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Amphi-enterobactin commonly produced among Vibrio campbellii and Vibrio harveyi strains can be taken up by a novel outer membrane protein FapA that also can transport canonical Fe(III)-enterobactin

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A Correction to this article was published on 05 October 2018

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Abstract

Vibrio campbellii BAA-1116 (formerly Vibrio harveyi) is a model organism for quorum sensing study and produces the siderophores anguibactin and amphi-enterobactin. This study examined the mechanisms and specificity of siderophore uptake in V. campbellii and V. harveyi, and surveyed the diversity of siderophore production in V. campbellii and V. harveyi strains. The amphi-enterobactin gene cluster of BAA-1116 harbors a gene, named fapA, that is a homologue of genes encoding Fe(III)-siderophore-specific outer membrane receptors. Another strain, V. campbellii HY01, a strain pathogenic to shrimp, also carries this cluster including fapA. Our siderophore bioassay results using HY01-derived indicator strains show that the FapA protein localized in the outer membrane fraction of V. campbellii HY01 is essential for the uptake of Fe(III)-amphi-enterobactin as well as exogenous siderophores, including enterobactin from E. coli, but not vanchrobactin from V. anguillarum RV22 while Fe(III)-amphi-enterobactin can be utilized by V. anguillarum. Electrospray ionization mass spectrometry as well as bioassay revealed that various V. campbellii and V. harveyi strains produce a suite of amphi-enterobactins with various fatty acid appendages, including several novel amphi-enterobactins, and these amphi-enterobactins can be taken up by V. campbellii HY01 via FapA, indicating that amphi-enterobactin production is a common phenotype among V. campbellii and V. harveyi, whereas our previous work, confirmed herein, showed that anguibactin is only produced by V. campbellii strains. These results along with the additional finding that a 2,3-dihydroxybenzoic acid biosynthesis gene, aebA, located in the amphi-enterobactin gene cluster, is essential for both anguibactin and amphi-enterobactin biosynthesis, suggest the possibility that amphi-enterobactin is a native siderophore of V. campbellii and V. harveyi, while the anguibactin system has been acquired by V. campbellii during evolution.

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Change history

  • 05 October 2018

    In the original publication, third author’s name was incorrectly published as Aneta L. Jelowicki.

References

  1. Crichton R (2016) Iron metabolism: from molecular mechanisms to clinical consequences. Wiley, New York

    Book  Google Scholar 

  2. Crosa JH, Walsh CT (2002) Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev 66:223–249

    Article  CAS  Google Scholar 

  3. Crosa JH, Mey AR, Payne SM (2004) Iron transport in bacteria. ASM Press, Washington, D.C.

    Book  Google Scholar 

  4. Owens L, Busico-Salcedo N (2006) Vibrio harveyi: pretty problems in paradise. In: Thompson FL, Austin B, Swings J (eds) The biology of vibrios. ASM Press, Washington, D.C., pp 266–280

    Chapter  Google Scholar 

  5. Austin B, Zhang X (2006) Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol 43:119–124

    Article  CAS  Google Scholar 

  6. Wang L, Chen Y, Huang H, Huang Z, Chen H, Shao Z (2015) Isolation and identification of Vibrio campbellii as a bacterial pathogen for luminous vibriosis of Litopenaeus vannamei. Aquac Res 46:395–404

    Article  CAS  Google Scholar 

  7. Phuoc LH, Corteel M, Nauwynck HJ, Pensaert MB, Alday-Sanz V, Van den Broeck W, Sorgeloos P, Bossier P (2008) Increased susceptibility of white spot syndrome virus-infected Litopenaeus vannamei to Vibrio campbellii. Environ Microbiol 10:2718–2727

    Article  CAS  Google Scholar 

  8. Liu J, Zhao Z, Deng Y, Shi Y, Liu Y, Wu C, Luo P, Hu C (2017) Complete genome sequence of Vibrio campbellii LMB 29 isolated from red drum with four native megaplasmids. Front Microbiol 8:2035

    Article  Google Scholar 

  9. Gomez-Gil B, Soto-Rodríguez S, García-Gasca A, Roque A, Vazquez-Juarez R, Thompson FL, Swings J (2004) Molecular identification of Vibrio harveyi-related isolates associated with diseased aquatic organisms. Microbiology 150:1769–1777

    Article  CAS  Google Scholar 

  10. Lin B, Wang Z, Malanoski AP, O’Grady EA, Wimpee CF, Vuddhakul V, Alves N, Thompson FL, Gomez-Gil B, Vora GJ (2010) Comparative genomic analyses identify the Vibrio harveyi genome sequenced strains BAA-1116 and HY01 as Vibrio campbellii. Environ Microbiol Rep 2:81–89

    Article  CAS  Google Scholar 

  11. Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222

    Article  CAS  Google Scholar 

  12. Papenfort K, Bassler BL (2016) Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol 14:576–588

    Article  CAS  Google Scholar 

  13. Espinoza-Valles I, Vora GJ, Lin B, Leekitcharoenphon P, González-Castillo A, Ussery D, Høj L, Gomez-Gil B (2015) Unique and conserved genome regions in Vibrio harveyi and related species in comparison with the shrimp pathogen Vibrio harveyi CAIM 1792. Microbiology 161:1762–1779

