nature , 1985 . 317 ( 6035 ): 315 - 353 . DOI: 10.1038/317351a0 http://doi.org/10.1038/317351a0 .

L Kolesnikova , T Strecker , E Morita , F Zielecki , E Mittler , C Crump , S Becker . Vacuolar protein sorting pathway contributes to the release of Marburg virus . Journal of Virology , 2009 . 83 ( 5 ): 2 327 - 2 337 . DOI: 10.1128/JVI.02184-08 http://doi.org/10.1128/JVI.02184-08 .

H Li , X Y Huang , Z H Zeng , X X Peng , B Peng . Identification of the interactome between fish plasma proteins and Edwardsiella tarda reveals tissue-specific strategies against bacterial infection . The International Journal of Biochemistry & Cell Biology , 2016 . 78 260 - 267 . DOI: 10.1016/j.biocel.2016.07.021 http://doi.org/10.1016/j.biocel.2016.07.021 .

E Martins , A Figueras , B Novoa , R Serrão Santos , R Moreira , R Bettencourt . Comparative study of immune responses in the deep-sea hydrothermal vent mussel Bathymodiolus azoricus and the shallow-water mussel Mytilus galloprovincialis challenged with Vibrio bacteria . Fish & Shellfish Immunology , 2014 . 40 ( 2 ): 485 - 499 . DOI: 10.1016/j.fsi.2014.07.018 http://doi.org/10.1016/j.fsi.2014.07.018 .

R Ponnudurai , M Kleiner , L Sayavedra , J M Petersen , M Moche , A Otto , D Becher , T Takeuchi , N Satoh , N Dubilier , T Schweder , S Markert . Metabolic and physiological interdependencies in the Bathymodiolus azoricus symbiosis . The ISME Journal , 2017 . 11 ( 2 ): 463 - 477 . DOI: 10.1038/ismej.2016.124 http://doi.org/10.1038/ismej.2016.124 .

L Sayavedra , M Kleiner , R Ponnudurai , S Wetzel , E Pelletier , V Barbe , N Satoh , E Shoguchi , D Fink , C Breusing , T B H Reusch , P Rosenstiel , M B Schilhabe , D Becher , T Schweder , S Markert , N Dubilier , J M Petersen . Abundant toxin-related genes in the genomes of beneficial symbionts from deep-sea hydrothermal vent mussels . eLife , 2015 . 4 e07966 DOI: 10.7554/eLife.07966.001 http://doi.org/10.7554/eLife.07966.001 .

M Sibuet , K Olu . Biogeography, biodiversity and fluid dependence of deep-sea cold-seep communities at active and passive margins . Deep Sea Research Part Ⅱ: Topical Studies in Oceanography , 1998 . 45 ( 1-3 ): 517 - 567 . DOI: 10.1016/s0967-0645(97)00074-x http://doi.org/10.1016/s0967-0645(97)00074-x .

S M Sievert , C Vetriani . Chemoautotrophy at deep-sea vents: past, present, and future . Oceanography , 2015 . 25 ( 1 ): 218 - 233 . DOI: 10.5670/oceanog.2012.21 http://doi.org/10.5670/oceanog.2012.21 .

J Sun , Y Zhang , T Xu , Y Zhang , H W Mu , Y J Zhang , Y Lan , C J Fields , J H L Hui , W P Zhang , R S Li , W Y Nong , F K M Cheung , J W Qiu , P Y Qian . Adaptation to deep-sea chemosynthetic environments as revealed by mussel genomes . Nature Ecology & Evolution , 2017 . 1 ( 5 ): 0121 DOI: 10.1038/s41559-017-0121 http://doi.org/10.1038/s41559-017-0121 .

C L Van Dover , C R German , K G Speer , L M Parson , R C Vrijenhoek . Evolution and biogeography of deep-sea vent and seep invertebrates . Science , 2002 . 295 ( 5558 ): 1 253 - 1 257 . DOI: 10.1126/science.1067361 http://doi.org/10.1126/science.1067361 .

P Van Lint , C Libert . Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and inflammation . Journal of Leukocyte Biology , 2007 . 82 ( 6 ): 1 375 - 1 381 . DOI: 10.1189/jlb.0607338 http://doi.org/10.1189/jlb.0607338 .

R P Verma , C Hansch . Matrix metalloproteinases(MMPs): chemical-biological functions and (Q)SARs . Bioorganic & Medicinal Chemistry , 2007 . 15 ( 6 ): 2 223 - 2 268 . DOI: 10.1016/j.bmc.2007.01.011 http://doi.org/10.1016/j.bmc.2007.01.011 .

C Wentrup , A Wendeberg , J Y Huang , C Borowski , N Dubilier . Shift from widespread symbiont infection of host tissues to specific colonization of gills in juvenile deepsea mussels . The ISME Journal , 2013 . 7 ( 6 ): 1 244 - 1 247 . DOI: 10.1038/ismej.2013.5 http://doi.org/10.1038/ismej.2013.5 .

Y J Won , S J Hallam , G D O'Mullan , I L Pan , K R Buck , R C Vrijenhoek . Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus Bathymodiolus . Applied and Environmental Microbiology , 2003 . 69 ( 11 ): 6 785 - 6 792 . DOI: 10.1128/aem.69.11.6785-6792.2003 http://doi.org/10.1128/aem.69.11.6785-6792.2003 .

Y H Wong , J Sun , L S He , L G Chen , J W Qiu , P Y Qian . High-throughput transcriptome sequencing of the cold seep mussel Bathymodiolus platifrons . Scientific Reports , 2015 . 5 ( 1 ): 16597 DOI: 10.1038/srep16597 http://doi.org/10.1038/srep16597 .

C L Wu , K Söderhäll , I Söderhäll . Two novel ficolin-like proteins act as pattern recognition receptors for invading pathogens in the freshwater crayfish Pacifastacus leniusculus . Proteomics , 2011 . 11 ( 11 ): 2 249 - 2 264 . DOI: 10.1002/pmic.201000728 http://doi.org/10.1002/pmic.201000728 .

J C Xu , S Jiang , Y Q Li , M J Li , Q Cheng , D P Zhao , B Yang , Z H Jia , L L Wang , L S Song . Caspase-3 serves as an intracellular immune receptor specific for lipopolysaccharide in oyster Crassostrea gigas . Developmental & Comparative Immunology , 2016 . 61 1 - 12 . DOI: 10.1016/j.dci.2016.03.015 http://doi.org/10.1016/j.dci.2016.03.015 .

P Zheng , M X Wang , C L Li , X Q Sun , X C Wang , Y Sun , S Sun . Insights into deep-sea adaptations and hostsymbiont interactions: a comparative transcriptome study on Bathymodiolus mussels and their coastal relatives . Molecular Ecology , 2017 . 26 ( 19 ): 5 133 - 5 148 . DOI: 10.1111/mec.14160 http://doi.org/10.1111/mec.14160 .

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Identification and characterization of endosymbiosis-related immune genes in deep-sea mussels Gigantidas platifrons

DOI：10.1007/s00343-020-0040-7

摘要

Abstract

关键词

Keywords

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