Role of riboflavin biosynthesis gene duplication and transporter in Aeromonas salmonicida virulence in marine teleost fish

References

• De Colibus L, Mattevi A. New frontiers in structural flavoenzymology. Curr Opin Struct Biol. 2006;16(6):722–23.
   PubMed Web of Science ®Google Scholar
• Abbas CA, Sibirny AA. Genetic control of biosynthesis and transport of riboflavin and flavin nucleotides and construction of robust biotechnological producers. Microbiol Mol Biol Rev. 2011;75(2):321–360.
   PubMed Web of Science ®Google Scholar
• Crossley RA, Gaskin DJH, Holmes K, et al. Riboflavin biosynthesis is associated with assimilatory ferric reduction and iron acquisition by campylobacter jejuni. Appl Environ Microbiol. 2007;73(24):7819–7825.
   PubMed Web of Science ®Google Scholar
• Marsili E, Baron DB, Shikhare ID, et al. Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci U S A. 2008;105(10):3968–3973.
   PubMed Web of Science ®Google Scholar
• Yurgel SN, Rice J, Domreis E, et al. Sinorhizobium meliloti flavin secretion and bacteria-host interaction: role of the bifunctional RibBA protein. Mol Plant Microbe Interact. 2014;27(5):437–445.
   PubMed Web of Science ®Google Scholar
• Rajamani S, Bauer WD, Robinson JB, et al. The Vitamin riboflavin and its derivative lumichrome activate the lasr bacterial quorum-sensing receptor. Mol Plant Microbe Interact. 2008;21(9):1184–1192.
   PubMed Web of Science ®Google Scholar
• Bonomi HR, Marchesini MI, Klinke S, et al. An atypical riboflavin pathway is essential for Brucella abortus virulence. PLoS ONE. 2010;5(2):e9435.
   PubMed Web of Science ®Google Scholar
• Skaar EP, Madhani HD. The battle for iron between bacterial pathogens and their vertebrate hosts. PLOS Pathog. 2010;6(8):1–2.
   Web of Science ®Google Scholar
• Gnanagobal H, Santander J. Host–pathogen interactions of marine gram-positive bacteria. Biology (Basel). 2022;11(9):1316.
   PubMedGoogle Scholar
• Prentice AM, Ghattas H, Cox SE. Host-Pathogen Interactions: can Micronutrients Tip the Balance? J Nutr. 2007;137(5):1334–1337.
   PubMed Web of Science ®Google Scholar
• García-Angulo VA. Overlapping riboflavin supply pathways in bacteria. Crit Rev Microbiol. 2017;43(2):196–209.
   PubMed Web of Science ®Google Scholar
• Jaehme M, Slotboom DJS. Function, evolution, and application of bacterial pnu-type vitamin transporters. Biol Chem. 2015;396(9–10):955–966.
   PubMed Web of Science ®Google Scholar
• Bacher A, Eberhardt S, Fischer M, et al. Biosynthesis of Vitamin B2 (Riboflavin). Annu Rev Nutr. 2000;20(1):153–167.
   PubMedGoogle Scholar
• Dauner M, Sonderegger M, Hochuli M, et al. Intracellular carbon fluxes in riboflavin-producing bacillus subtilis during growth on two-carbon substrate mixtures. Appl Environ Microbiol. 2002;68(4):1760–1771.
   PubMed Web of Science ®Google Scholar
• Fischer M, Bacher A. Biosynthesis of Flavocoenzymes. Nat Prod Rep. 2005;22(3):324–350.
   PubMed Web of Science ®Google Scholar
• Haase I, Gräwert T, Illarionov B, et al. Recent Advances in Riboflavin Biosynthesis. Methods Mol Biol. 2014;1146:15–40.
   PubMedGoogle Scholar
• Vitreschak AG, Rodionov DA, Mironov AA, et al. Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation. Nucleic Acids Res. 2002;30(14):3141–3151.
   PubMed Web of Science ®Google Scholar
• Angulo VAG, Bonomi HR, Posadas DM, et al. Identification and Characterization of RibN, a novel family of riboflavin transporters from rhizobium leguminosarum and other proteobacteria. 2013, 195, 4611–4619, doi:10.1128/JB.00644-13. 20
   Google Scholar
• Jaehme M, Slotboom DJ. Diversity of membrane transport proteins for vitamins in bacteria and archaea. Biochim Biophys Acta. 2015;1850(3):565–576.
