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| Function of Crustin Gene in Regulation of Intestinal Microbiota Homeostasis in Ridgetail White Prawn Exopalaemon carinicauda |
| XU Kai1,2, LIU Dexue1,2, CHENG Weitao1, HAN Wanyu1,2, WANG Chao1,2, WANG Weili1,2, YAN Peiwen1, LU Xiao1, HU Guangwei1,2, YAN Binlun1,2, GAO Huan1,2 |
1. Jiangsu Key Laboratory of Marine Bioresources and Environment/Jiangsu Key Laboratory of Marine Biotechnology, School of Marine Science and Fisheries, Jiangsu Ocean University, Lianyungang 222005, China;
2. Co-Innovation Center of Jiangsu Marine Bio-industry Technology, Jiangsu Ocean University, Lianyungang 222005, China |
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Abstract In order to investigate the function of crustin in regulation of intestinal microbiota homeostasis in ridgetail white prawn Exopalaemon carinicauda, the intestinal microbiota characteristics were investigated in the ridgetail white prawn with body length of (5.47±0.31) cm with 16S rRNA sequencing technology. The results showed that there was significant change in composition of intestinal microflora in the ridgetail white prawn exposed to EcCrustin2 gene knockdown, without significant difference in α-diversity between the control and siEcCrustin2 gene groups. Proteobacteria, Tenericutes and Firmicutes were found to be the dominant phyla in the intestinal microbiota in the ridgetail white prawn exposed to EcCrustin2 gene knockdown at the phylum level. The relative abundance of Proteobacteria was increased in siEcCrustin2 group, and those in Tenericutes and Firmicutes were decreased. Photobacterium and Vibrio were the dominant bacterial genera in the intestinal microbiota of E. carinicauda group at the genus level, with significant decrease in relative abundance of Photobacterium, and the significant increase in abundance of Vibrio in siEcCrustin2 group. Photobacterium damselae subsp. damselae was shown to be the dominant species, with significantly elevated abundance after EcCrusin2 gene knockdown at the species level. Functional prediction by Tax4Fun revealed that intestinal microbiota were involved in carbohydrate metabolism, lipid metabolism, infectious diseases, cell motility and membrane transport more apparently in the RNAi group than those in control group. There was close relationship between the EcCrustin2 and the intestinal microflora in E. carinicauda group. The findings will contribute to comprehensive understanding of the composition and plasticity of the shrimp microbiota, which will provide innovative strategies for promoting the development of aquaculture industry.
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Received: 29 August 2023
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[1] SCHNAPP D, KEMP G D, SMITH V J. Purification and characterization of a proline-rich antibacterial peptide, with sequence similarity to bactenecin-7, from the haemocytes of the shore crab, Carcinus maenas[J]. European Journal of Biochemistry,1996,240(3):532-539.
[2] RELF J M, CHISHOLM J R, KEMP G D, et al. Purification and characterization of a cysteine-rich 11.5-kDa antibacterial protein from the granular haemocytes of the shore crab, Carcinus maenas[J]. European Journal of Biochemistry,1999,264(2):350-357.
[3] BARTLETT T C, CUTHBERTSON B J, SHEPARD E F, et al. Crustins, homologues of an 11.5-kDa antibacterial peptide, from two species of penaeid shrimp, Litopenaeus vannamei and Litopenaeus setiferus[J]. Marine Biotechnology,2002,4(3):278-293.
[4] DONPUDSA S, VISETNAN S, SUPUNGUL P, et al. Type Ⅰ and type Ⅱ crustins from Penaeus monodon, genetic variation and antimicrobial activity of the most abundant crustinPm4[J]. Developmental & Comparative Immunology,2014,47(1):95-103.
[5] HAUTON C, BROCKTON V, SMITH V J. Cloning of a crustin-like, single whey-acidic-domain, antibacterial peptide from the haemocytes of the European lobster, Homarus gammarus, and its response to infection with bacteria[J]. Molecular Immunology,2006,43(9):1490-1496.
[6] TINCU J A, TAYLOR S W. Antimicrobial peptides from marine invertebrates[J]. Antimicrobial Agents and Chemotherapy,2004,48(10):3645-3654.
