Vibrio splendidus virulence to Apostichopus japonicus is mediated by hppD through glutamate metabolism and flagellum assembly

References

• Zhang X, Austin B. Haemolysins in Vibrio species. J Appl Microbiol. 2005;98(5):1011–1019.
   PubMed Web of Science ®Google Scholar
• Craig BA, Oliver JD, Munirul A, et al. Vibrio spp. infections. Nat Rev Dis Primers. 2018;4(1):8.
   PubMedGoogle Scholar
• Chibani CM, Poehlein A, Roth O, et al. Draft genome sequence of Vibrio splendidus DSM 19640. Genome Announc. 2017;5(48): e01368-17. doi:10.1128/genomeA.01368-17.
   PubMedGoogle Scholar
• Thomson R, Macpherson HL, Riaza A, et al. Vibrio splendidus biotype 1 as a cause of mortalities in hatchery-reared larval turbot Scophthalmus maximus(l.). J Appl Microbiol. 2005;99(2):243–250. DOI:10.1111/j.1365-2672.2005.02602.x
   PubMed Web of Science ®Google Scholar
• Lacoste A, Jalabert F, Malham S, et al. A Vibrio splendidus strain is associated with summer mortality of juvenile oysters Crassostrea gigas in the Bay of Morlaix (North Brittany, France). Dis Aquat Organ. 2001;46(2):139–145. DOI:10.3354/dao046139
   PubMed Web of Science ®Google Scholar
• Li H, Qiao G, Li Q, et al. Biological characteristics and pathogenicity of a highly pathogenic Shewanella marisflavi infecting sea cucumber, Apostichopus japonicus. J Fish Dis. 2010;33(11):865–877. DOI:10.1111/j.1365-2761.2010.01189.x
   PubMed Web of Science ®Google Scholar
• Rafidah O, Firdaus-Nawi M, Raehanah MSS, et al. An outbreak of Vibrio alginolyticus infection in juvenile sea cucumbers Holothuria scabra in Sabah, Malaysia. Pertanika J Trop Agric Sci. 2017;40:691–696.
   Web of Science ®Google Scholar
• Delroisse J, Wayneberghe KV, Flammang P, et al. Epidemiology of a Skin Ulceration Disease (SKUD) in the sea cucumber Holothuria scabra with a review on the SKUDs in Holothuroidea (Echinodermata). Sci Rep. 2020;10(1):22150. DOI:10.1038/s41598-020-78876-0
   PubMed Web of Science ®Google Scholar
• Eeckhaut I, Wayenberghe KV, Nicolas F, et al. Skin ulcerations in Holothuria scabra can be induced by various types of food. SPC Beche-de-Mer Inf Bull. 2019;39:31–35.
   Google Scholar
• Deng H, He C, Zhou Z, et al. Isolation and pathogenicity of pathogens from skin ulceration disease and viscera ejection syndrome of the sea cucumber Apostichopus japonicus. Aquaculture. 2009;287(1–2):18–27. DOI:10.1016/j.aquaculture.2008.10.015
   Web of Science ®Google Scholar
• Liu H, Zheng F, Sun X, et al. Identification of the pathogens associated with skin ulceration and peristome tumescence in cultured sea cucumbers Apostichopus japonicus (Selenka). J Invertebr Pathol. 2010;105(3):236–242. DOI:10.1016/j.jip.2010.05.016
   PubMed Web of Science ®Google Scholar
• Austin B, Austin DA. Bacterial fish pathogens: disease of farmed and wild fish. 3rd edn (revised ed. Godalming: Springer-Praxis; 1999.
   Google Scholar
• Zhang C, Liang W, Zhang W, et al. Characterization of a metalloprotease involved in Vibrio splendidus infection in the sea cucumber, Apostichopus japonicus. Microb Pathog. 2016;101:96–103.
   PubMed Web of Science ®Google Scholar
• Zhang C, Zhang W, Liang W, et al. A sigma factor RpoD negatively regulates temperature-dependent metalloprotease expression in a pathogenic Vibrio splendidus. Microb Pathog. 2019;128:311–316.
