Early infection with white spot syndrome virus promotes changes in the gut microbiome and immune-energy related genes of shrimps Litopenaeus vannamei (Boone, 1931)
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Abstract
The white spot syndrome virus (WSSV) is currently the main threat to the shrimp industry due to significant economic losses associated with shrimp mortality. The first hours of host-parasite interactions are crucial for the fate of WSSV infection, which becomes irreversible after 72 h. During this critical period, there is still a limited understanding of the interaction between the gut microbiota and the host response. In this study, we evaluated the effect of WSSV on the Pacific white shrimp Litopenaeus vannamaei (Boone, 1931) at the gut microbiome level and the expression of four genes in hemocytes and hepatopancreas associated with aerobic (ATP synthase) and anaerobic (LDH) metabolism, cell pathogen internalization (AP-2), and immune response (α2M). The genes LDH and α2M were overexpressed in hemocytes and hepatopancreas, while the AP-2 gene was overexpressed only in hemocytes. In infected shrimps, we observed a positive correlation between the increase in viral load (VL), the upregulation of the genes LDH and AP-2, and the augmentation of the relative abundance of Ideonella, Actinobacter, Flavobacterium, Caldalkalibacillus, Gemmobacter, Pirellula, Metilophylus, Hydrogenophaga, Pseudomona, Methylophaga, Candidatus Bacilloplasma, and Novosphingobium. Whereas the gut microbiome in uninfected shrimps was represented by Motilimonas, Tamlana, Shimia, Spongiimonas, Pseudoalteromonas, Aeromones, and Shewanella. Results from this study contribute to understanding the intricate interplay between WSSV infection, the host response, and gut microbiota in aquaculture settings.
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Stentiford GD, Oidtmann B, Scott A, Peeler EJ. Crustacean diseases in European legislation: Implications for importing and exporting nations. Aquaculture. 2010;306(1−4):27–34. doi: 10.1016/j.aquaculture.2010.06.004.
Asche F, Anderson JL, Botta R, Kumar G, Abrahamsen EB, Nguyen LT, et al. The economics of shrimp disease. Journal of Invertebrate Pathology. 2021;186:107397. doi: 10.1016/j.jip.2020.107397.
Zhang Y, Song L, Zhao J, Wang L, Kong P, Liu L, et al. Protective immunity induced by CpG ODNs against white spot syndrome virus (WSSV) via intermediation of virus replication indirectly in Litopenaeus vannamei. Developmental & Comparative Immunology. 2010;34(4):418–424. doi: 10.1016/j.dci.2009.11.012.
Jiravanichpaisal P, Söderhäll K, Söderhäll I. Characterization of white spot syndrome virus replication in in vitro-cultured haematopoietic stem cells of freshwater crayfish, Pacifastacus leniusculus. Journal of General Virology. 2006;87(4):847–854. doi: 10.1099/vir.0.81758-0.
Mayor S, Presley JF, Maxfield FR. Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process. The Journal of Cell Biology. 1993;121(6):1257–1269. doi: 10.1083/jcb.121.6.1257.
McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nature Reviews Molecular Cell Biology. 2011;12(8):517–533. doi: 10.1038/nrm3151.
Aguilar RC, Ohno H, Roche KW, Bonifacino JS. Functional domain mapping of the clathrin-associated adaptor medium chains 1 and 2. Journal of Biological Chemistry. 1997;272(43):27160–27166. doi: 10.1074/jbc.272.43.27160.
Rapoport I, Chen YC, Cupers P, Shoelson SE, Kirchhausen T. Dileucine-based sorting signals bind to the beta chain of AP-1 at a site distinct and regulated differently from the tyrosine-based motif-binding site. The EMBO Journal 1998;17(8):2148–2155. doi: 10.1093/emboj/17.8.2148.
Mousavi SA, Malerød L, Berg T, Kjeken R. Clathrin-dependent endocytosis. Biochemical Journal. 2004;377(1):1–16. doi: 10.1042/bj20031000.
