Transcriptome analysis reveals immune-related genes in tissues of <italic style="font-style: italic">Vibrio anguillarum</italic>-infected turbot <italic style="font-style: italic">Scophthalmus maximus</italic>

Yuting SONG; Maqsood Ahmed SOOMRO; Xianzhi DONG; Guobin HU

doi:10.1007/s00343-023-2363-7

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Transcriptome analysis reveals immune-related genes in tissues of Vibrio anguillarum-infected turbot Scophthalmus maximus

Aquaculture and Fisheries | Updated：2024-10-15

- Transcriptome analysis reveals immune-related genes in tissues of Vibrio anguillarum-infected turbot Scophthalmus maximus
- Transcriptome analysis reveals immune-related genes in tissues of Vibrio anguillarum-infected turbot Scophthalmus maximus
- 海洋湖沼学报(英文) 2024年42卷第1期页码：332-344
- Affiliations：
  
  1.College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
  2.Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao 266003, China
  3.Institute of Biophysis, Chinese Academy of Sciences, Beijing 100101, China
- Author bio：
  
  xzdong@ibp.ac.cn
  huguobin@ouc.edu.cn
- Funds：
  
  the National Key Research and Development Program of the Ministry of Science and Technology (CN)(2022YFD2400401);the Key Research and Development Plan of Shandong Province (CN) (for Academician Team in Shandong)(2023ZLYS02);the Fundamental Research Funds for the Central Universities(202261029);the Enterprise Authorized Project(20200025)
- DOI：10.1007/s00343-023-2363-7
  中图分类号：
- 收稿：2022-09-15，
  
  录用：2022-11-04，
  
  网络首发：2023-02-16，
  
  纸质出版：2024-01-03
- Accepted：
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Transcriptome analysis reveals immune-related genes in tissues of Vibrio anguillarum-infected turbot Scophthalmus maximus[J]. 海洋湖沼学报(英文), 2024,42(1):332-344.

SONG Yuting,SOOMRO Maqsood Ahmed,DONG Xianzhi,et al.Research PaperTranscriptome analysis reveals immune-related genes in tissues of Vibrio anguillarum-infected turbot Scophthalmus maximus[J].Journal of Oceanology and Limnology,2024,42(01):332-344.
Transcriptome analysis reveals immune-related genes in tissues of Vibrio anguillarum-infected turbot Scophthalmus maximus[J]. 海洋湖沼学报(英文), 2024,42(1):332-344. DOI： 10.1007/s00343-023-2363-7.

SONG Yuting,SOOMRO Maqsood Ahmed,DONG Xianzhi,et al.Research PaperTranscriptome analysis reveals immune-related genes in tissues of Vibrio anguillarum-infected turbot Scophthalmus maximus[J].Journal of Oceanology and Limnology,2024,42(01):332-344. DOI： 10.1007/s00343-023-2363-7.

摘要

Abstract

Turbot

Scophthalmus maximus

is an important mariculture fish species with high economic value.

However

the bacterial diseases caused by

Vibrio anguillarum

infection bring huge economic losses to the turbot aquaculture industry. To understand the immune response of the turbot against

anguillarum

infection and to explore novel immune-related genes

the transcriptome analysis of turbot spleen and gills were conducted after

anguillarum

infection. Differentially expressed genes (DEGs) were identified in spleen and gill of the turbot amounted to 17 261 and 16 436

respectively. A large number of immune-related DEGs were enriched in cytokine-cytokine receptor interaction signaling pathway

and the others by the kyoto encyclopedia of genes and genomes (KEGG) enrichment. The gene ontology (GO) classification analysis revealed that

anguillarum

infection had the greatest effect on biological processes and cellular components. Twelve immune-related DEGs were identified in the spleen (

cstl

egfl6

lamb21

v2rx4

calcr

and

gpr78a

) and gills (

ghra

sh3gl2a

cst12

inhbaa

cxcl8

and

) by heat map. The protein-protein interaction (PPI) networks were constructed to analyze the

immune mechanism. The results demonstrate that the maturation and antigen processing of major histocompatibility complex (MHC) class II molecule

and calcitonin- or adrenomedullin-regulated physiological activity were important events in the immunity of turbot against

anguillarum

infection. In the gills

the protein interactions in TGF-β signaling pathway

production of inflammatory factors

and endocytosis regulation were most significant. Our research laid a foundation for discovering novel immune-related genes and enriching the knowledge of immune mechanisms of turbot against

anguillarum

infection.