   PubMed Web of Science ®Google Scholar
• Zhang S, Liu N, Liang W, et al. Quorum sensing-disrupting coumarin suppressing virulence phenotypes in Vibrio splendidus. Appl Microbiol Biotechnol. 2017;101(8):3371–3378. DOI:10.1007/s00253-016-8009-3
   PubMed Web of Science ®Google Scholar
• Song T, Liu H, Lv T, et al. Characteristics of the iron uptake-related process of a pathogenic Vibrio splendidus strain associated with massive mortalities of the sea cucumber Apostichopus japonicus. J Invertebr Pathol. 2018;155:25–31.
   PubMed Web of Science ®Google Scholar
• Liang W, Zhang C, Liu N, et al. Cloning and characterization of Vshppd, a gene inducing haemolysis and immunity response of Apostichopus japonicus. Aquaculture. 2016;464:246–252.
   Web of Science ®Google Scholar
• Moran GR. 4-Hydroxyphenylpyruvate dioxygenase. Arch Biochem Biophys. 2005;433(1):117–128.
   PubMed Web of Science ®Google Scholar
• Hegedus ZL, Nayak U. Homogentisic acid and structurally related compounds as intermediates in plasma soluble melanin formation and in tissue toxicities. Arch Int Physiol Biochim Biophys. 1994;102(3):175–181.
   PubMedGoogle Scholar
• Hegedus ZL. The probable involvement of soluble and deposited melanins, their intermediates and the reactive oxygen side-products in human diseases and aging. Toxicology. 2000;145(2–3):85–101.
   PubMed Web of Science ®Google Scholar
• Lee CM, Yeo YS, Lee JH, et al. Identification of a novel 4-hydroxyphenylpyruvate dioxygenase from the soil metagenome. Biochem Biophys Res Commun. 2008;370(2):322–326. DOI:10.1016/j.bbrc.2008.03.102
   PubMed Web of Science ®Google Scholar
• Liang W, Zhang W, Shao Y, et al. Dual functions of a 4-hydroxyphenylpyruvate dioxygenase for Vibrio splendidus survival and infection. Microb Pathog. 2018;120:47–54.
   PubMed Web of Science ®Google Scholar
• Sorek R, Cossart P. Prokaryotic transcriptomics: a new view on regulation, physiology and pathogenicity. Nat Rev Genet. 2010;11(1):9–16.
   PubMed Web of Science ®Google Scholar
• Zhang W, Liang W, Li C. Inhibition of marine Vibrio sp. by pyoverdine from Pseudomonas aeruginosa PA1. J Hazard Mater. 2016;302:217–224.
   PubMed Web of Science ®Google Scholar
• Hu Y, Liu C, Hou J, et al. Identification, characterization, and molecular application of a virulence-associated autotransporter from a pathogenic Pseudomonas fluorescens strain. Appl Environ Microbiol. 2009;75(13):4333–4340. DOI:10.1128/AEM.00159-09
   PubMed Web of Science ®Google Scholar
• Gu D, Meng H, Li Y, et al. A GntR family transcription factor (VPA1701) for swarming motility and colonization of Vibrio parahaemolyticus. Pathogens. 2019;8(4):235. DOI:10.3390/pathogens8040235
   PubMed Web of Science ®Google Scholar
• Langmead B, and Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–359. doi:10.1038/nmeth.1923.
   PubMed 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
• Luo G, Huang L, Su Y, et al. flra, ?rb and ?rc regulate adhesion by controlling the expression of critical virulence genes in Vibrio alginolyticus. Emerg Microbes Infect. 2016;5(8):e85. DOI:10.1038/emi.2016.82
   PubMed Web of Science ®Google Scholar
• Wang Z, Lin B, Mostaghim A, et al. Vibrio campbellii hmgA-mediated pyomelanization impairs quorum sensing, virulence, and cellular fitness. Front Microbiol. 2013;4:379.
   PubMed Web of Science ®Google Scholar
• Pathak S, Awuh JA, Leversen NA, et al. Counting mycobacteria in infected human cells and mouse tissue: a comparison between qPCR and CFU. PLoS One. 2012;7(4):e34931. DOI:10.1371/journal.pone.0034931
   PubMed Web of Science ®Google Scholar
• Ouwehand AC, Kirjavainen PV, Gronlund MM, et al. Adhesion of probiotic micro-organisms to intestinal mucus. Int Dairy J. 1999;9(9):623–630. DOI:10.1016/S0958-6946(99)00132-6
   Web of Science ®Google Scholar
• Beceiro A, Tomás M, Bou G. Antimicrobial resistance and virulence: a successful or deleterious association in the bacterial world? Clin Microbiol Rev. 2013;26(2):185–230.