Kobiler O, Drayman N, Butin-Israeli V, Oppenheim A. Virus strategies for passing the nuclear envelope barrier. Nucleus. 2012;3(6):526–539. doi: 10.4161/nucl.21979.
Sánchez-Paz A. White spot syndrome virus: an overview on an emergent concern. Veterinary Research. 2010;41(6):43. doi: 10.1051/vetres/2010015.
Huang X, Madan A. CAP3: a DNA sequence assembly program. Genome Research. 1999;9(9):868–877. doi: 10.1101/gr.9.9.868.
Wongpanya R, Aoki T, Hirono I, Yasuike M, Tassanakajon A. Analysis of gene expression in haemocytes of shrimp Penaeus monodon challenged with white spot syndrome virus by cDNA microarray. Science Asia. 2007;33:165–174. doi: 10.2306/scienceasia1513-1874.2007.33.165.
Wang X-F, Liu Q-H, Wu Y, Huang J. Litopenaeus vannamei clathrin coat AP17 involved in white spot syndrome virus infection. Fish & Shellfish Immunology. 2016;52:309–316. doi: 10.1016/j.fsi.2016.03.007.
Hernández-Pérez A, Zamora-Briseño JA, Ruiz-May E, Pereira-Santana A, Elizalde-Contreras JM, Pozos-González S, et al. Proteomic profiling of the white shrimp Litopenaeus vannamei (Boone, 1931) hemocytes infected with white spot syndrome virus reveals the induction of allergy-related proteins. Developmental & Comparative Immunology. 2019;91:37–49. doi: 10.1016/j.dci.2018.10.002.
Diamantino TC, Almeida E, Soares AMVM, Guilhermino L. Lactate dehydrogenase activity as an effect criterion in toxicity tests with Daphnia magna straus. Chemosphere. 2001;45(4−5):553−560. doi: 10.1016/s0045-6535(01)00029-7.
Soñanez-Organis JG, Rodriguez-Armenta M, Leal-Rubio B, Peregrino-Uriarte AB, Gómez-Jiménez S, Yepiz-Plascencia G. Alternative splicing generates two lactate dehydrogenase subunits differentially expressed during hypoxia via HIF-1 in the shrimp Litopenaeus vannamei. Biochimie. 2012;94(5):1250−1260. doi: 10.1016/j.biochi.2012.02.015.
Hernández-Palomares MLE, Godoy-Lugo JA, Gómez-Jiménez S, Gámez-Alejo LA, Ortiz RM, Muñoz-Valle JF, et al. Regulation of lactate dehydrogenase in response to WSSV infection in the shrimp Litopenaeus vannamei. Fish & Shellfish Immunology. 2018;74:401−409. doi: 10.1016/j.fsi.2018.01.011.
Lin X, Kim Y-A, Lee BL, Söderhäll K, Söderhäll I. Identification and properties of a receptor for the invertebrate cytokine astakine, involved in hematopoiesis. Experimental Cell Research. 2009;315(7):1171−1180. doi: 10.1016/j.yexcr.2009.01.001.
Liang Y, Xu M-L, Wang X-W, Gao X-X, Cheng J-J, Li C, et al. ATP synthesis is active on the cell surface of the shrimp Litopenaeus vannamei and is suppressed by WSSV infection. Virology Journal. 2015;12(1):49. doi: 10.1186/s12985-015-0275-7.
Armstrong PB, Quigley JP. α 2 -macroglobulin: an evolutionarily conserved arm of the innate immune system. Developmental & Comparative Immunology. 1999;23(4−5):375−390. doi: 10.1016/s0145-305x(99)00018-x.
Aspán A, Hall M, Söderhäll K. The effect of endogeneous proteinase inhibitors on the prophenoloxidase activating enzyme, a serine proteinase from crayfish haemocytes. Insect Biochemistry. 1990;20(5):485−492. doi: 10.1016/0020-1790(90)90030-x.