关键词

Keywords

references

Aiyar N , Disa J , Ao Z H et al . 2002 . Molecular cloning and pharmacological characterization of bovine calcitonin receptor-like receptor from bovine aortic endothelial cells . Biochemical Pharmacology , 63 ( 11 ): 1949 - 1959 , https://doi.org/10.1016/S0006-2952(02)00990-5 https://doi.org/10.1016/S0006-2952(02)00990-5 .

Cerdà-Cuéllar M , Rosselló-Mora R A , Lalucat J et al . 1997 . Vibrio scophthalmi sp. nov., a new species from turbot ( Scophthalmus maximus ) . International Journal of Systematic Bacteriology , 47 ( 1 ): 58 - 61 , https://doi.org/10.1099/00207713-47-1-58 https://doi.org/10.1099/00207713-47-1-58 .

Cestra G , Castagnoli L , Dente L et al . 1999 . The SH3 domains of endophilin and amphiphysin bind to the proline-rich region of synaptojanin 1 at distinct sites that display an unconventional binding specificity . Journal of Biological Chemistry , 274 ( 45 ): 32001 - 32007 , https://doi.org/10.1074/jbc.274.45.32001 https://doi.org/10.1074/jbc.274.45.32001 .

Chai Y M , Huang X H , Cong B L et al . 2006 . Involvement of VAMP-2 in exocytosis of IL-1β in turbot ( Scophthalmus maximus ) leukocytes after Vibrio anguillarum infection . Biochemical and Biophysical Research Communications , 342 ( 2 ): 509 - 513 , https://doi.org/10.1016/j.bbrc.2006.01.138 https://doi.org/10.1016/j.bbrc.2006.01.138 .

Cullinan E B , Kwee L , Nunes P et al . 1998 . IL-1 receptor accessory protein is an essential component of the IL-1 receptor . The Journal of Immunology , 161 ( 10 ): 5614 - 5620 , https://doi.org/10.4049/jimmunol.161.10.5614 https://doi.org/10.4049/jimmunol.161.10.5614 .

Dalmo R A , Ingebrigtsen K , Bøgwald J . 1997 . Non-specific defence mechanisms in fish, with particular reference to the reticuloendothelial system (RES) . Journal of Fish Diseases , 20 ( 4 ): 241 - 273 , https://doi.org/10.1046/j.1365-2761.1997.00302.x https://doi.org/10.1046/j.1365-2761.1997.00302.x .

Estes R M , Friedman C S , Elston R A et al . 2004 . Pathogenicity testing of shellfish hatchery bacterial isolates on Pacific oyster Crassostrea gigas larvae . Diseases of Aquatic Organisms , 58 ( 2-3 ): 223 - 230 , https://doi.org/10.3354/dao058223 https://doi.org/10.3354/dao058223 .

Fang J F , Xu C X , Li Q . 2022 . Transcriptome analysis of inbreeding depression in the Pacific oyster Crassostrea gigas . Aquaculture , 557 : 738314 , https://doi.org/10.1016/j.aquaculture.2022.738314 https://doi.org/10.1016/j.aquaculture.2022.738314 .

Fernández-González R , Pérez-Pérez M , Garza-Gil M D . 2021 . An analysis of production factors for Galician-farmed turbot: from boom to stagnation . Aquaculture Economics & Management , 25 ( 3 ): 320 - 338 , https://doi.org/10.1080/13657305.2020.1840659 https://doi.org/10.1080/13657305.2020.1840659 .

