Anti‐Lipopolysaccharide Factor from Banana Shrimp (Fenneropenaeus merguiensis) Exhibits Antibacterial Activity
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Abstract
Anti-lipopolysaccharide factor (ALF) is a type of antimicrobial peptide that plays an important role in the innate immune system of crustaceans such as shrimps and crabs. In the present study, anti-lipopolysaccharide factor isoform 3 (ALF3) was identified and characterized from banana shrimp (Fenneropenaeus merguiensis) named as FmALF3. The full-length cDNA of FmALF3 was 643 bp. The open reading frame of FmALF3 was 372 bp and encoded a polypeptide of 123 amino acids with a signal peptide of 25 amino acid residues. Its calculated molecular mass is 13.67 kDa with an isoelectric point of 9.88. FmALF3 is a cationic ALF, that consists of lipopolysaccharide-binding domain and two highly conserved cysteine residues at position 55 and 76. It shared 96.7% similarity with FiALF-B from F. indicus. The mRNA transcript of FmALF3 was detected in all examined tissues with the highest expression in hemocytes. The temporal expression of FmALF3 mRNA in hemocytes after Vibrio parahaemolyticus injection was analyzed by quantitative real-time PCR (qRT-PCR). FmALF3 was up regulated at 3 h and reached the highest level at 12 h. After that, the expression level of FmALF3 was decreased at 24, 48 and 72 h. The recombinant of FmALF3 (rFmALF3) was expressed in Escherichia coli BL21*(DE3) and purified. The purified rFmALF3 could inhibit the growth of Gram-positive and Gram-negative bacteria. Therefore, all these results indicated that FmALF3 is an inducible protein and could play a key biological role in the innate immune defense of F. mergueinsis.
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References
Antony, S.P., I.S.B. Singh, R.M. Jose, P. Kumar and R. Philip. 2011. Antimicrobial peptide gene expression in tiger shrimp, Penaeus monodon in response to gram-positive bacterial probionts and white spot virus challenge. Aquaculture 316: 6–12.
Arockiaraj, J., V. Kumaresan, P. Bhatt, R. Palanisamy, A.J. Gnanam, M. Pasupuleti, M. Kasi and M.K. Chaurasia. 2014. A novel single-domain peptide, anti-LPS factor from prawn: Synthesis of peptide, antimicrobial properties and complete molecular characterization. Peptides 53: 79–88.
Chimnuala, J., W. Potiyanadecha, J. Saetanb and W. Chotigeat. 2022. Primordial germ cell migration in banana shrimp: Fenneropenaeus merguiensis. Agriculture and Natural Resources 56(3): 497–502.
Chungjit, A., S. Wuthisuthimethavee, S. Poompuang and S. Tunkijjanukij. 2016. Gene expression profiles in giant freshwater prawn Macrobrachium rosenbergi infected with Macrobrachium rosenbergi Nodavirus (MrNV) by DD-PCR technique. Kasetsart University Fisheries Research Bulletin 40(2): 39–50.
Destoumieux-Garzón, D., R.D. Rosa, P. Schmitt, C. Barreto, J. Vidal-Dupiol, G. Mitta, Y. Gueguen and E. Bachère. 2016. Antimicrobial peptides in marine invertebrate health and disease. Philosophical Transactions of the Royal Society B 371: 20150300. DOI: 10.1098/rstb.2015.0300.
Elshikh, M., S. Ahmed, S. Funston, P. Dunlop, M. McGaw, R. Marchant and I.M. Banat. 2016. Resazurin-based 96-well plate microdilution method for the determination of minimum inhibitory concentration of biosurfactants. Biotechnology Letters 38(6): 1015–1019.
Guaní-Guerra, E., T. Santos-Mendoza, S.O. Lugo-Reyes and L.M. Terán. 2010. Antimicrobial peptides: General overview and clinical implications in human health and disease. Clinical Immunology 135(1): 1–11.
Guo, S., S. Li, F. Li, X. Zhang and J. Xiang. 2014. Modification of a synthetic LPS-binding domain of anti-lipopolysaccharide factor from shrimp reveals strong structure-activity relationship in their antimicrobial characteristics. Developmental and Comparative Immunology 45(2): 227–232.
Hoffmann, J.A., F.C. Kafatos, C.A. Janeway and R.A.B. Ezekowitz. 1999. Phylogenetic perspectives in innate immunity. Science 284: 1313–1318.
Jaree, P., A. Tassanakajon and K. Somboonwiwat. 2012. Effect of the anti-lipopolysaccharide factor isoform 3 (ALFPm3) from Penaeus monodon on Vibrio harveyi cells. Developmental and Comparative Immunology 38(4): 554–560.
Jiang, H.S., Q. Zhang, Y.R. Zhao, W.M. Jia, X.F. Zhao and J.X. Wang. 2015. A new group of anti-lipopolysaccharide factors from Marsupenaeus japonicus functions in antibacterial response. Developmental and Comparative Immunology 48(1): 33–42.
Johansson, M.W., P. Keyser, K. Sritunyalucksana and K. Söderhäll. 2000. Crustacean haemocytes and haematopoiesis. Aquaculture 191: 45–52.