Buresova V, Hajdusek O, Franta Z, Sojka D, Kopacek P. IrAM—An α2-macroglobulin from the hard tick Ixodes ricinus: Characterization and function in phagocytosis of a potential pathogen Chryseobacterium indologenes. Developmental & Comparative Immunology. 2009;33(4):489−498. doi: 10.1016/j.dci.2008.09.011.
Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell. 2014;157(1):121−141. doi: 10.1016/j.cell.2014.03.011.
Lin L, Zhang J. Role of intestinal microbiota and metabolites on gut homeostasis and human diseases. BMC Immunology. 2017;18(1):2. doi: 10.1186/s12865-016-0187-3.
Clarke G, Stilling RM, Kennedy PJ, Stanton C, Cryan JF, Dinan TG. Minireview: gut microbiota: the neglected endocrine organ. Molecular Endocrinology. 2014;28(8):1221−1238. doi: 10.1210/me.2014-1108.
Xiong J, Zhu J, Dai W, Dong C, Qiu Q, Li C. Integrating gut microbiota immaturity and disease‐discriminatory taxa to diagnose the initiation and severity of shrimp disease. Environmental Microbiology. 2017;19(4):1490−1501. doi: 10.1111/1462-2920.13701.
Cornejo-Granados F, Lopez-Zavala AA, Gallardo-Becerra L, Mendoza-Vargas A, Sánchez F, Vichido R, et al. Microbiome of Pacific Whiteleg shrimp reveals differential bacterial community composition between wild, aquacultured and AHPND/EMS outbreak conditions. Scientific Reports. 2017;7(1):11783. doi: 10.1038/s41598-017-11805-w.
Chen W-Y, Ng TH, Wu J-H, Chen J-W, Wang H-C. Microbiome dynamics in a shrimp grow-out pond with possible outbreak of acute hepatopancreatic necrosis disease. Scientific Reports. 2017;7(1):9395. doi: 10.1038/s41598-017-09923-6.
Yu W, Wu J-H, Zhang J, Yang W, Chen J, Xiong J. A meta-analysis reveals universal gut bacterial signatures for diagnosing the incidence of shrimp disease. FEMS Microbiology Ecology. 2018;94(10):147. doi: 10.1093/femsec/fiy147.
Wang J, Huang Y, Xu K, Zhang X, Sun H, Fan L, et al. White spot syndrome virus (WSSV) infection impacts intestinal microbiota composition and function in Litopenaeus vannamei. Fish & Shellfish Immunology. 2019;84:130−137. doi: 10.1016/j.fsi.2018.09.076.
Gracia-Valenzuela MH, Coronado-Molina D, Hernández-López J, Gollas-Galván T. A simple method for purifying the White Spot Syndrome Virus using ultrafiltration. Aquaculture Research. 2009;40(6):737−743. doi: 10.1111/j.1365-2109.2008.02155.x.
Vargas-Albores F, Hernández-López J, Gollas-Galván T, Montaño-Pérez K, Jiménez-Vega F, Yepiz-Plascencia G. Activation of shrimp cellular defence functions by microbial products. In: Flegel TW, editor. Advances in Shrimp Biotechnology. Bangkok (Thailand): National Center for Genetic Engineering and Biotechnology; 1998. pp. 161–166.
Wang H-C, Wang H-C, Leu J-H, Kou G-H, Wang AH-J, Lo C-F. Protein expression profiling of the shrimp cellular response to white spot syndrome virus infection. Developmental & Comparative Immunology. 2007;31(7):672−686. doi: 10.1016/j.dci.2006.11.001.
Zhang L, Orth K. Virulence determinants for Vibrio parahaemolyticus infection. Current Opinion in Microbiology. 2013;16(1):70−77. doi: 10.1016/j.mib.2013.02.002.