Fitzsimmons T J , Zhao X L , Wank S A . 2003 . The extracellular domain of receptor activity-modifying protein 1 is sufficient for calcitonin receptor-like receptor function . Journal of Biological Chemistry , 278 ( 16 ): 14313 - 14320 , https://doi.org/10.1074/jbc.M211946200 https://doi.org/10.1074/jbc.M211946200 .

Frans I , Michiels C W , Bossier P et al . 2011 . Vibrio anguillarum as a fish pathogen: virulence factors, diagnosis and prevention . Journal of Fish Diseases , 34 ( 9 ): 643 - 661 , https://doi.org/10.1111/j.1365-2761.2011.01279.x https://doi.org/10.1111/j.1365-2761.2011.01279.x .

Gao C B , Cai X , Fu Q et al . 2019 . Dynamics of miRNA transcriptome in turbot ( Scophthalmus maximus L.) intestine following Vibrio anguillarum infection . Marine Biotechnology , 21 ( 4 ): 550 - 564 , https://doi.org/10.1007/s10126-019-09903-z https://doi.org/10.1007/s10126-019-09903-z .

Gao Y H , Gao Y T , Huang B et al . 2020 . Reference gene validation for quantification of gene expression during ovarian development of turbot ( Scophthalmus maximus ) . Scientific Reports , 10 ( 1 ): 823 , https://doi.org/10.1038/s41598-020-57633-3 https://doi.org/10.1038/s41598-020-57633-3 .

Guanhua Y , Wang C , Wang X T et al . 2018 . Complete genome sequence of the marine fish pathogen Vibrio anguillarum and genome-wide transposon mutagenesis analysis of genes essential for in vivo infection . Microbiological Research , 216 : 97 - 107 , https://doi.org/10.1016/j.micres.2018.08.011 https://doi.org/10.1016/j.micres.2018.08.011 .

Gunčar G , Pungerčič G , Klemenčič I et al . 1999 . Crystal structure of MHC class II-associated p41 II fragment bound to cathepsin L reveals the structural basis for differentiation between cathepsins L and S . The EMBO Journal , 18 ( 4 ): 793 - 803 , https://doi.‍org/10.1093/emboj/18.4.793 https://doi.‍org/10.1093/emboj/18.4.793 . https://do 10.1093/emboj/18.4.793 http://dx.doi.org/10.1093/emboj/18.4.793

Hilairet S , Foord S M , Marshall F H et al . 2001 . Protein-protein interaction and not glycosylation determines the binding selectivity of heterodimers between the calcitonin receptor-like receptor and the receptor activity-modifying proteins . Journal of Biological Chemistry , 276 ( 31 ): 29575 - 29581 , https://doi.org/10.1074/jbc.M102722200 https://doi.org/10.1074/jbc.M102722200 .

Hu Y H , Chen L , Sun L . 2011 . CXCL8 of Scophthalmus maximus : expression, biological activity and immunoregulato ry effect . Developmental & Comparative Immunology , 35 ( 10 ): 1032 - 1039 , https://doi.org/10.1016/j.dci.2011.04.002 https://doi.org/10.1016/j.dci.2011.04.002 .

Huang S P , Yang Z Y . 2011 . Economical analysis on the turbot industrial cultivation in China . Guangdong Agricultural Sciences , 38 ( 16 ): 113 - 116 , https://doi.org/10.16768/j.issn.1004-874x.2011.16.015. https://doi.org/10.16768/j.issn.1004-874x.2011.16.015. (in Chinese with English abstract)

Jia P , Jia K T , Yi M S . 2015 . Complete genome sequence of a fish nervous necrosis virus isolated from sea perch ( Lateolabrax japonicus ) in China . Genome Announcements , 3 ( 3 ): e00048 - 15 , https://doi.org/10.1128/genomeA.00048-15 https://doi.org/10.1128/genomeA.00048-15 .

Karbalaei M , Khorshidi M , Sisakht-Pour B et al . 2020 . What are the effects of IL-1β (rs1143634), IL-17A promoter (rs2275913) and TLR4 (rs4986790) gene polymorphism on the outcomes of infection with H . pylori within as Iranian population; A systematic review and meta-analysis . Gene Reports , 20 : 100735 , https://doi.org/10.1016/j.genrep.2020.100735 https://doi.org/10.1016/j.genrep.2020.100735 .