Kamysz, W., M. Okrój and J. Lukasiak. 2003. Novel properties of antimicrobial peptides. Acta Biochimica Polonica 50(2): 461–469.
Kumar, S., G. Stecher and K. Tamura. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7): 1870–1874.
Laemmli, U.K. 1970. Cleavage of structure protein during assembly of head of bacteriophage T4. Nature 227: 680–685.
Li, S., S. Guo, F. Li and J. Xiang. 2015. Functional diversity of anti-lipopolysaccharide factor isoforms in shrimp and their characters related to antiviral activity. Marine Drugs 13(5): 2602–2616.
Lightner, D.V., R.M. Redman, C.R. Pantoja, B.L. Noble and L. Tran. 2012. Early mortality syndrome affects shrimp in Asia. Global Aquaculture Advocate 15: 40.
Liu, F., Y. Liu, F. Li, B. Dong and J. Xiang. 2005. Molecular cloning and expression profile of putative antilipopolysaccharide factor in Chinese shrimp (Fenneropenaeus chinensis). Marine Biotechnology 7(6): 600–608.
Liu, Y., Z. Cui, X. Li, C. Song and G. Shi. 2013. A newly identified anti-lipopolysaccharide factor from the swimming crab Portunus trituberculatus with broad spectrum antimicrobial activity. Fish and Shellfish Immunology 34(2): 463–470.
Long, S., F. Chen and K.J. Wang. 2021. Characterization of a new homologous anti-lipopolysaccharide factor SpALF7 in mud crab Scylla paramamosain. Aquaculture 534: 736333. DOI: 10.1016/j.aquaculture.2020.736333.
Matos, G.M., P. Schmitt, C. Barreto, N.D. Farias, G. Toledo-Silva, F. Guzmán, D. Destoumieux-Garzón, L.M. Perazzolo and R.D. Rosa. 2018. massive gene expansion and sequence diversification is associated with diverse tissue distribution, regulation and antimicrobial properties of anti-lipopolysaccharide factors in shrimp. Marine Drugs 16(10): 381. DOI: 10.3390/md16100381.
Methatham, T., P. Boonchuen, P. Jaree, A. Tassanakajon and K. Somboonwiwat. 2017. Antiviral action of the antimicrobial peptide ALFPm3 from Penaeus monodon against white spot syndrome virus. Developmental and Comparative Immunology 69: 23–32.
Morita, T., S. Ohtsubo, T. Nakamura, S. Tanaka, S. Iwanaga, K. Ohashi and M. Niwa. 1985. Isolation and biological activities of limulus anticoagulant (Anti-LPS Factor) which interacts with lipopolysaccharide (LPS). Journal of Biochemistry 97(6): 1611–1620.
Petersen, T.N., S. Brunak, G. von Heijne and H. Nielsen. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8(10): 785–786.
Ponprateep, S., K. Somboonwiwat and A. Tassanakajon. 2009. Recombinant anti-lipopolysaccharide factor isoform 3 and the prevention of vibriosis in the black tiger shrimp, Penaeus monodon. Aquaculture 289(3–4): 219–224.
Rosa, R.D. and M.A. Barracco. 2010. Antimicrobial peptides in crustaceans. Invertebrate Survival Journal 7(2): 262–284.
Somboonwiwat, K., M. Marcos, A. Tassanakajon, S. Klinbunga, A. Aumelas, B. Romestand, Y. Gueguen, H. Boze, G. Moulin and E. Bachère. 2005. Recombinant expression and anti-microbial activity of anti-lipopolysaccharide factor (ALF) from the black tiger shrimp Penaeus monodon. Developmental and Comparative Immunology 29(10): 841–851.
Somboonwiwat, K., E. Bachère, V. Rimphanitchayakit and A. Tassanakajon. 2008. Localization of anti-lipopolysaccharide factor (ALFPm3) in tissues of the black tiger shrimp, Penaeus monodon, and characterization of its binding properties. Developmental and Comparative Immunology 32(10): 1170–1176.
Srisapoome, P., N. Klongklaew, N. Areechon and R. Wongpanya. 2018. Molecular and functional analyses of novel anti-lipopolysaccharide factors in giant river prawn (Macrobrachium rosenbergii, De Man) and their expression responses under pathogen and temperature exposure. Fish and Shellfish Immunology 80: 357–375.
Supungul, P., S. Klinbunga, R. Pichyangkura, S. Jitrapakdee, I. Hirono, T. Aoki and A. Tassanakajon. 2002. Identification of immune-related genes in hemocytes of black tiger shrimp (Penaeus monodon). Marine Biotechnology 4(5): 487–494.
Supungul, P., P. Jaree, K. Somboonwiwat, W. Junprung, P. Proespraiwong, R. Mavichak and A. Tassanakajon. 2017. A potential application of shrimp antilipopolysaccharide factor in disease control in aquaculture. Aquaculture Research 48: 809–821.