Liang G-F, Liang Y, Xue Q, Lu J-F, Cheng J-J, Huang J. Astakine LvAST binds to the β subunit of F1-ATP synthase and likely plays a role in white shrimp Litopeneaus vannamei defense against white spot syndrome virus. Fish & Shellfish Immunology. 2015;43(1):75−81. doi: 10.1016/j.fsi.2014.12.015.
Motley AM, Berg N, Taylor MJ, Sahlender DA, Hirst J, Owen DJ, et al. Functional analysis of AP-2 α and μ2 subunits. Molecular Biology of the Cell. 2006;17(12):5298−5308. doi: 10.1091/mbc.e06-05-0452.
Lin Y-C, Vaseeharan B, Chen J-C. Molecular cloning and phylogenetic analysis on α2-macroglobulin (α2-M) of white shrimp Litopenaeus vannamei. Developmental & Comparative Immunology. 2008;32(4):317−329. doi: 10.1016/j.dci.2007.07.002.
Valenzuela-Castillo A, Mendoza-Cano F, Enríquez-Espinosa T, Grijalva-Chon JM, Sánchez-Paz A. Selection and validation of candidate reference genes for quantitative real-time PCR studies in the shrimp Penaeus vannamei under viral infection. Molecular and Cellular Probes. 2017;33:42−50. doi: 10.1016/j.mcp.2017.02.005.
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research. 2013;41(1):e1. doi: 10.1093/nar/gks808.
Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research. 2001;29(9):e45. doi: 10.1093/nar/29.9.e45.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25(4):402−408. doi: 10.1006/meth.2001.1262.
Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST©) for a group-wise comparison and statistical analysis of relative expression results in real- time PCR. Nucleic Acids Research. 2002;30(9):e36. doi: 10.1093/nar/30.9.e36.
McKight PE, Najab J. Kruskal‐Wallis test. In: IB Weiner, WE Craighead, editors. The Corsini Encyclopedia of Psychology. Hoboken, NJ: Wiley Online Library. 2010. p. 1. doi: 10.1002/9780470479216.corpsy0491.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nature Methods. 2010;7(5):335−336. doi: 10.1038/nmeth.f.303.
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods. 2016;13(7):581−583. doi: 10.1038/nmeth.3869.
Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584. doi: 10.7717/peerj.2584.
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biology. 2011;12(6):R60. doi: 10.1186/gb-2011-12-6-r60.
Legendre P, De Cáceres M. Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecology Letters. 2013;16(8):951−963. doi: 10.1111/ele.12141.
Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. Vegan: community ecology package (2.6-2). Vienna, Austria: R Foundation for Statistical Computing. 2022. 295 pp.
Li F, Li M, Ke W, Ji Y, Bian X, Yan X. Identification of the immediate-early genes of white spot syndrome virus. Virology. 2009;385(1):267−274. doi: 10.1016/j.virol.2008.12.007.
Han F, Xu J, Zhang X. Characterization of an early gene (wsv477) from shrimp white spot syndrome virus (WSSV). Virus Genes. 2007;34(2):193−198. doi: 10.1007/s11262-006-0053-0.
Verbruggen B, Bickley LK, Van Aerle R, Bateman KS, Stentiford GD, Santos EM, et al. Molecular mechanisms of white spot syndrome virus infection and perspectives on treatments. Viruses. 2016;8(1):23. doi: 10.3390/v8010023.
Friesen PD. Regulation of baculovirus early gene expression. In: Miller LE, editor. The Baculoviruses. The Viruses. Boston, MA: Springer Nature. 1997. pp. 141−170. doi: 10.1007/978-1-4899-1834-5_6.
Sánchez-Martínez JG, Aguirre-Guzmán G, Mejía-Ruíz H. White spot syndrome virus in cultured shrimp: A review. Aquaculture Research. 2007;38(13):1339−1354. doi: 10.1111/j.1365-2109.2007.01827.x.
