Comparative transcriptomic analysis of Macrobrachium nipponense in response to Aeromonas veronii or Staphylococcus aureus infection -- Journal of Oceanology and Limnology,2022,40(1):347-359

	Cite this paper:
	Chong HAN, Zhipeng ZHANG, Qiang LI, Qinghua CHEN, Jianrong HUANG. Comparative transcriptomic analysis of Macrobrachium nipponense in response to Aeromonas veronii or Staphylococcus aureus infection[J]. Journal of Oceanology and Limnology, 2022, 40(1): 347-359

Comparative transcriptomic analysis of Macrobrachium nipponense in response to Aeromonas veronii or Staphylococcus aureus infection

Chong HAN¹, Zhipeng ZHANG¹, Qiang LI³, Qinghua CHEN⁴, Jianrong HUANG^1,2

1 State Key Laboratory of Biocontrol, Institute of Aquatic Economic Animals and Guangdong Provincial Key Laboratory for Aquatic Economic Animals, School of life Sciences, Sun Yat-Sen University, Guangzhou 510275, China;
2 Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai 519082, China;
3 School of life Sciences, Guangzhou University, Guangzhou 510006, China;
4 South China Institute of Environmental Science, MEE, Guangzhou 510610, China

Abstract:

Macrobrachium nipponense is an economically important freshwater prawn that is often threatened by many aquatic pathogens. In this study, comparative transcriptomic analysis was firstly used to explore the transcriptional response of M. nipponense to Aeromonas veronii or Staphylococcus aureus stimulation. A total of 400.19 million clean reads were obtained and assembled into 56 944 unigenes with an average length of 1 253 bp. A total of 1 857 differentially expressed genes were found after A. veronii infection, including 677 genes that were up-regulated and 1 180 genes that were down-regulated, while 1 061 significant differentially expressed genes were identified after S. aureus infection, including 390 up-regulated and 671 down-regulated genes. Many immune-related genes including Spaetzle, prophenoloxidase activating factor, C-type lectin, anti-lipopolysaccharide factor, and inhibitor of apoptosis 2 protein were commonly up-regulated after A. veronii or S. aureus infection. This study will enrich our understanding of the immune response to gram-positive and gram-negative bacteria infection in crustaceans.

Key words: Macrobrachium nipponense|differentially expressed genes|Aeromonas veronii|Staphylococcus aureus|immune response

Received: 2020-09-29 Revised:

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Articles by Zhipeng ZHANG

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Articles by Qinghua CHEN

Articles by Jianrong HUANG

References:
Arch R H, Gedrich R W, Thompson C B. 1998. Tumor necrosis factor receptor-associated factors (TRAFs)—a family of adapter proteins that regulates life and death. Genes & Development, 12(18): 2 821-2 830.
Aruoma O I. 1998. Free radicals, oxidative stress, and antioxidants in human health and disease. Journal of the American Oil Chemists’ Society, 75(2): 199-212.
Ashburner M, Ball C A, Blake J A, Botstein D, Butler H, Cherry J M, Davis A P, Dolinski K, Dwight S S, Eppig J T, Harris M A, Hill D P, Issel-Tarver L, Kasarskis A, Lewis S, Matese J C, Richardson J E, Ringwald M, Rubin G M, Sherlock G. 2000. Gene ontology: tool for the unification of biology. Nature Genetics, 25(1): 25-29.
Bao L S, Xia J L. 2017. Global analysis of transcriptome sequences highlights accelerated evolution of immune genes in Danio choprae and Danio albolineatus. Fish & Shellfish Immunology, 66: 390-397.
Belvin M P, Anderson K V. 1996. A conserved signaling pathway: the Drosophila toll-dorsal pathway. Annual Review of Cell and Developmental Biology, 12: 393-416.
Cai Y X, Ng P K L. 2002. The freshwater palaemonid prawns (Crustacea: decapoda: caridea) of Myanmar. Hydrobiologia, 487(1): 59-83.
Cai Y, Dai A Y. 1999. Freshwater shrimps (Crustacea: decapoda: caridea) from the Xishuangbanna region of Yunnan Province, southern China. Hydrobiologia, 400: 211-241.
Cambi A, Figdor C G. 2005. Levels of complexity in pathogen recognition by C-type lectins. Current Opinion in Immunology, 17(4): 345-351.
Chen X W, Wang J, Yue W C, Liu J S, Wang C H. 2017. Hepatopancreas transcriptome analysis of Chinese mitten crab (Eriocheir sinensis) with white hepatopancreas syndrome. Fish & Shellfish Immunology, 70: 302-307.
Fang H, Chen C Z, Zhang X J, Gong Y F, Ge M X. 2008. Examination of the pathogenic Aeromonas veronii isolated from crab Eriocheir sinensis. Chinese Journal of Zoonoses, 24(1): 45-49. (in Chinese with English abstract)
Garber M, Grabherr M G, Guttman M, Trapnell C. 2011. Computational methods for transcriptome annotation and quantification using RNA-seq. Nature Methods, 8(6): 469-477.
Garzoni C, Kelley W L. 2009. Staphylococcus aureus: new evidence for intracellular persistence. Trends in Microbiology, 17(2): 59-65.
Havixbeck J J, Rieger A M, Churchill L J, Barreda D R. 2017. Neutrophils exert protection in early Aeromonas veronii infections through the clearance of both bacteria and dying macrophages. Fish & Shellfish Immunology, 63: 18-30.
Hoffmann J A. 2003. The immune response of Drosophila. Nature, 426(6962): 33-38.
Huang Y, Zhang R D, Gao T H, Xu H, Wu T, Ren Q. 2019. 2-Transmembrane C-type lectin from oriental river prawn Macrobrachium nipponense participates in antibacterial immune response. Fish & Shellfish Immunology, 91: 58-67.
Janda J M, Abbott S L. 2010. The genus Aeromonas: taxonomy, pathogenicity, and infection. Clinical Microbiology Reviews, 23(1): 35-73.
Jang I H, Nam H J, Lee W J. 2008. CLIP-domain serine proteases in Drosophila innate immunity. BMB Reports, 41(2): 102-107.
Jiang G M, Qian C Y, Gu X L, Wei B, Xu L, Song X H. 2016. The etiological agents of bacterial septicemia in Eriocheir sinensis and Procambarus clarkia. Journal of Aquaculture, 37(4): 46-51. (in Chinese with English abstract)
Jiang H B, Wang Y, Kanost M R. 1998. Pro-phenol oxidase activating proteinase from an insect, Manduca sexta: a bacteria-inducible protein similar to Drosophila easter. Proceedings of the National Academy of Sciences of the United States of America, 95(21): 12 220-12 225.
Kan H N, Kim C H, Kwon H M, Park J W, Roh K B, Lee H, Park B J, Zhang R, Zhang J H, Söderhäll K, Ha N C, Lee B L. 2008. Molecular control of phenoloxidase-induced melanin synthesis in an insect. Journal of Biological Chemistry, 283(37): 25 316-25 323.
Kim H Y, Rikihisa Y. 2002. Roles of p38 mitogen-activated protein kinase, NF-κB, and protein kinase C in proinflammatory cytokine mRNA expression by human peripheral blood leukocytes, monocytes, and neutrophils in response to Anaplasma phagocytophila. Infection and Immunity, 70(8): 4 132-4 141.
Langmead B, Salzberg S L. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4): 357-359.