   PubMed Web of Science ®Google Scholar
• Hemberger S, Pedrolli DB, Stolz J, et al. RibM from Streptomyces davawensis is a riboflavin/roseoflavin transporter and may be useful for the optimization of riboflavin production strains. BMC Biotechnol. 2011;11(1):119.
   PubMedGoogle Scholar
• Cisternas IS, Torres A, Flores AF, et al. Differential Regulation of Riboflavin Supply Genes in Vibrio cholerae. Gut Pathog. 2017;9(1):1–7.
   PubMedGoogle Scholar
• Rivera-Lugo R, Light SH, Garelis NE, et al. RibU is an essential determinant of listeria pathogenesis that mediates acquisition of FMN and FAD during intracellular growth. Proc Natl Acad Sci. 2022;119(13):e2122173119.
   PubMed Web of Science ®Google Scholar
• Winkler WC, Cohen-Chalamish S, Breaker RR. An MRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci U S A. 2002;99(25):15908–15913.
   PubMed Web of Science ®Google Scholar
• Vicens Q, Mondragón E, Batey RT. Molecular sensing by the aptamer domain of the FMN Riboswitch: a general model for ligand binding by conformational selection. Nucleic Acids Res. 2011;39(19):8586–8598.
   PubMed Web of Science ®Google Scholar
• Gutiérrez-Preciado A, Gabriel Torres A, Merino E, et al. Extensive identification of bacterial riboflavin transporters and their distribution across bacterial species. 2015, doi:10.1371/journal.pone.0126124.
   Google Scholar
• Pedrolli D, Langer S, Hobl B, et al. The RibB FMN Riboswitch from Escherichia coli operates at the transcriptional and translational level and regulates riboflavin biosynthesis. FEBS J. 2015;282(16):3230–3242.
   PubMed Web of Science ®Google Scholar
• Vitreschak AG, Rodionov DA, Mironov AA, et al. Riboswitches: the oldest mechanism for the regulation of gene expression? Trends Genet. 2004;20(1):44–50.
   PubMed Web of Science ®Google Scholar
• Adler M, Anjum M, Berg OG, et al. High fitness costs and instability of gene duplications reduce rates of evolution of new genes by duplication-divergence mechanisms. Mol Biol Evol. 2014;31(6):1526–1535.
   PubMed Web of Science ®Google Scholar
• Maerk M, Johansen J, Ertesvåg H, et al. Safety in numbers: multiple occurrences of highly similar homologs among azotobacter vinelandii carbohydrate metabolism proteins probably confer adaptive benefits. BMC genom. 2014;15(1). DOI:10.1186/1471-2164-15-192
   PubMedGoogle Scholar
• Wilson AC, Pardee AB. Regulation of flavin synthesis by Escherichia coli. J Gen Microbiol. 1962;28(2):283–303.
   PubMedGoogle Scholar
• Perkins JB, Pero JG. Biosynthesis of riboflavin, biotin, folic acid, and cobalamin. In: Sonenshein AL, Losick R, editors. Bacillus subtilis and other gram‐positive bacteria: Biochemistry, physiology, and molecular genetics. 1993. p. 391–394.
   Google Scholar
• Fuller TE, Mulks MH. Characterization of actinobacillus pleuropneumoniae riboflavin biosynthesis genes. J Bacteriol. 1995;177(24):7265–7270.
   PubMed Web of Science ®Google Scholar
• Beaz-Hidalgo R, Figueras MJ. Aeromonas spp. whole genomes and virulence factors implicated in fish disease. J Fish Dis. 2013;36(4):371–388.
   PubMed Web of Science ®Google Scholar
• Dallaire-Dufresne S, Tanaka KH, Trudel MV, et al. Genomic features, and plasticity of Aeromonas salmonicida subsp Salmonicida, the Causative Agent of Fish Furunculosis. Vet Microbiol. 2014;169(1–2):1–7.