Karsi A , Cao D F , Li P et al . 2002 . Transcriptome analysis of channel catfish ( Ictalurus punctatus ): initial analysis of gene expression and microsatellite-containing cDNAs in the skin . Gene , 285 ( 1-2 ): 157 - 168 , https://doi.org/10.1016/S0378-1119(02)00414-6 https://doi.org/10.1016/S0378-1119(02)00414-6 .

Kroeker A L , Berard A R , Coombs K M . 2012 . Fishing beyond the peer: future omic analyses of virus-host interactions . Journal of Virology & Antiviral Research , 1 : 1 , https://doi.org/10.4172/2324-8955.1000e101 https://doi.org/10.4172/2324-8955.1000e101 .

Li G X , Zhao Y L , Liu Z H et al . 2015 . De novo assembly and characterization of the spleen transcriptome of common carp ( Cyprinus carpio ) using Illumina paired-end sequencing . Fish & Shellfish Immunology , 44 ( 2 ): 420 - 429 , https://doi.org/10.1016/j.fsi.2015.03.014 https://doi.org/10.1016/j.fsi.2015.03.014 .

Li Y K , Xia P Z , Wu J Y et al . 2020 . The potential sensing molecules and signal cascades for protecting teleost fishes against lipopolysaccharide . Fish & Shellfish Immunology , 97 : 235 - 247 , https://doi.org/10.1016/j.fsi.2019.12.050 https://doi.org/10.1016/j.fsi.2019.12.050 .

Librán-Pérez M , Pereiro P , Figueras A et al . 2022 . Transcriptome analysis of turbot ( Scophthalmus maximus ) infected with Aeromonas salmonicida reveals a direct effect on leptin synthesis as a neuroendocrine mediator of inflammation and metabolism regulation . Frontiers in Marine Science , 9 : 888115 , https://doi.org/10.3389/fmars.2022.888115 https://doi.org/10.3389/fmars.2022.888115 .

Martens J W M , de Winter J P , Timmerman M A et al . 1997 . Inhibin interferes with activin signaling at the level of the activin receptor complex in Chinese hamster ovary cells . Endocrinology , 138 ( 7 ): 2928 - 2936 , https://doi.org/10.1210/endo.138.7.5250 https://doi.org/10.1210/endo.138.7.5250 .

Martin S A , Caplice N C , Davey G C et al . 2002 . EST-based identification of genes expressed in the liver of adult Atlantic salmon ( Salmo salar ) . Biochemical and Biophysical Research Communications , 293 ( 1 ): 578 - 585 , https://doi.org/10.1016/S0006-291X(02)00263-2 https://doi.org/10.1016/S0006-291X(02)00263-2 .

McLatchie L M , Fraser N J , Main M J et al . 1998 . RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor . Nature , 393 ( 6683 ): 333 - 339 , https://doi.org/10.1038/30666 https://doi.org/10.1038/30666 .

Meijer A H , Verbeek F J , Salas-Vidal E et al . 2005 . Transcriptome profiling of adult zebrafish at the late stage of chronic tuberculosis due to Mycobacterium marinum infection . Molecular Immunology , 42 ( 10 ): 1185 - 1203 , https://doi.org/10.1016/j.molimm.2004.11.014 https://doi.org/10.1016/j.molimm.2004.11.014 .

Micheva K D , Ramjaun A R , Kay B K et al . 1997 . SH3 domain-dependent interactions of endophilin with amphiphysin . FEBS Letters , 414 ( 2 ): 308 - 312 , https://doi.org/10.1016/S0014-5793(97)01016-8 https://doi.org/10.1016/S0014-5793(97)01016-8 .

Modregger J , Schmidt A A , Ritter B et al . 2003 . Characterization of Endophilin B1b, a brain-specific membrane-associated lysophosphatidic acid acyl transferase with properties distinct from endophilin A1 . Journal of Biological Chemistry , 278 ( 6 ): 4160 - 4167 , https://doi.org/10.1074/jbc.M208568200 https://doi.org/10.1074/jbc.M208568200 .