Lee S Y, Soderhall K. 2001. Characterization of a pattern recognition protein, a masquerade-like protein, in the freshwater crayfish Pacifastacus leniusculus. The Journal of Immunology, 166(12): 7 319-7 326.
Lin C Y, Hu K Y, Ho S H, Song Y L. 2006. Cloning and characterization of a shrimp clip domain serine protease homolog (c-SPH) as a cell adhesion molecule. Developmental & Comparative Immunology, 30(12): 1 132-1 144.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the method. Methods, 25(4): 402-408.
Meng Q G, Chen J, Xu C C, Huang Y Q, Wang Y, Wang T T, Zhai X T, Gu W, Wang W. 2013. The characterization, expression and activity analysis of superoxide dismutases (SODs) from Procambarus clarkii. Aquaculture, 406-407: 131-140.
Mu C K, Zhao J M, Wang L L, Song L S, Song X Y, Zhang H, Qiu L M, Gai Y C, Cui Z X. 2009. A thioredoxin with antioxidant activity identified from Eriocheir sinensis. Fish & Shellfish Immunology, 26(5): 716-723.
Núñez-Acuña G, Gallardo-Escárate C. 2013. Identification of immune-related SNPs in the transcriptome of Mytilus chilensis through high-throughput sequencing. Fish & Shellfish Immunology, 35(6): 1 899-1 905.
Otto M. 2014. Staphylococcus aureus toxins. Current Opinion in Microbiology, 17: 32-37.
Pan C Y, Peng K C, Lin C H, Chen J Y. 2011. Transgenic expression of tilapia hepcidin 1-5 and shrimp chelonianin in zebrafish and their resistance to bacterial pathogens. Fish & Shellfish Immunology, 31(2): 275-285.
Pan X T, Li T T, Yang C H, Ren Q, Zhang X W. 2019. A toll receptor is involved in antibacterial defense in the oriental river prawn, Macrobrachium nipponense. Fish & Shellfish Immunology, 92: 583-589.
Rao R, Zhu Y B, Alinejad T, Tiruvayipati S, Thong K L, Wang J, Bhassu S. 2015. RNA-seq analysis of Macrobrachium rosenbergii hepatopancreas in response to Vibrio parahaemolyticus infection. Gut Pathogens, 7: 6.
Ren Q, Xu Z L, Wang X W, Zhao X F, Wang J X. 2009. Clip domain serine protease and its homolog respond to Vibrio challenge in Chinese white shrimp, Fenneropenaeus chinensis. Fish & Shellfish Immunology, 26(5): 787-798.
Ren Y P, Xue J L, Yang H H, Pan B P, Bu W J. 2017. Transcriptome analysis of Ruditapes philippinarum hepatopancreas provides insights into immune signaling pathways under Vibrio anguillarum infection. Fish & Shellfish Immunology, 64: 14-23.
Robinson M D, McCarthy D J, Smyth G K. 2010. EdgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26(1): 139-140.
Sahoo P K, Mahapatra K D, Saha J N, Barat A, Sahoo M, Mohanty B R, Gjerde B, Ødegård J, Rye M, Salte R. 2008. Family association between immune parameters and resistance to Aeromonas hydrophila infection in the Indian major carp, Labeo rohita. Fish & Shellfish Immunology, 25(1-2): 163-169.
Satoh D, Horii A, Ochiai M, Ashida M. 1999. Prophenoloxidaseactivating enzyme of the silkworm, Bombyx mori: purification, characterization, and cDNA cloning. Journal of Biological Chemistry, 274(11): 7 441-7 453.
Shi X Z, Zhang R R, Jia Y P, Zhao X F, Yu X Q, Wang J X. 2009. Identification and molecular characterization of a Spätzle-like protein from Chinese shrimp (Fenneropenaeus chinensis). Fish & Shellfish Immunology, 27(5): 610-617.
Song C W, Cui Z X, Liu Y, Wang S Y, Li Q Q. 2012. First report of two thioredoxin homologues in crustaceans: molecular characterization, genomic organization and expression pattern in swimming crab Portunus trituberculatus. Fish & Shellfish Immunology, 32(5): 855-861.
Song L S, Wang L L, Zhang H, Wang M Q. 2015. The immune system and its modulation mechanism in scallop. Fish & Shellfish Immunology, 46(1): 65-78.
Sun W W, Zhang X X, Wan W S, Wang S Q, Wen X B, Zheng H P, Zhang Y L, Li S K. 2017. Tumor necrosis factor receptor-associated factor 6 (TRAF6) participates in antilipopolysaccharide factors (ALFs) gene expression in mud crab. Developmental & Comparative Immunology, 67: 361-376.
Vazquez-Juarez R C, Gomez-Chiarri M, Barrera-Saldaña H, Hernandez-Saavedra N, Dumas S, Ascencio F. 2005. Evaluation of DNA vaccination of spotted sand bass (Paralabrax maculatofasciatus) with two major outermembrane protein-encoding genes from Aeromonas veronii. Fish & Shellfish Immunology, 19(2): 153-163.
Wang K J, Ren H L, Xu D D, Cai L, Yang M. 2008. Identification of the up-regulated expression genes in hemocytes of variously colored abalone (Haliotis diversicolor Reeve, 1846) challenged with bacteria. Developmental & Comparative Immunology, 32(11): 1 326-1 347.