   PubMed Web of Science ®Google Scholar
• Powell A, Treasurer JW, Pooley CL, et al. Use of lumpfish for sea-lice control in salmon farming: challenges and opportunities. Rev Aquac. 2018;10(3):683–702.
   Web of Science ®Google Scholar
• Imsland AKD, Hanssen A, Nytrø AV, et al. Lumpfish can significantly lower sea lice infestation in large-scale salmon farming. Biol Open. 2018;7(9):1–6.
   Web of Science ®Google Scholar
• Gulla S, Duodu S, Nilsen A, et al. Aeromonas salmonicida infection levels in pre- and post-stocked cleaner fish assessed by culture and an amended qPCR assay. J Fish Dis. 2016;39(7):867–877.
   PubMed Web of Science ®Google Scholar
• Rouleau FD, Vincent AT, Charette SJ. Genomic and phenotypic characterization of an atypical Aeromonas salmonicida strain isolated from a lumpfish and producing unusual granular structures. J Fish Dis. 2018;41(4):673–681.
   PubMed Web of Science ®Google Scholar
• Fast MD, Tse B, Boyd JM, et al. Mutations in the Aeromonas salmonicida subspsalmonicida Type III secretion system affect Atlantic salmon leucocyte activation and downstream immune responses. Fish Shellfish Immunol. 2009;27(6):721–728.
   PubMed Web of Science ®Google Scholar
• Valderrama K, Saravia M, Santander J. Phenotype of Aeromonas salmonicida sp. salmonicida cyclic adenosine 3’,5’-monophosphate receptor protein (crp) mutants and its virulence in rainbow trout (Oncorhynchus mykiss). J Fish Dis. 2017;40(12):1849–1856.
   PubMed Web of Science ®Google Scholar
• Vasquez I, Cao T, Hossain A, et al. Aeromonas salmonicida infection kinetics and protective immune response to vaccination in sablefish (Anoplopoma fimbria). Fish Shellfish Immunol. 2020;104(May):557–566.
   PubMedGoogle Scholar
• Gauthier J, Marquis H, Paquet VE, et al. Genomic perspectives on Aeromonas salmonicida subsp. salmonicida strain 890054 as a model system for pathogenicity studies and mitigation of fish infections. Front Mar Sci. 2021, 8 (November), 1–8, doi:10.3389/fmars.2021.744052.
   PubMed Web of Science ®Google Scholar
• Inglis V, Robertson D, Miller K, et al. Antibiotic Protection against recrudescence of latent Aeromonas salmonicida during furunculosis vaccination. J Fish Dis. 1996;19(5):341–348.
   Web of Science ®Google Scholar
• Sommerset I, Krossøy B, Biering E, et al. Vaccines for Fish in Aquaculture. Expert Rev Vaccines. 2005;4(1):89–101.
   PubMed Web of Science ®Google Scholar
• Gudding R, Van Muiswinkel WB. A history of fish vaccination: science-based disease prevention in aquaculture. Fish Shellfish Immunol. 2013;35(6):1683–1688.
   PubMed Web of Science ®Google Scholar
• Menanteau-Ledouble S, Krauss I, Santos G, et al. Effect of a phytogenic feed additive on the susceptibility of Oncorhynchus mykiss to Aeromonas salmonicida. Dis Aquat Organ. 2015;115(1):57–66.
   PubMed Web of Science ®Google Scholar
• Roland K, Curtiss R 3rd, Sizemore D. Construction and Evaluation of a delta cya delta crp salmonella typhimurium strain expressing avian pathogenic Escherichia coli O78 LPS as a vaccine to prevent airsacculitis in chickens. Avian Dis. 1999;43(3):429–441.
   PubMed Web of Science ®Google Scholar
• Santander J, Wanda SY, Nickerson CA, et al. Role of RpoS in fine-tuning the synthesis of Vi capsular polysaccharide in salmonella enterica serotype typhi. Infect Immun. 2007;75(3):1382–1392.
   PubMed Web of Science ®Google Scholar
• Datsenko KA, Wanner BL. One-Step Inactivation of Chromosomal Genes in Escherichia coli K-12 Using PCR Products. Proc Natl Acad Sci U S A. 2000;97(12):6640–6645.