Morozova O , Hirst M , Marra M A . 2009 . Applications of new sequencing technologies for transcriptome analysis . Annual Review of Genomics and Human Genetics , 10 : 135 - 151 , https://doi.org/10.1146/annurev-genom-082908-145957 https://doi.org/10.1146/annurev-genom-082908-145957 .

Mutz K O , Heilkenbrinker A , Lönne M et al . 2013 . Transcriptome analysis using next-generation sequencing . Current Opinion in Biotechnology , 24 ( 1 ): 22 - 30 , https://doi.org/10.1016/j.copbio.2012.09.004 https://doi.org/10.1016/j.copbio.2012.09.004 .

Nie X B , Zhang C F , Jiang C X et al . 2020 . Characterizing transcriptome changes in gill tissue of turbot ( Scophthalmus maximus ) for waterless preservation . Aquaculture , 518 : 734830 , https://doi.org/10.1016/j.aquaculture.2019.734830 https://doi.org/10.1016/j.aquaculture.2019.734830 .

Nikitenko L L , MacKenzie I Z , Rees M C et al . 2000 . Adrenomedullin is an autocrine regulator of endothelial growth in human endometrium . Molecular Human Reproduction , 6 ( 9 ): 811 - 819 , https://doi.org/10.1093/molehr/6.9.811 https://doi.org/10.1093/molehr/6.9.811 .

Oisson J C , Jöborn A , Westerdahl A et al . 1996 . Is the turbot, Scophthalmus maximus (L.), intestine a portal of entry for the fish pathogen Vibrio anguillarum ? Journal of Fish Diseases , 19 ( 3 ): 225 - 234 , https://doi.org/10.1111/j.1365-2761.1996.tb00129.x https://doi.org/10.1111/j.1365-2761.1996.tb00129.x .

Pereiro P , Balseiro P , Romero A et al . 2012 . High-throughput sequence analysis of turbot ( Scophthalmus maximus ) tra nscriptome using 454-pyrosequencing for the discovery of antiviral immune genes . PLoS ONE , 7 ( 5 ): e35369 , https://doi.org/10.1371/journal.pone.0035369 https://doi.org/10.1371/journal.pone.0035369 .

Pujalte M J , Sitjà-Bobadilla A , Macián M C et al . 2003 . Virulence and molecular typing of Vibrio harveyi strains isolated from cultured dentex, gilthead sea bream and European sea bass . Systematic and Applied Microbiology , 26 ( 2 ): 284 - 292 , https://doi.org/10.1078/072320203322346146 https://doi.org/10.1078/072320203322346146 .

Robledo D , Ronza P , Harrison P W et al . 2014 . RNA-seq analysis reveals significant transcriptome changes in turbot ( Scophthalmus maximus ) suffering severe enteromyxosis . BMC Genomics , 15 ( 1 ): 1149 , https://doi.org/10.1186/1471-2164-15-1149 https://doi.org/10.1186/1471-2164-15-1149 .

Ronza P , Robledo D , Bermúdez R et al . 2019 . Corrigendum: integrating genomic and morphological approaches in fish pathology research: the case of turbot ( Scophthalmus Maximus ) enteromyxosis . Frontiers in Genetics , 10 : 225 , https://doi.org/10.3389/fgene.2019.00225 https://doi.org/10.3389/fgene.2019.00225 .

Song L F , Dong X Z , Hu G B . 2021a . Transcriptome analysis of red sea bream ( Pagrus major ) head kidney and spleen infected by Vibrio anguillarum . Aquaculture Reports , 21 : 100789 , https://doi.org/10.1016/J.AQREP.2021.100789 https://doi.org/10.1016/J.AQREP.2021.100789 .