Wang K L, Espinosa E P, Tanguy A, Allam B. 2016. Alterations of the immune transcriptome in resistant and susceptible hard clams (Mercenaria mercenaria) in response to Quahog Parasite Unknown (QPX) and temperature. Fish & Shellfish Immunology, 49: 163-176.
Wang L, Zhang Y, Wang L, Yang J, Zhou Z, Gai Y, Qiu L, Song L. 2011. A new anti-lipopolysaccharide factor (EsALF-3) from Eriocheir sinensis with antimicrobial activity. African Journal of Biotechnology, 10(77): 17 678-17 689.
Wang M Q, Wang B J, Jiang K Y, Liu M, Shi X W, Wang L. 2018. A mitochondrial manganese superoxide dismutase involved in innate immunity is essential for the survival of Chlamys farreri. Fish & Shellfish Immunology, 72: 282-290.
Wang Y L, Tang T, Gu J H, Li X, Yang X, Gao X B, Liu F S, Wang J H. 2015. Identification of five antilipopolysaccharide factors in oriental river prawn, Macrobrachium nipponense. Fish & Shellfish Immunology, 46(2): 252-260.
Wang Y, Cheng T C, Rayaprolu S, Zou Z, Xia Q Y, Xiang Z H, Jiang H B. 2007. Proteolytic activation of pro-spätzle is required for the induced transcription of antimicrobial peptide genes in lepidopteran insects. Developmental & Comparative Immunology, 31(10): 1 002-1 012.
Weber A N R, Tauszig-Delamasure S, Hoffmann J A, Lelièvre E, Gascan H, Ray K P, Morse M A, Imler J L, Gay N J. 2003. Binding of the Drosophila cytokine Spätzle to Toll is direct and establishes signaling. Nature Immunology, 4(8): 794-800.
Xia J H, Liu P, Liu F, Lin G, Sun F, Tu R J, Yue G H. 2013. Analysis of stress-responsive transcriptome in the intestine of Asian seabass (Lates calcarifer) using RNA-Seq. DNA Research, 20(5): 449-460.
Xiu Y J, Hou L B, Liu X Q, Wang Y H, Gu W, Meng Q G, Wang W. 2015a. Isolation and characterization of two novel C-type lectins from the oriental river prawn, Macrobrachium nipponense. Fish & Shellfish Immunology, 46(2): 603-611.
Xiu Y J, Wang Y H, Bi J X, Liu Y H, Ning M X, Liu H, Li S, Gu W, Wang W, Meng Q G. 2016. A novel C-type lectin is involved in the innate immunity of Macrobrachium nipponense. Fish & Shellfish Immunology, 50: 117-126.
Xiu Y J, Wang Y H, Jing Y T, Qi Y K, Ding Z F, Meng Q G, Wang W. 2015b. Molecular cloning, characterization, and expression analysis of two different types of lectins from the oriental river prawn, Macrobrachium nipponense. Fish & Shellfish Immunology, 45(2): 465-469.
Xiu Y J, Wu T, Du J, Yao W, Li W J, Ding Z F, Ren Q, Gu W, Meng Q G, Wang W. 2013. Molecular characterization and expression analysis of extracellular copper/zinc superoxide dismutase (ecCuZnSOD) from oriental river prawn, Macrobrachium nipponense. Aquaculture, 380-383: 23-28.
Xu Z X, Li T Y, Li E C, Chen K, Ding Z L, Qin J G, Chen L Q, Ye J Y. 2016. Comparative transcriptome analysis reveals molecular strategies of oriental river prawn Macrobrachium nipponense in response to acute and chronic nitrite stress. Fish & Shellfish Immunology, 48: 254-265.
Yao C L, Wang A L, Wang W N, Sun R Y. 2004. Purification and partial characterization of Mn superoxide dismutase from muscle tissue of the shrimp Macrobrachium nipponense. Aquaculture, 241(1-4): 621-631.
Yu X Q, Gan H, Kanost M R. 1999. Immulectin, an inducible C-type lectin from an insect, Manduca sexta, stimulates activation of plasma prophenol oxidase. Insect Biochemistry and Molecular Biology, 29(7): 585-597.
Zhang R, Cho H Y, Kim H S, Ma Y G, Osaki T, Kawabata S I, Söderhäll K, Lee B L. 2003. Characterization and properties of a 1, 3-β-d-glucan pattern recognition protein of Tenebrio molitor larvae that is specifically degraded by serine protease during Prophenoloxidase activation. Journal of Biological Chemistry, 278(43): 42 072-42 079.
Zhang X M, Cui W Y, Ding S Q, Li W M, Zhang Q H. 2017. Isolation, identification and antibiotic sensitivity of Aeromonas veronii from Litopenaeus vannamei. Microbiology China, 44(12): 2 795-2 804. (in Chinese with English abstract)
Zhang X W, Xu W T, Wang X W, Mu Y, Zhao X F, Yu X Q, Wang J X. 2009. A novel C-type lectin with two CRD domains from Chinese shrimp Fenneropenaeus chinensis functions as a pattern recognition protein. Molecular Immunology, 46(8-9): 1 626-1 637.
Zhao X L, Duan X M, Wang Z H, Zhang W W, Li Y, Jin C H, Xiong J B, Li C H. 2017. Comparative transcriptome analysis of Sinonovacula constricta in gills and hepatopancreas in response to Vibrio parahaemolyticus infection. Fish & Shellfish Immunology, 67: 523-535.