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Gallium(III) Nitrate Inhibits Pathogenic Vibrio splendidus Vs by Interfering with the Iron Uptake Pathway

Ming Guo|Tongxiang Song|Xuelin Zhao|Yina Shao|Chenghua Li|Weiwei Zhang
한국미생물·생명공학회 (The Korean Society For Microbiology And Biotechnology)|2019.06|Journal of Microbiology and Biotechnology|제29권 제6호|pp. 973-983|DOI 10.4014/jmb.1903.03008

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참고문헌

키워드

iron uptakeVibrio splendidus VsGa(NO3)3 inhibitionHGA-melanin-mediated Fe2+ uptake
주제분류생물학

초록

It is well known that iron is critical for bacterial growth and pathogenic virulence. Due to chemical similarity, Ga3+ competes with Fe3+ for binding to compounds that usually bind Fe3+, thereby interfering with various essential biological reactions. In our present study, gallium(III) nitrate [Ga(NO3)3] could repress the growth of V. splendidus Vs without complete inhibition. In the presence of Ga(NO3)3, the secretion of homogentisic acid-melanin (HGAmelanin) in V. splendidus Vs cells could be increased by 4.8-fold, compared to that in the absence of Ga(NO3)3. HGA-melanin possessed the ability to reduce Fe3+ to Fe2+. In addition, HGA-melanin increased the mRNA levels of feoA and feoB, genes coding Fe2+ transport system proteins to 1.86- and 6.1-fold, respectively, and promoted bacterial growth to 139.2%. Similarly, the mRNA expression of feoA and feoB was upregulated 4.11-fold and 2.71-fold in the presence of 640 μM Ga(NO3)3, respectively. In conclusion, our study suggested that although Ga(NO3)3 could interfere with the growth of V. splendidus Vs, it could also stimulate both the production of Fe3+-reducing HGA-melanin and the expression of feoA and feoB , which facilitate Fe2+ transport in V. splendidus Vs.

Abstract

It is well known that iron is critical for bacterial growth and pathogenic virulence. Due to chemical similarity, Ga3+ competes with Fe3+ for binding to compounds that usually bind Fe3+, thereby interfering with various essential biological reactions. In our present study, gallium(III) nitrate [Ga(NO3)3] could repress the growth of V. splendidus Vs without complete inhibition. In the presence of Ga(NO3)3, the secretion of homogentisic acid-melanin (HGAmelanin) in V. splendidus Vs cells could be increased by 4.8-fold, compared to that in the absence of Ga(NO3)3. HGA-melanin possessed the ability to reduce Fe3+ to Fe2+. In addition, HGA-melanin increased the mRNA levels of feoA and feoB, genes coding Fe2+ transport system proteins to 1.86- and 6.1-fold, respectively, and promoted bacterial growth to 139.2%. Similarly, the mRNA expression of feoA and feoB was upregulated 4.11-fold and 2.71-fold in the presence of 640 μM Ga(NO3)3, respectively. In conclusion, our study suggested that although Ga(NO3)3 could interfere with the growth of V. splendidus Vs, it could also stimulate both the production of Fe3+-reducing HGA-melanin and the expression of feoA and feoB , which facilitate Fe2+ transport in V. splendidus Vs.

참고문헌 (52)