Song Y T , Dong X Z , Hu G B . 2022 . Transcriptome analysis of turbot ( Scophthalmus maximus ) head kidney and liver reveals immune mechanism in response to Vibrio anguillarum infection . Journal of Fish Diseases , 45 ( 7 ): 1045 - 1057 , https://doi.org/10.1111/jfd.13628 https://doi.org/10.1111/jfd.13628 .

Song Y T , Song L F , Soomro M A et al . 2021b . Transcriptome analysis reveals immune-related differentially expressed genes in the hepatopancreas and gills of Penaeus vannamei after Vibrio anguillarum infection . Aquaculture Research , 52 ( 9 ): 4303 - 4316 , https://doi.org/10.1111/ARE.15268 https://doi.org/10.1111/ARE.15268 .

Tan D M , Dahl A , Middelboe M . 2015 . Vibriophages differentially influence biofilm formation by Vibrio anguillarum strains . Applied and Environmental Microbiology , 81 ( 13 ): 4489 - 4497 , https://doi.org/10.1128/AEM.00518-15 https://doi.org/10.1128/AEM.00518-15 .

Thompson T B , Lerch T F , Cook R W et al . 2005 . The structure of the follistatin: activin complex reveals antagonism of both type I and type II receptor binding . Developmental Cell , 9 ( 4 ): 535 - 543 , https://doi.org/10.1016/j.devcel.2005.09.008 https://doi.org/10.1016/j.devcel.2005.09.008 .

Xie Z Y , Hu C Q , Zhang L P et al . 2007 . Identification and pathogenicity of Vibrio ponticus affecting cultured Japanese sea bass, Lateolabrax japonicus (Cuvier in Cuvier and Valenciennes) . Letters in Applied Microbiology , 45 ( 1 ): 62 - 67 , https://doi.org/10.1111/j.1472-765X.2007.02141.x https://doi.org/10.1111/j.1472-765X.2007.02141.x .

Xiu Y , Su L , Guo B et al . 2022 . Transcriptomic profiling reveals the protection mechanism of bivalent inactivated bacteria vaccine Aeromonas salmonicida and Vibrio scophthalmi in turbot ( Scophthalmus maximus ) . Aquaculture , 560 : 738479 , https://doi.org/10.1016/j.aquaculture.2022.738479 https://doi.org/10.1016/j.aquaculture.2022.738479 .

Xue T , Liu Y P , Cao M et al . 2021a . Transcriptome analysis reveals deep insights into the early immune response of turbot ( Scophthalmus maximus ) induced by inactivated Aeromonas salmonicida vaccine . Fish & Shellfish Immunology , 119 : 163 - 172 , https://doi.org/10.1016/j.fsi.2021.09.027 https://doi.org/10.1016/j.fsi.2021.09.027 .

Xue T , Liu Y P , Cao M et al . 2021b . Revealing new landscape of turbot ( Scophthalmus maximus ) spleen infected with Aeromonas salmonicida through immune related circ RNA-miRNA-mRNA axis . Biology , 10 ( 7 ): 626 , https://doi.org/10.3390/biology10070626 https://doi.org/10.3390/biology10070626 .

Yang L , Kong Y , Ren H L et al . 2017 . Upregulation of CD74 and its potential association with disease severity in subjects with ischemic stroke . Neurochemistry International , 107 : 148 - 155 , https://doi.org/10.1016/j.neuint.2016.11.007 https://doi.org/10.1016/j.neuint.2016.11.007 .

Zhu J J , Li C , Ao Q W et al . 2015 . Trancriptomic profiling revealed the signatures of acute immune response in tilapia ( Oreochromis niloticus ) following Streptococcus iniae challenge . Fish & Shellfish Immunology , 46 ( 2 ): 346 - 353 , https://doi.org/10.1016/j.fsi.2015.06.027 https://doi.org/10.1016/j.fsi.2015.06.027 .

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Transcriptome analysis reveals immune-related genes in tissues of Vibrio anguillarum-infected turbot Scophthalmus maximus

Transcriptome analysis reveals immune-related genes in tissues of Vibrio anguillarum-infected turbot Scophthalmus maximus

DOI：10.1007/s00343-023-2363-7

摘要

Abstract

关键词

Keywords

references