Yi G, Wang Z, Qi Y, Yao L, Qian J, Hu L. Vp28 of shrimp white spot syndrome virus is involved in the attachment and penetration into shrimp cells. BMB Reports. 2004;37(6):726−734. doi: 10.5483/bmbrep.2004.37.6.726.
OIE. Enfermedades de la Lista de la OIE 2019. Oficina Internacional de Epizootias. 2019. https://www.woah.org/fileadmin/Home/esp/Health_standards/aahm/current/2.2.08_WSD_ESP.pdf
Mowery YM, Pizzo SV. The antitumorigenic trifecta. Blood. 2009;114(9):1727−1728. doi: 10.1182/blood-2009-06-226233.
Chen I-T, Aoki T, Huang Y-T, Hirono I, Chen T-C, Huang J-Y, et al. White spot syndrome virus induces metabolic changes resembling the Warburg effect in shrimp hemocytes in the early stage of infection. Journal of Virology. 2011;85(24):12919−12928. doi: 10.1128/jvi.05385-11.
Su M-A, Huang Y-T, Chen I-T, Lee D-Y, Hsieh Y-C, Li C-Y, et al. An invertebrate Warburg effect: a shrimp virus achieves successful replication by altering the host metabolome via the PI3K-Akt-mTOR pathway. PLOS Pathogens 2014;10(6):e1004196. doi: 10.1371/journal.ppat.1004196.
Fregoso-Peñuñuri AA, Valenzuela-Soto EM, Figueroa-Soto CG, Peregrino-Uriarte AB, Ochoa-Valdez M, Leyva-Carrillo L, et al. White shrimp Litopenaeus vannamei recombinant lactate dehydrogenase: Biochemical and kinetic characterization. Protein Expression and Purification. 2017;137:20−25. doi: 10.1016/j.pep.2017.06.010.
Cerenius L, Söderhäll K. The prophenoloxidase‐activating system in invertebrates. Immunological Reviews. 2004;198(1):116−126. doi: 10.1111/j.0105-2896.2004.00116.x.
Ma H, Wang B, Zhang J, Li F, Xiang J. Multiple forms of alpha-2 macroglobulin in shrimp Fenneropenaeus chinesis and their transcriptional response to WSSV or Vibrio pathogen infection. Developmental & Comparative Immunology. 2010;34(6):677−684. doi: 10.1016/j.dci.2010.01.014.
Tonganunt M, Phongdara A, Chotigeat W, Fujise K. Identification and characterization of syntenin binding protein in the black tiger shrimp Penaeus monodon. Journal of Biotechnology. 2005;120(2):135−145. doi: 10.1016/j.jbiotec.2005.06.006.
Somboonwiwat K, Chaikeeratisak V, Wang HC, Lo CF, Tassanakajon A. Proteomic analysis of differentially expressed proteins in Penaeus monodon hemocytes after Vibrio harveyi infection. Proteome Science. 2010;8(1):39. doi: 10.1186/1477-5956-8-39.
Perazzolo LM, Bachère E, Rosa RD, Goncalves P, Andreatta ER, Daffre S, et al. Alpha2-macroglobulin from an Atlantic shrimp: biochemical characterization, sub-cellular localization and gene expression upon fungal challenge. Fish & Shellfish Immunology. 2011;31(6):938−943. doi: 10.1016/j.fsi.2011.08.011.
Shanthi S, Vaseeharan B. Alpha 2 macroglobulin gene and their expression in response to GFP tagged Vibrio parahaemolyticus and WSSV pathogens in Indian white shrimp Fenneropenaeus indicus. Aquaculture. 2014;418-419:48−54. doi: 10.1016/j.aquaculture.2013.10.003.
Chotigeat W, Deachamag P, Phongdara A. Identification of a protein binding to the phagocytosis activating protein (PAP) in immunized black tiger shrimp. Aquaculture. 2007;271(1−4):112−120. doi: 10.1016/j.aquaculture.2007.03.019.