  1. Han QX, "A review of sea cucumber aquaculture, ranching, and stock enhancement in China", Rev. Fish. Sci. Aquac, 24, pp.326~341 (2016)
  2. Li Z, "Efficiency of a bacteriophage in controlling vibrio infection in the juvenile sea cucumber Apostichopus japonicus", Aquac, 451, pp.345~352 (2016)
  3. Zhang CY, "Isolation and identification of causative pathogen for skin ulcerative syndrome in Apostichopus japonicus", J. Fish. Sci. China, 30, pp.118~123 (2006)
  4. Kirchman DL, "Carbon versus iron limitation of bacterial growth in the California upwelling regime", Limnol. Oceanogr, 45, pp.1681~1688 (2000)
  5. Larson JA, "Replication of Neisseria meningitidis within epithelial cells requires TonB-dependent acquisition of host cell iron", Infect. Immun, 70, pp.1461~1467 (2002)
  6. Sritharan M, "Iron as a candidate in virulence and pathogenesis in mycobacteria and other microorganisms", World. J. Microiol. Biotechnol, 16, pp.769~780 (2000)
  7. Raymond KN, "Coordination chemistry and microbial iron transport", Accounts Chem. Res, 12, pp.183~190 (1979)
  8. Wandersman C, "Bacterial iron sources : from siderophores to hemophores", Annu. Rev. Microbiol, 58, pp.611~647 (2004)
  9. Méndez P, "An overview of virulence–associated factors of gram-negative fish pathogenic bacteria", Health. Environ, 5, pp.133~156 (2012)
  10. Cartron ML, "Feo--transport of ferrous iron into bacteria", Biometals, 19, pp.143~157 (2006)
  11. Robey M, "Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection", Infect. Immun, 70, pp.5659~5669 (2002)
  12. Zheng H X, "Secreted pyomelanin of Legionella pneumophila promotes bacterial iron uptake and growth under iron-limiting conditions", Infect. Immun, 81, pp.4182~4191 (2013)
  13. Zhang WW, "Inhibition of marine Vibrio sp, by pyoverdine from Pseudomonas aeruginosa PA1", J. Hazard. Mater, 302, pp.217~224 (2016)
  14. Song TX, "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, 155, pp.25~31 (2018)
  15. Ross-Gillespie A, "Gallium-mediated siderophore quenching as an evolutionarily robust antibacterial treatment", Evol. Med. Public Health, 1, pp.18~19 (2014)
  16. Rodriguez GM, "Utilization of Fe3+-acinetoferrin analogs as an iron source by Mycobacterium tuberculosis", Biometals, 21, pp.93~103 (2008)
  17. Stojiljkovic I, "Non-iron metalloporphyrins : potent antibacterial compounds that exploit haem", Hb uptake systems of pathogenic bacteria, 1999, pp.31, 429~442
  18. Minandri F, "Promises and failures of gallium as an antibacterial agent", Future Microbiol, 9, pp.379~397 (2014)
  19. Kaneko Y, "The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity", J. Clin. Invest, 117, pp.877~888 (2007)
  20. Deleon K, "Gallium maltolate treatment eradicates Pseudomonas aeruginosa infection in thermally injured mice", Antimicrob. Agents Chemother, 53, pp.1331~1337 (2009)
  21. Chitambar CR, "Gallium and its competing roles with iron in biological systems", Biochim. Biophys. Acta, 1863, pp.2044~2053 (2016)
  22. Schwyn B, "Universal chemical assay for the detection and determination of siderophores", Anal. Biochem, 160, pp.47~56 (1987)
  23. Payne SM, "Detection, isolation, and characterization of siderophores", Methods Enzymol, 235, pp.329~344 (1994)
  24. Zhu S, "Isolation and identification of a gene encoding 4-hydroxyphenylpyruvate dioxygenase from the red-brown pigment-producing bacterium Alteromonas stellipolaris LMG 21856", Folia Microbiol, 60, pp.1~8 (2015)
  25. Chatfield CH, "The secreted pyomelanin pigment of Legionella pneumophila confers ferric reductase activity", Infect. Immun, 75, pp.4062~4070 (2007)
  26. Brewster JD, "A simple micro-growth assay for enumerating bacteria", J. Microbiol. Methods, 53, pp.77~86 (2003)
  27. Zhang WW, "Characterization of DegQVh, a serine protease and a protective immunogen from a pathogenic Vibrio harveyi strain", Appl. Environ. Microbiol, 74, pp.6254~6262 (2008)
  28. Torresi M, "Detection of Vibrio splendidus and related species in Chamelea gallina sampled in the Adriatic along the Abruzzi coastline", Vet. Ital, 47, pp.371~378 (2011)