   PubMed Web of Science ®Google Scholar
• Qin Y, Lin G, Chen W, et al. Flagellar motility contributes to the invasion and survival of Aeromonas hydrophila in Anguilla japonica macrophages. Fish Shellfish Immunol. 2014;39(2):273–279. DOI:10.1016/j.fsi.2014.05.016
   PubMed Web of Science ®Google Scholar
• Luo G, Sun Y, Huang L, et al. Time-Resolved dual RNA-seq of tissue uncovers pseudomonas plecoglossicida key virulence genes in host-pathogen interaction with Epinephelus coioides. Environ Microbiol. 2020;22(2):677–693. DOI:10.1111/1462-2920.14884
   PubMed Web of Science ®Google Scholar
• Guo L, Huang L, Su Y, et al. secA, secD, secF, yajC, and yidC contribute to the adhesion regulation of Vibrio alginolyticus. Microbiologyopen. 2018;7(2):e00551. DOI:10.1002/mbo3.551
   PubMed Web of Science ®Google Scholar
• Liu W, Huang L, Su Y, et al. Contributions of the oligopeptide permeases in multistep of Vibrio alginolyticus pathogenesis. Microbiologyopen. 2017;6(5):e00511. DOI:10.1002/mbo3.511
   PubMed Web of Science ®Google Scholar
• Singh D, Kumar J, Kumar A. Isolation of pyomelanin from bacteria and evidences showing its synthesis by 4-hydroxyphenylpyruvate dioxygenase enzyme encoded by hppD gene. Int J Biol Macromol. 2018;119:864–873.
   PubMed Web of Science ®Google Scholar
• Denoya CD, Skinner DD, Morgenstern MR. A Streptomyces avermitilis gene encoding a 4-hydroxyphenylpyruvic acid dioxygenase-like protein that directs the production of homogentisic acid and an ochronotic pigment in Escherichia coli. J Bacteriol. 1994;176(17):5312–5319.
   PubMed Web of Science ®Google Scholar
• Brownlee JM, Johnson-Winters K, Harrison DH, et al. Structure of the ferrous form of (4-hydroxyphenyl) pyruvate dioxygenase from Streptomyces avermitilis in complex with the therapeutic herbicide, NTBC. Biochemistry. 2004;43(21):6370–6377. DOI:10.1021/bi049317s
   PubMed Web of Science ®Google Scholar
• Liu B, Peng Q, Sheng M, et al. Isolation and characterization of a topramezone-resistant 4-hydroxyphenylpyruvate dioxygenase from Sphingobium sp. TPM-19. J Agric Food Chem. 2020;68(4):1022–1029. DOI:10.1021/acs.jafc.9b06871
   PubMed Web of Science ®Google Scholar
• Serre L, Sailland A, Sy D, et al. Crystal structure of Pseudomoans ?uorescens 4-hydroxyphenylpyruvate dioxygenase: an enzyme involved in the tyrosine degradation pathway. Structure. 1999;7(8):977–988. DOI:10.1016/S0969-2126(99)80124-5
   PubMed Web of Science ®Google Scholar
• Steinert M, Flugel M, Schuppler M, et al. The Lly protein is essential for p-hydroxyphenylpyruvate dioxygenase activity in Legionella pneumophila. FEMS Microbiol Lett. 2001;203(1):41–47. DOI:10.1111/j.1574-6968.2001.tb10818.x
   PubMed Web of Science ®Google Scholar
• Steinert M, Engelhard H, Flugel M, et al. The Lly protein protects Legionella pneumophila from light but does not directly infuence its intracellular survival in Hartmannella vermiformis. Appl Environ Microbiol. 1995;61(6):2428–2430. DOI:10.1128/aem.61.6.2428-2430.1995
   PubMed Web of Science ®Google Scholar
• Gutierrez West CK, Klein SL, Lovell CR. High frequency of virulence factor genes tdh, trh, and tlh in Vibrio parahaemolyticus strains isolated from a pristine estuary. Appl Environ Microbiol. 2013;79(7):2247–2252.