Pan L, Xie P, Hu F. Responses of prophenoloxidase system and related defence parameters of Litopenaeus vannamei to low salinity. Journal of Ocean University of China. 2010;9(3):273−278. doi: 10.1007/s11802-010-1711-3.
Huang J, Li F, Wu J, Yang F. White spot syndrome virus enters crayfish hematopoietic tissue cells via clathrin-mediated endocytosis. Virology. 2015;486:35−43. doi: 10.1016/j.virol.2015.08.034.
Moss SM, LeaMaster BR, Sweeney JN. Relative abundance and species composition of gram‐negative, aerobic bacteria associated with the gut of juvenile white shrimp Litopenaeus vannamei reared in oligotrophic well water and eutrophic pond water. Journal of the World Aquaculture Society. 2000;31(2):255−263. doi: 10.1111/j.1749-7345.2000.tb00361.x.
Oxley APA, Shipton W, Owens L, McKay D. Bacterial flora from the gut of the wild and cultured banana prawn, Penaeus merguiensis. Journal of Applied Microbiology. 2002;93(2):214−223. doi: 10.1046/j.1365-2672.2002.01673.x.
Liu W-J, Chang Y-S, Wang C-H, Kou G-H, Lo C-F. Microarray and RT-PCR screening for white spot syndrome virus immediate-early genes in cycloheximide-treated shrimp. Virology. 2005;334(2):327−341. doi: 10.1016/j.virol.2005.01.047.
Liu H, Wang L, Liu M, Wang B, Jiang K, Ma S, et al. The intestinal microbial diversity in Chinese shrimp (Fenneropenaeus chinensis) as determined by PCR–DGGE and clone library analyses. Aquaculture. 2011;317(1-4):32−36. doi: 10.1016/j.aquaculture.2011.04.008.
Gomez-Gil B, Tron-Mayén L, Roque A, Turnbull JF, Inglis V, Guerra-Flores AL. Species of Vibrio isolated from hepatopancreas, haemolymph and digestive tract of a population of healthy juvenile Penaeus vannamei. Aquaculture. 1998;163(1−2):1−9. doi: 10.1016/s0044-8486(98)00162-8.
Gao S, Pan L, Huang F, Song M, Tian C, Zhang M. Metagenomic insights into the structure and function of intestinal microbiota of the farmed Pacific white shrimp (Litopenaeus vannamei). Aquaculture. 2019;499:109−118. doi: 10.1016/j.aquaculture.2018.09.026.
De Bruijn I, Liu Y, Wiegertjes GF, Raaijmakers JM. Exploring fish microbial communities to mitigate emerging diseases in aquaculture. FEMS Microbiology Ecology. 2017;94(1):161. doi: 10.1093/femsec/fix161.
Sung H-H, Hsu S-F, Chen C-K, Ting Y-Y, Chao W-L. Relationships between disease outbreak in cultured tiger shrimp (Penaeus monodon) and the composition of Vibrio communities in pond water and shrimp hepatopancreas during cultivation. Aquaculture. 2001;192(2−4):101−110. doi: 10.1016/s0044-8486(00)00458-0.
Chatterjee S, Haldar S. Vibrio related diseases in aquaculture and development of rapid and accurate identification methods. Journal of Marine Science: Research & Development. 2012;s1:002. doi: 10.4172/2155-9910.s1-002.
Xing M, Hou Z, Yuan J, Liu Y, Qu Y, Liu B. Taxonomic and functional metagenomic profiling of gastrointestinal tract microbiome of the farmed adult turbot (Scophthalmus maximus). FEMS Microbiology Ecology. 2013;86(3):432−443. doi: 10.1111/1574-6941.12174.
Dierckens KR, Vandenberghe J, Beladjal L, Huys G, Mertens J, Swings J. Aeromonas hydrophila causes ‘black disease’ in fairy shrimps (Anostraca; Crustacea). Journal of Fish Diseases. 1998;21(2):113−119. doi: 10.1046/j.1365-2761.1998.00085.x.