  29. Olakanmi O, "Gallium disrupts iron metabolism of mycobacteria residing within human macrophages", Infect. Immun, 68, pp.5619~5627 (2000)
  30. Banin E, "The potential of desferrioxaminegallium as an anti-pseudomonas therapeutic agent", Proc. Natl. Acad. Sci. USA, 105, pp.16761~16766 (2008)
  31. Menon S, "Studies on gallium accumulation in inflammatory lesions: II, Uptake by Staphylococcus aureus: concise communication", J. Nucl. Med, 19, pp.44~47 (1978)
  32. Antunes LCS, "In vitro and in vivo antimicrobial activities of gallium nitrate against multidrug-resistant Acinetobacter baumannii", Antimicrob. Agents Chemother, 56, pp.5961~5970 (2012)
  33. Harrington JR, "Antimicrobial activity of gallium against virulent Rhodococcus equiin vitro and in vivo", J. Vet. Pharmacol. Ther, 29, pp.121~127 (2006)
  34. Fecteau ME, "Comparison of the antimicrobial activities of gallium nitrate and gallium maltolate against Mycobacterium avium subsp, paratuberculosis in vitro", Vet. J, 202, pp.195~197 (2014)
  35. Oyebode Olakanmi, "Gallium nitrate is efficacious in murine models of tuberculosis and inhibits key bacterial Fe-dependent enzymes", Antimicrob. Agents Chemother, 57, pp.6074~6080 (2013)
  36. Mitchell G, "Evaluation of gallium citrate formulations against a multidrug-resistant strain of Klebsiella pneumoniae in a murine wound model of infection", Antimicrob. Agents Chemother, 59, pp.6484~6493 (2015)
  37. Xu ZR, "Antimicrobial effect of gallium nitrate against bacteria encountered in burn wound infections", Rsc. Adv, 7, pp.52266~52273 (2017)
  38. Emery T, "Role of ferrichrome as a ferric ionophore in Ustilago sphaerogena", Biochemistry, 10, pp.1483~1488 (1971)
  39. Leong J, "Coordination isomers of biological iron transport compounds III, (1) Transport of λ-cis-chromic desferriferrichrome by Ustilago sphaerogena", Biochem. Biophys. Res. Commun, 60, pp.1066~1071 (1974)
  40. Yabuuchi E, "Characterization of"pyomelanin"-producing strains of Pseudomonas aeruginosa", Int. J. Syst. Bacteriol, 22, pp.53~64 (1972)
  41. Ogunnariwo J, "Brown-and redpigmented Pseudomonas aeruginosa : differentiation between melanin and pyorubrin", J. Med. Microbiol, 8, pp.199~203 (1975)
  42. Coon SL, "Homogentisic acid is the product of MelA, which mediates melanogenesis in the marine bacterium Shewanella colwelliana D", Appl. Environ. Microbiol, 60, pp.3006~3010 (1994)
  43. David C, "Formation of polymeric pigments in the presence of bacteria and comparison with chemical oxidative coupling-II, Catabolism of tyrosine and hydroxyphenylacetic acid by Alcaligenes eutrophus CH34 and mutants", Eur. Polym. J, 32, pp.669~697 (1996)
  44. Zughaier SM, "A melanin pigment purified from an epidemic strain of Burkholderia cepacia attenuates monocyte respiratory burst activity by scavenging superoxide anion", Infect. Immun, 67, pp.908~913 (1999)
  45. Steinert M, "The Lly protein is essential for p-hydroxyphenylpyruvate dioxygenase activity in Legionella pneumophila", FEMS. Microbiol. Lett, 203, pp.41~47 (2001)
  46. Turick CE, "The role of 4-hydroxyphenylpyruvate dioxygenase in enhancement of solid-phase electron tra by Shewanella oneidensis MR-1", FEMS. Microbiol. Ecol, 68, pp.223~235 (2009)
  47. Turick CE, "Pyomelanin is produced by Shewanella algae BrY and affected by exogenous iron", Can. J. Microbiol, 54, pp.334~339 (2008)
  48. Stojiljkovic I, "Escherichia coli K12 ferrous iron uptake mutants are impaired in their ability to colonize the mouse intestine", FEMS. Microbiol. Lett, 108, pp.111~115 (1993)
  49. Tsolis RM, "Contribution of TonB-and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse", Infect. Immun, 64, pp.4549~4556 (1996)
  50. Troxell B, "Transcriptional regulation by Ferric Uptake Regulator(Fur)in pathogenic bacteria", Front. Cell Infect. Microbiol, 3, pp.59~ (2013)
  51. Mey AR, "Iron and fur regulation in Vibrio cholerae and the role of fur in virulence", Infect. Immun, 73, pp.8167~8178 (2005)
  52. Aranda J, "Contribution of the FeoB transporter to Streptococcus suis virulence", Int. Microbiol, 12, pp.137~143 (2009)

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