[7] FELDHAAR H, GROSS R. Immune reactions of insects on bacterial pathogens and mutualists[J]. Microbes and Infection,2008,10(9):1082-1088.
[8] FJELL C D, HISS J A, HANCOCK R E W, et al. Designing antimicrobial peptides:form follows function[J]. Nature Reviews. Drug Discovery,2011,11(1):37-51.
[9] LIU N, LAN J F, SUN J J, et al. A novel crustin from Marsupenaeus japonicus promotes hemocyte phagocytosis[J]. Developmental & Comparative Immunology,2015,49(2):313-322.
[10] BAO M N, LIANG Y, LANG L, et al. A novel type II crustin in the innate immune response of the freshwater crab (Sinopotamon henanense) against infection and its expression changes by cadmium[J]. Fish & Shellfish Immunology,2023,134:108559.
[11] LV X J, LI S H, YU Y, et al. The immune function of a novel crustin with an atypical WAP domain in regulating intestinal microbiota homeostasis in Litopenaeus vannamei[J]. Developmental & Comparative Immunology,2020,111:103756.
[12] QIAO F, LIU Y K, SUN Y H, et al. Influence of different dietary carbohydrate sources on the growth and intestinal microbiota of Litopenaeus vannamei at low salinity[J]. Aquaculture Nutrition,2017,23(3):444-452.
[13] SALZMAN N H, HUNG K, HARIBHAI D, et al. Enteric defensins are essential regulators of intestinal microbial ecology[J]. Nature Immunology,2010,11(1):76-83.
[14] 王兴强,阎斌伦,马甡,等.脊尾白虾生物学及养殖生态学研究进展[J].齐鲁渔业,2005,22(8):21-23.
[15] 梁俊平,李健,刘萍,等.脊尾白虾生物学特性与人工繁育的研究进展[J].中国农学通报,2012,28(17):109-116.
[16] XU K, WANG W L, LIU D, et al. Characterization of a crustin-like peptide involved in shrimp immune response to bacteria and Enterocytozoon hepatopenaei (EHP) infection in Palaemon carinicauda[J]. Fish & Shellfish Immunology,2023,139:108871.
[17] MA H K, GAO H, XU W Y, et al. Cloning and functional study of fatty acid-binding protein-like gene of the ridgetail white prawn, Exopalaemon carinicauda[J]. Aquaculture International,2020,28(4):1517-1530.
[18] CHEN S F, ZHOU Y Q, CHEN Y R, et al. Fastp:an ultra-fast all-in-one FASTQ preprocessor[J]. Bioinformatics,2018,34(17):i884-i890.
[19] EDGAR R C. UPARSE:highly accurate OTU sequences from microbial amplicon reads[J]. Nature Methods,2013,10(10):996-998.
[20] NILSSON R H, LARSSON K H, TAYLOR A F S, et al. The UNITE database for molecular identification of fungi:handling dark taxa and parallel taxonomic classifications[J]. Nucleic Acids Research,2019,47(D1):D259-D264.
[21] CAPORASO J G, KUCZYNSKI J, STOMBAUGH J, et al. QIIME allows analysis of high-throughput community sequencing data[J]. Nature Methods,2010,7(5):335-336.
[22] EDGAR R C. MUSCLE:multiple sequence alignment with high accuracy and high throughput[J]. Nucleic Acids Research, 2004,32(5):1792-1797.
[23] PRICE M N,DEHAL P S, ARKIN A P. FastTree 2—approximately maximum-likelihood trees for large alignments[J]. PLoS One,2010,5(3):e9490.
[24] OKSANEN J, BLANCHET F, KINDT R, et al. Vegan:community Ecology Package. R package version 1.17-8.2011[EB/OL]. (2021)[2024-03-01]. http://CRAN.R-project.org/package=vegan.
[25] AßHAUER K P, WEMHEUER B, DANIEL R, et al. Tax4Fun:predicting functional profiles from metagenomic 16S rRNA data[J]. Bioinformatics,2015,31(17):2882-2884.
[26] DUERKOP B A, VAISHNAVA S, HOOPER L V. Immune responses to the microbiota at the intestinal mucosal surface[J]. Immunity,2009,31(3):368-376.
