Skip to main content
SpringerLink
Log in

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

  • Aquaculture and Fisheries
  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Data Availability Statement

All the raw data of nine sequencing libraries have been submitted to NCBI Sequence Read Archive with accession numbers SRR7665577, SRR7665578, SRR7665579, SRR7665580, SRR7665581, SRR7665582, SRR7665583, SRR7665584, and SRR7665585.

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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Cai Y X, Ng P K L. 2002. The freshwater palaemonid prawns (Crustacea: decapoda: caridea) of Myanmar. Hydrobiologia, 487(1): 59–83.

    Article  Google Scholar 

  • Cai Y, Dai A Y. 1999. Freshwater shrimps (Crustacea: decapoda: caridea) from the Xishuangbanna region of Yunnan Province, southern China. Hydrobiologia, 400: 211–241.

    Article  Google Scholar 

  • Cambi A, Figdor C G. 2005. Levels of complexity in pathogen recognition by C-type lectins. Current Opinion in Immunology, 17(4): 345–351.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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)

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Garzoni C, Kelley W L. 2009. Staphylococcus aureus: new evidence for intracellular persistence. Trends in Microbiology, 17(2): 59–65.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hoffmann J A. 2003. The immune response of Drosophila. Nature, 426(6962): 33–38.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Janda J M, Abbott S L. 2010. The genus Aeromonas: taxonomy, pathogenicity, and infection. Clinical Microbiology Reviews, 23(1): 35–73.

    Article  Google Scholar 

  • Jang I H, Nam H J, Lee W J. 2008. CLIP-domain serine proteases in Drosophila innate immunity. BMB Reports, 41(2): 102–107.

    Article  Google Scholar 

  • 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)

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Langmead B, Salzberg S L. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4): 357–359.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Otto M. 2014. Staphylococcus aureus toxins. Current Opinion in Microbiology, 17: 32–37.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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)

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  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

    Chong Han, Zhipeng Zhang & Jianrong Huang

  2. Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, 519082, China

    Jianrong Huang

  3. School of life Sciences, Guangzhou University, Guangzhou, 510006, China

    Qiang Li

  4. South China Institute of Environmental Science, MEE, Guangzhou, 510610, China

    Qinghua Chen

Authors
  1. Chong Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhipeng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qinghua Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jianrong Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jianrong Huang.

Additional information

Supported by the Research on the Diversity of Freshwater Fish, Shrimp and Crab in Macau (No. 20183300042411016) and the Guangdong Special Environmental Fund (Nos. PM-zx555-202107-208, PM-zx555-202106-195)

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, C., Zhang, Z., Li, Q. et al. Comparative transcriptomic analysis of Macrobrachium nipponense in response to Aeromonas veronii or Staphylococcus aureus infection. J. Ocean. Limnol. 40, 347–359 (2022). https://doi.org/10.1007/s00343-021-0364-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-021-0364-y

Keyword

Search

Navigation