   PubMed Web of Science ®Google Scholar
• Nerland AH, Hogh BT, Olsen AB, et al. Aeromonas salmonicida ssp. salmonicida requires exogenous arginine and methionine for growth. J Fish Dis. 1993;16(6):605–608.
   Web of Science ®Google Scholar
• Bertani G. Studies on Lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol. 1951, 62 (3), 293–300, doi:10.1128/jb.62.3.293-300.1951.
   PubMed Web of Science ®Google Scholar
• Reith ME, Singh RK, Curtis B, et al. The genome of Aeromonas salmonicida subsp. salmonicida a449: insights into the evolution of a fish pathogen. BMC Genomics. 2008;9(1):427.
   PubMedGoogle Scholar
• Kanehisa M, Sato Y, Kawashima M, et al. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 2015;44(D1):457–462.
   PubMed Web of Science ®Google Scholar
• Abreu-Goodger C, Merino E. RibEx: a web server for locating riboswitches and other conserved bacterial regulatory elements. Nucleic Acids Res. 2005;33(Web Server issue):W690–2.
   PubMedGoogle Scholar
• Waterhouse AM, Procter JB, Martin DMA, et al. Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009;25(9):1189–1191.
   PubMed Web of Science ®Google Scholar
• Gouet P, Robert X, Courcelle E Espript/Endscript: extracting and Rendering Sequence and 3D Information from Atomic Structures of Proteins. 2003, doi:10.1093/nar/gkg556.
   Google Scholar
• Sö J, Biegert A, Lupas AN The hhpred interactive server for protein homology detection and structure prediction. 2005, doi:10.1093/nar/gki408.
   Google Scholar
• Humphrey W, Dalke A, Schulten KV. Visual molecular dynamics. J Mol Graph. 1996;14(1):33–38.
   PubMedGoogle Scholar
• Du Z, Su H, Wang W, et al. The TrRosetta server for fast and accurate protein structure prediction. Nat Protoc. 2021;16(12):5634–5651.
   PubMed Web of Science ®Google Scholar
• Connors E, Soto-Dávila M, Hossain A, et al. Identification and validation of reliable Aeromonas salmonicida subspecies salmonicida reference genes for differential gene expression analyses. Infect Genet Evol. 2019;73:314–321.
   PubMed Web of Science ®Google Scholar
• Sambrook J, Russel W. Molecular Cloning: a Laboratory Manual. 2nd ed. New York: Cold Spring Harbor Laboratory Press; 2001.
   Google Scholar
• Umasuthan N, Valderrama K, Vasquez I, et al. A Novel marine pathogen isolated from wild cunners (tautogolabrus adspersus): comparative genomics and transcriptome profiling of pseudomonas sp. strain J380. Microorganisms. 2021;9(4):812.
   PubMed Web of Science ®Google Scholar
• Chakraborty S, Hossain A, Cao T, et al. Multi-organ transcriptome response of lumpfish (cyclopterus lumpus) to Aeromonas salmonicida subspecies salmonicida systemic infection. Microorganisms. 2022;10(11):2113.
   PubMed Web of Science ®Google Scholar
• Ewels P, Magnusson M, Lundin S, et al. Summarize analysis results for multiple tools and samples in a single report. Bioinformatics. 2016;32(19):3047–3048.
   PubMed Web of Science ®Google Scholar
• Li B, Ruotti V, Stewart RM, et al. RNA-Seq gene expression estimation with read mapping uncertainty. Bioinformatics. 2010;26(4):493–500.
   PubMed Web of Science ®Google Scholar
• Teng M, Love MI, Davis CA, et al. Erratum to: a Benchmark for RNA-Seq quantification pipelines. Genome Biol. 2016;17(1):203.
   PubMedGoogle Scholar
• Pereira MB, Wallroth M, Jonsson V, et al. Comparison of normalization methods for the analysis of metagenomic gene abundance data. BMC Genomics. 2018;19(1):274.
   PubMedGoogle Scholar
• Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29(9):e45.
   PubMed Web of Science ®Google Scholar
• Vandesompele J, De Preter K, Pattyn F, et al. Accurate normalization of real-time quantitative rt-pcr data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3(7):1–12.
   Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Gnanagobal H, Cao T, Hossain A, et al. Lumpfish (Cyclopterus lumpus) is Susceptible to Renibacterium salmoninarum Infection and Induces Cell-Mediated Immunity in the Chronic Stage. Front Immunol. 2021;12:4647.
   Web of Science ®Google Scholar
• Santander J, Martin T, Loh A, et al. Mechanisms of Intrinsic resistance to antimicrobial peptides of edwardsiella ictaluri and its influence on fish gut inflammation and virulence. Microbiology. 2013;159(Pt 7):1471–1486.
   PubMedGoogle Scholar
• Edwards RA, Keller LH, Schifferli DM. Improved allelic exchange vectors and their use to analyze 987p fimbria gene expression. Gene. 1998;207:149–157.
   PubMed Web of Science ®Google Scholar
• Reyrat J, Pelicic V, Gicquel B. Counterselectable Markers: untapped tools for bacterial genetics and pathogenesis. Infect Immun. 1998;66(9):4011–4017.
   PubMed Web of Science ®Google Scholar
• Kelly MJS, Ball LJ, Krieger C, et al. The NMR Structure of the 47-KDa Dimeric Enzyme 3,4-Dihydroxy-2-Butanone-4-Phosphate Synthase and Ligand Binding Studies Reveal the Location of the Active Site. Proc Natl Acad Sci U S A. 2001;98(23):13025–13030.
   PubMed Web of Science ®Google Scholar
• Ren J, Kotaka M, Lockyer M, et al. GTP Cyclohydrolase II Structure and Mechanism. J Biol Chem. 2005;280(44):36912–36919.
   PubMed Web of Science ®Google Scholar
• Islam Z, Kumar A, Singh S, et al. Structural Basis for Competitive Inhibition of 3,4-Dihydroxy-2-Butanone-4-Phosphate Synthase from Vibrio cholerae. J Biol Chem. 2015;290(18):11293–11308.
   PubMed Web of Science ®Google Scholar
• Brutinel ED, Dean AM, Gralnick JA. Description of a riboflavin biosynthetic gene variant prevalent in the phylum proteobacteria. J Bacteriol. 2013;195(24):5479–5486.
   PubMed Web of Science ®Google Scholar
• Nouwen N, Arrighi JF, Gully D, et al. RibBX of bradyrhizobium ORS285 plays an important role in intracellular persistence in various aeschynomene host plants. Mol Plant-Microbe Interact. 2021;34(1):88–99.
   PubMed Web of Science ®Google Scholar
• Illarionov B, Kemter K, Eberhardt S, et al. Riboflavin synthase of Escherichia coli. effect of single amino acid substitutions on reaction rate and ligand binding properties. J Biol Chem. 2001;276(15):11524–11530.
   PubMed Web of Science ®Google Scholar
• Serer MI, Bonomi HR, Guimarães BG, et al. Crystallographic and kinetic study of riboflavin synthase from Brucella abortus, a chemotherapeutic target with an enhanced intrinsic flexibility. Acta Crystallogr D Biol Crystallogr. 2014;70(Pt 5):1419–1434.
   PubMedGoogle Scholar
• Ma Y, Pan C, Wang Q. Crystal structure of bacterial cyclopropane-fatty-Acyl-Phospholipid synthase with phospholipid. J Biochem. 2019;166(2):139–147.
   PubMed Web of Science ®Google Scholar
• Sepúlveda-Cisternas I, Lozano Aguirre L, Fuentes Flores A, et al. Transcriptomics reveals a cross-modulatory effect between riboflavin and iron and outlines responses to riboflavin biosynthesis and uptake in vibrio cholerae. Sci Rep. 2018;8(1):3149.
   PubMedGoogle Scholar
• Gelfand MS, Mironov AA, Jomantas J, et al. A conserved RNA structure element involved in the regulation of bacterial riboflavin synthesis genes. Trends Genet. 1999;15(11):439–442.
   PubMed Web of Science ®Google Scholar
• Burgess CM, Slotboom DJ, Geertsma ER, et al. The riboflavin transporter ribu in Lactococcus lactis: molecular characterization of gene expression and the transport mechanism. J Bacteriol. 2006;188(8):2752–2760.