[27] LEGRAND T P R A, WYNNE J W, WEYRICH L S, et al. A microbial sea of possibilities:current knowledge and prospects for an improved understanding of the fish microbiome[J]. Reviews in Aquaculture,2020,12(2):1101-1134.
[28] 金若晨,江敏,孙世玉,等.凡纳滨对虾养殖环境及肠道微生物群落特征分析[J].水产学报,2020,44(12):2037-2054.
[29] CHANG J Y,ANTONOPOULOS D A, KALRA A, et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile—associated diarrhea[J]. The Journal of Infectious Diseases,2008,197(3):435-438.
[30] MARCHESI J R, ADAMS D H, FAVA F, et al. The gut microbiota and host health:a new clinical frontier[J]. Gut,2016,65(2):330-339.
[31] ZHENG L, XIE S W, ZHUANG Z X, et al. Effects of yeast and yeast extract on growth performance, antioxidant ability and intestinal microbiota of juvenile Pacific white shrimp (Litopenaeus vannamei)[J]. Aquaculture,2021,530:735941.
[32] RIVAS A J, LEMOS M L, OSORIO C R. Photobacterium damselae subsp. damselae, a bacterium pathogenic for marine animals and humans[J]. Frontiers in Microbiology,2013,4:283.
[33] XING C F, HU H H, HUANG J B, et al. Diet supplementation of Pediococcus pentosaceus in cobia (Rachycentron canadum) enhances growth rate, respiratory burst and resistance against photobacteriosis[J]. Fish & Shellfish Immunology,2013,35(4):1122-1128.
[34] PELLIZZARI C, KRASNOV A, AFANASYEV S, et al. High mortality of juvenile gilthead sea bream (Sparus aurata) from photobacteriosis is associated with alternative macrophage activation and anti-inflammatory response:results of gene expression profiling of early responses in the head kidney[J]. Fish & Shellfish Immunology,2013,34(5):1269-1278.
[35] LIU F, LIU G X, LI F H. Characterization of two pathogenic Photobacterium strains isolated from Exopalaemon carinicauda causing mortality of shrimp[J]. Aquaculture,2016,464:129-135.
[36] ZHANG Z, YU Y X, WANG K, et al. First report of skin ulceration caused by Photobacterium damselae subsp. damselae in net-cage cultured black rockfish (Sebastes schlegeli)[J]. Aquaculture,2019,503:1-7.
[37] OSORIO C R. Horizontal Gene Transfer: Breaking Borders Between Living Kingdoms [M]. Cham:Springer, 2019:175-199.
[38] GOUIFE M, CHEN S Y, HUANG K J, et al. Photobacterium damselae subsp. damselae in mariculture[J]. Aquaculture International,2022,30(3):1453-1480.
[39] RAY A K, GHOSH K, RINGØ E. Enzyme-producing bacteria isolated from fish gut:a review[J]. Aquaculture Nutrition,2012,18(5):465-492.
[40] XUE H B, WU X J, LI Z H, et al. Correlation and causation between the intestinal microbiome and male morphotypes in the giant freshwater prawn Macrobrachium rosenbergii[J]. Aquaculture,2021,531:735936.
[41] YANG G M, BAO B L, PEATMAN E, et al. Analysis of the composition of the bacterial community in puffer fish Takifugu obscurus[J]. Aquaculture,2007,262(2/3/4):183-191.
[42] FRAUNE S, ZIMMER M. Host-specificity of environmentally transmitted Mycoplasma-like isopod symbionts[J]. Environmental Microbiology, 2008,10(10):2497-2504.
[43] PAN X H, LIU Q, WEN L T, et al. RETRACTED:improving tilapia (Oreochromis mossambicus) resistance to streptococcal disease by improving the gut biome through administration of the microorganisms Bacillus subtilis and Enterococcus faecalis[J]. Aquaculture Reports,2021,20:100636.
[44] 段健诚,胡吉卉,沈宇航,等. 虾肝肠胞虫感染对脊尾白虾肠道菌群的影响[J].渔业科学进展,2022,43(3):75-83.
[45] XUE M Y, JIANG N, FAN Y D, et al. White spot syndrome virus (WSSV) infection alters gut histopathology and microbiota composition in crayfish (Procambarus clarkii)[J]. Aquaculture Reports,2022,22:101006. |
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