Zhou J, Fang W, Yang X, Zhou S, Hu L, Li X, et al. A nonluminescent and highly virulent Vibrio harveyi strain is associated with “bacterial white tail disease” of Litopenaeus vannamei shrimp. PloS One. 2012;7(2):e29961. doi: 10.1371/journal.pone.0029961.
Rigottier-Gois L. Dysbiosis in inflammatory bowel diseases: the oxygen hypothesis. The ISME Journal. 2013;7(7):1256−1261. doi: 10.1038/ismej.2013.80.
Takahashi E, Ozaki H, Fujii Y, Kobayashi H, Yamanaka H, Arimoto S, et al. Properties of hemolysin and protease produced by Aeromonas trota. PloS One. 2014;9(3):e91149. doi: 10.1371/journal.pone.0091149.
Nayak SK. Probiotics and immunity: A fish perspective. Fish & Shellfish Immunology. 2010;29(1):2−14. doi: 10.1016/j.fsi.2010.02.017.
Zadeh SS, Saad CR, Christianus A, Kamarudin MS, Sijam K, Shamsudin MN, et al. Assessment of growth condition for a candidate probiotic, Shewanella algae, isolated from digestive system of a healthy juvenile Penaeus monodon. Aquaculture International. 2010;18(6):1017−1026. doi: 10.1007/s10499-010-9319-6.
Coyte KZ, Schluter J, Foster KR. The ecology of the microbiome: networks, competition, and stability. Science. 2015;350(6261):663−666. doi: 10.1126/science.aad2602.
Abdelkarim M, Kamel C, Fathi K, Amina B. Use of Pseudomonas stutzeri and Candida utilis in the improvement of the conditions of Artemia culture and protection against pathogens. Brazilian Journal of Microbiology. 2010;41(1):107−115. doi: 10.1590/s1517-83822010000100017.
Mahdhi A, Harbi B, Esteban MÁ, Chaieb K, Kamoun F, Bakhrouf A. Using mixture design to construct consortia of potential probiotic Bacillus strains to protect gnotobiotic Artemia against pathogenic Vibrio. Biocontrol Science and Technology. 2010;20(9):983–996. doi: 10.1080/09583157.2010.495185.
Ibrahem MD. Evolution of probiotics in aquatic world: potential effects, the current status in Egypt and recent prospectives. Journal of Advanced Research. 2015;6(6):765−791. doi: 10.1016/j.jare.2013.12.004.
Zumft WG, Braun C, Cuypers H. Nitric oxide reductase from Pseudomonas stutzeri. European Journal of Biochemistry 1994;219(1−2):481−490. doi: 10.1111/j.1432-1033.1994.tb19962.x.
Mackenzie BW, Waite DW, Hoggard M, Douglas RG, Taylor MW, Biswas K. Bacterial community collapse: a meta‐analysis of the sinonasal microbiota in chronic rhinosinusitis. Environmental Microbiology. 2017;19(1):381−392. doi: 10.1111/1462-2920.13632.
Dai W, Yu W, Zhang J, Zhu J, Tao Z, Xiong J. The gut eukaryotic microbiota influences the growth performance among cohabitating shrimp. Applied Microbiology and Biotechnology. 2017;101(16):6447−6457. doi: 10.1007/s00253-017-8388-0.
Mallon CA, van Elsas JD, Salles JF. Microbial invasions: the process, patterns, and mechanisms. Trends in Microbiology. 2015;23(11):719−729. doi: 10.1016/j.tim.2015.07.013.
Hou D, Huang Z, Zeng S, Liu J, Weng S, He J. Comparative analysis of the bacterial community compositions of the shrimp intestine, surrounding water, and sediment. Journal of Applied Microbiology. 2018;125(3):792−799. doi: 10.1111/jam.13919.
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