   PubMed Web of Science ®Google Scholar
• Schott K, Kellermann J, Lottspeich F, et al. Riboflavin synthases of bacillus subtilis. purification and amino acid sequence of the alpha subunit. J Biol Chem. 1990;265(8):4204–4209.
   PubMed Web of Science ®Google Scholar
• Grill S, Yamaguchi H, Wagner H, et al. Identification and characterization of two Streptomyces davawensis riboflavin biosynthesis gene clusters. Arch Microbiol. 2007;188(4):377–387.
   PubMed Web of Science ®Google Scholar
• Hickman AB, Dyda F, Chandler M Mechanisms of DNA Transposition. Microbiol Spectr. 2015, 3 (2), MDNA3-2014, doi:10.1128/microbiolspec.MDNA3-0034-2014.
   PubMedGoogle Scholar
• Mahillon J, Chandler M. Insertion Sequences. Microbiol Mol Biol Rev. 1998;62(3):725–774.
   PubMed Web of Science ®Google Scholar
• Tanaka KH, Frenette M, Charette SJ. IS-Mediated loss of virulence by Aeromonas salmonicida. Mob Genet Elements. 2013;3(1):e23498.
   PubMedGoogle Scholar
• Lysnyansky I, Calcutt MJ, Ben-Barak I, et al. Molecular characterization of newly Identified IS3, IS4 and IS30 insertion sequence-like elements in mycoplasma bovis and their possible roles in genome plasticity. FEMS Microbiol Lett. 2009 May;294(2):172–182.
   PubMed Web of Science ®Google Scholar
• Schmid-Appert M, Zoller K, Traber H, et al. Association of Newly Discovered is Elements with the Dichloromethane Utilization Genes of Methylotrophic Bacteria. Microbiology. 1997;143(Pt8):2557–2567.
   PubMedGoogle Scholar
• Balado M, Souto A, Vences A, et al. Two catechol siderophores, acinetobactin and amonabactin, are simultaneously produced by Aeromonas salmonicida subsp salmonicida sharing part of the biosynthetic pathway. ACS Chem Biol. 2015;10(12):2850–2860.
   PubMed Web of Science ®Google Scholar
• Chakraborty S, Cao T, Hossain A, et al. Vibrogen-2 vaccine trial in lumpfish (cyclopterus lumpus) against vibrio anguillarum. J Fish Dis. 2019;42(7):1057–1064.
   PubMed Web of Science ®Google Scholar
• Dang M, Cao T, Vasquez I, et al. Oral immunization of larvae and juvenile of lumpfish (cyclopterus lumpus) against vibrio anguillarum does not influence systemic immunity. Vaccines. 2021;9(8):819.
   Web of Science ®Google Scholar
• Fuller TE, Thacker BJ, Mulks MH. A riboflavin auxotroph of actinobacillus pleuropneumoniae is attenuated in swine. Infect Immun. 1996;64(11):4659–4664.
   PubMed Web of Science ®Google Scholar
• Lopez AM, Townsend HGG, Allen AL, et al. Safety and immunogenicity of a live-attenuated auxotrophic candidate vaccine against the intracellular pathogen rhodococcus equi. Vaccine. 2008;26(7):998–1009.
   PubMed Web of Science ®Google Scholar
• Fuller TE, Thacker BJ, Duran CO, et al. A genetically-defined riboflavin auxotroph of actinobacillus pleuropneumoniae as a live attenuated vaccine. Vaccine. 2000;18(25):2867–2877.
   PubMed Web of Science ®Google Scholar
• Vaughan LM, Smith PR, Foster TJ. An aromatic-dependent mutant of the fish pathogen Aeromonas salmonicida is attenuated in fish and is effective as a live vaccine against the salmonid disease furunculosis. Infect Immun. 1993;61(5):2172–2181.
   PubMed Web of Science ®Google Scholar
• Swain B, Powell CT, Curtiss R. Pathogenicity and immunogenicity of edwardsiella piscicida Ferric Uptake Regulator (Fur) mutations in zebrafish. Fish Shellfish Immunol. 2020;107:497–510.
   PubMed Web of Science ®Google Scholar