   PubMed Web of Science ®Google Scholar
• Liu Y, Sui M, Ji D, et al. Protection from UV irradiation by melanin of mosquitocidal activity of Bacillus thuringiensis var. israelensis. J Invertebr Pathol. 1993;62(2):131–136. DOI:10.1006/jipa.1993.1088
   PubMed Web of Science ®Google Scholar
• Levin TC, Goldspiel BP, Malik HS. Density-Dependent resistance protects Legionella pneumophila from its own antimicrobial metabolite, HGA. Elife. 2019;8:e46086.
   PubMed Web of Science ®Google Scholar
• Kimura T, Kobayashi K, O’-Toole G. Role of glutamate synthase in biofilm formation by Bacillus subtilis. J Bacteriol. 2020;202(14). e00120-20. DOI:10.1128/JB.00120-20.
   PubMed Web of Science ®Google Scholar
• Abu Khweek A, Amer AO. Factors mediating environmental biofilm formation by Legionella pneumophila. Front Cell Infect Microbiol. 2018;8:38.
   PubMed Web of Science ®Google Scholar
• Zeng Z, Cai X, Wang P, et al. Biofilm formation and heat stress induce pyomelanin production in deep-sea Pseudoalteromonas sp. SM9913. Front Microbiol. 2017;8:1822.
   PubMed Web of Science ®Google Scholar
• Whitham JM, Moon JW, Rodriguez M, et al. Clostridium thermocellum LL1210 pH homeostasis mechanisms informed by transcriptomics and metabolomics. Biotechnol Biofuels. 2018;11:98.
   PubMed Web of Science ®Google Scholar
• Merrell BR, Walker RI, Joseph SW. In vitro and in vivo pathologic effects of Vibrio parahaemolyticus on human epithelial cells. Can J Microbiol. 1984;30(3):381–388.
   PubMed Web of Science ®Google Scholar
• Ushijima B, Hase CC, DiRita VJ. Influence of chemotaxis and swimming patterns on the virulence of the coral pathogen Vibrio coralliilyticus. J Bacteriol. 2018;200(15). e00791-17. DOI:10.1128/JB.00791-17.
   PubMed Web of Science ®Google Scholar
• Romagni JG, Meazza G, Nanayakkara NP, et al. The phytotoxic lichen metabolite, usnic acid, is a potent inhibitor of plant p -hydroxyphenylpyruvate dioxygenase. FEBS Lett. 2000;480(2–3):301–305. DOI:10.1016/S0014-5793(00)01907-4
   PubMed Web of Science ®Google Scholar
• Shabir A, Seung YL, Raees K, et al. Identification of a gene involved in the negative regulation of pyomelanin production in Ralstonia solanacearum. J Microbiol Biotechnol. 2017;27(9):1692–1700. DOI:10.4014/jmb.1705.05049
   PubMed Web of Science ®Google Scholar
• Shan C, Lu Z, Li Z, et al. 4-Hydroxyphenylpyruvate dioxygenase promotes lung cancer growth via pentose phosphate pathway (PPP) flux mediated by LKB1-AMPK/HDAC10/G6PD axis. Cell Death Dis. 2019;10(7):525. DOI:10.1038/s41419-019-1756-1
   PubMedGoogle Scholar
• Shimoji M, Figueroa RA, Neve E, et al. Molecular basis for the dual subcellular distribution of microsomal glutathione transferase 1. Biochim Biophys Acta Biomembr. 2017;1859(2):238–244. DOI:10.1016/j.bbamem.2016.11.014
   PubMed Web of Science ®Google Scholar
• Crespo M, Sole M. The use of juvenile Solea solea as sentinel in the marine platform of the Ebre Delta: in vitro interaction of emerging contaminants with the liver detoxification system. Environ Sci Pollut Res Int. 2016;23(19):19229–19236.
   PubMed Web of Science ®Google Scholar
• Liang W, Zhang W, Lv Z, et al. 4-Hydroxyphenylpyruvate dioxygenase from sea cucumber Apostichopus japonicus negatively regulates reactive oxygen species production. Fish Shellfish Immunol. 2020;101:261–268.
   PubMed Web of Science ®Google Scholar