Suraprasit, S., T. Methatham, P. Jaree, K. Phiwsaiya, S. Senapin, I. Hirono, C.F. Lo, A. Tassanakajon and K. Somboonwiwat. 2014. Anti-lipopolysaccharide factor isoform 3 from Penaeus monodon (ALFPm3) exhibits antiviral activity by interacting with WSSV structural proteins. Antiviral Research 110: 142–150.
Tanaka, S., T. Nakamura, T. Morita and S. Iwanaga. 1982. Limulus anti-LPS factor: An anticoagulant which inhibits the endotoxin-mediated activation of coagulation system. Biochemical and Biophysical Research Communications 105(2): 717–723.
Tang, T., J. Liu, S. Li, H. Li and F. Liu. 2020. Recombinant expression of an oriental river prawn anti-lipopolysaccharide factor gene in Pichia pastoris and its characteristic analysis. Fish and Shellfish Immunology 98: 414–419.
Tassanakajon, A., K. Somboonwiwat, P. Supungul and S. Tang. 2013. Discovery of immune molecules and their crucial functions in shrimp immunity. Fish and Shellfish Immunology 34(4): 954–967.
Tassanakajon, A., V. Rimphanitchayakit, S. Visetnan, P. Amparyup, K. Somboonwiwat, W. Charoensapsri and S. Tang. 2018. Shrimp humoral responses against pathogens: antimicrobial peptides and melanization. Developmental and Comparative Immunology 80: 81–93.
Tharntada, S., S. Ponprateep, K. Somboonwiwat, H. Liu, I. Söderhäll, K. Söderhäll and A. Tassanakajon. 2009. Role of anti-lipopolysaccharide factor from the black tiger shrimp, Penaeus monodon, in protection from white spot syndrome virus infection. Journal of General Virology 90(6): 1491–1498.
Tinwongger, S., J. Thawonsuwan, H. Kondo and I. Hirono. 2019. Identification of an anti-lipopolysaccharide factor AV-R isoform (LvALF AV-R) related to Vp_PirAB-like toxin resistance in Litopenaeus vannamei. Fish and Shellfish Immunology 84: 178–188.
Vazquez, L., J. Alpuche, G. Maldonado, C. Agundis, A. Pereyra-Morales and E. Zenteno. 2009. Review: Immunity mechanisms in crustaceans. Innate Immunity 15(3): 179–188.
Wu, X., Y. Huang, Z. Yu, C. Mu, W. Song, R. Li, L. Liu, Y. Ye, C. Shi and C. Wang. 2019. An MBT domain containing anti-lipopolysaccharide factor (PtALF8) from Portunus trituberculatus is involved in immune response to bacterial challenge. Fish and Shellfish Immunology 84: 252–258.
Yang, H., S. Li, F. Li, X. Lv and J. Xiang. 2015. Recombinant expression and functional analysis of an isoform of anti-lipopolysaccharide factors (FcALF5) from Chinese shrimp Fenneropenaeus chinensis. Developmental and Comparative Immunology 53(1): 47–54.
Yin, C.M., X.Y. Pan, X.T. Cao, T. Li, Y.H. Zhang and J.F. Lan. 2021. A crayfish ALF inhibits the proliferation of microbiota by binding to RPS4 and MscL of E. coli. Developmental and Comparative Immunology 121: 104106. DOI: 10.1016/j.dci.2021.104106.
Zhan, W., X. Tang, X. Wang, L. He and X. Wei. 2015. An anti-lipopolysaccharide factor in Litopenaeus vannamei participates in the immune defense against WSSV and Vibrio anguillarum. Journal of Crustacean Biology 35(5): 670–675.
Zhang, H., W. Cheng, L. Zheng, P. Wang, Q. Liu, Z. Li, T. Li, Y. Wei, Y. Mao and X. Yu. 2020. Identification of a group D anti-lipopolysaccharide factor (ALF) from kuruma prawn (Marsupenaeus japonicus) with antibacterial activity against Vibrio parahaemolyticus. Fish and Shellfish Immunology 102: 368–380.
Zhang, H., J. Zheng, W. Cheng, Y. Mao and X. Yu. 2022. Antibacterial activity of an anti-lipopolysaccharide factor (MjALF-D) identified from kuruma prawn (Marsupenaeus japonicus). Fish and Shellfish Immunology 127: 295–305.
Zhou, L., G. Li, A. Li, Y. Jiao, S. Li, J. Huang, L. Yang and C. Wang. 2019a. Characterization of a group D anti-lipopolysaccharide factor (ALF) involved in anti-Vibrio response in Penaeus monodon. Fish and Shellfish Immunology 89: 384–392.
Zhou, L., G. Li, Y. Jiao, D. Huang, A. Li, H. Chen, Y. Liu, S. Li, H. Li and C. Wang. 2019b. Molecular and antimicrobial characterization of a group G anti-lipopolysaccharide factor (ALF) from Penaeus monodon. Fish and Shellfish Immunology 94: 149–156.
Zorriehzahra, M.J. and R. Banaederakhshan. 2015. Early Mortality Syndrome (EMS) as new Emerging Threat in Shrimp Industry. Advances in Animal and Veterinary Sciences 3(2): 64–72.