    Article  CAS  Google Scholar 

  14. Ke HM, Prachumwat A, Yu CP, Yang YT, Promsri S, Liu KF, Lo CF, Lu MJ, Lai MC, Tsai IJ, Li WH (2017) Comparative genomics of Vibrio campbellii strains and core species of the Vibrio Harveyi clade. Sci Rep 7:41394

    Article  CAS  Google Scholar 

  15. Urbanczyk H, Ogura Y, Hayashi T (2013) Taxonomic revision of Harveyi clade bacteria (family Vibrionaceae) based on analysis of whole genome sequences. Int J Syst Evol Microbiol 63:2742–2751

    Article  Google Scholar 

  16. Zane HK, Naka H, Rosconi F, Sandy M, Haygood MG, Butler A (2014) Biosynthesis of amphi-enterobactin siderophores by Vibrio harveyi BAA-1116: identification of a bifunctional nonribosomal peptide synthetase condensation domain. J Am Chem Soc 136:5615–5618

    Article  CAS  Google Scholar 

  17. Naka H, Actis LA, Crosa JH (2013) The anguibactin biosynthesis and transport genes are encoded in the chromosome of Vibrio harveyi: a possible evolutionary origin for the pJM1 plasmid-encoded system of Vibrio anguillarum. MicrobiologyOpen 2:182–194

    Article  CAS  Google Scholar 

  18. Crosa JH (1980) A plasmid associated with virulence in the marine fish pathogen Vibrio anguillarum specifies an iron-sequestering system. Nature 284:566–568

    Article  CAS  Google Scholar 

  19. Naka H, Crosa JH (2011) Genetic determinants of virulence in the marine fish pathogen Vibrio anguillarum. Fish Pathol 46:1–10

    Article  Google Scholar 

  20. Sandy M, Han A, Blunt J, Munro M, Haygood M, Butler A (2010) Vanchrobactin and anguibactin siderophores produced by Vibrio sp. DS40M4. J Nat Prod 73:1038–1043

    Article  CAS  Google Scholar 

  21. Soengas RG, Anta C, Espada A, Paz V, Ares IR, Balado M, Rodriguez J, Lemos ML, Jimenez C (2006) Structural characterization of vanchrobactin, a new catechol siderophore produced by the fish pathogen Vibrio anguillarum serotype O2. Tetrahedron Lett 47:7113–7116

    Article  CAS  Google Scholar 

  22. Soengas RG, Anta C, Espada A, Nieto RM, Larrosa M, Rodríguez J, Jiménez C (2007) Vanchrobactin: absolute configuration and total synthesis. Tetrahedron Lett 48:3021–3024

    Article  CAS  Google Scholar 

  23. Reitz ZL, Sandy M, Butler A (2017) Biosynthetic considerations of triscatechol siderophores framed on serine and threonine macrolactone scaffolds. Metallomics 9:824–839

    Article  CAS  Google Scholar 

  24. Thode SK, Rojek E, Kozlowski M, Ahmad R, Haugen P (2018) Distribution of siderophore gene systems on a Vibrionaceae phylogeny: database searches, phylogenetic analyses and evolutionary perspectives. PLoS One 13:e0191860

    Article  Google Scholar 

  25. Taga ME, Xavier KB (2011) Methods for analysis of bacterial autoinducer-2 production. Curr Protoc Microbiol Chapter 1(Unit1C):1

    Google Scholar 

  26. Rogers HJ (1973) Iron-binding catechols and virulence in Escherichia coli. Infect Immun 7:445–456

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Senanayake SD, Brian DA (1995) Precise large deletions by the PCR-based overlap extension method. Mol Biotechnol 4:13–15

    Article  CAS  Google Scholar 

  28. Naka H, Crosa JH (2012) Identification and characterization of a novel outer membrane protein receptor FetA for ferric enterobactin transport in Vibrio anguillarum 775 (pJM1). Biometals 25:125–133

    Article  CAS  Google Scholar 

  29. Arnow LE (1937) Colorimetric determination of the components of 3, 4-dihydroxyphenylalanine-tyrosine mixtures. J Biol Chem 118:531–537

    CAS  Google Scholar 

  30. Naka H, López CS, Crosa JH (2008) Reactivation of the vanchrobactin siderophore system of Vibrio anguillarum by removal of a chromosomal insertion sequence originated in plasmid pJM1 encoding the anguibactin siderophore system. Environ Microbiol 10:265–277

    CAS  PubMed  Google Scholar 

  31. Naka H, Liu M, Actis LA, Crosa JH (2013) Plasmid- and chromosome-encoded siderophore anguibactin systems found in marine vibrios: biosynthesis, transport and evolution. Biometals 26:537–547

    Article  CAS  Google Scholar 

  32. Penwell WF, Arivett BA, Actis LA (2012) The Acinetobacter baumannii entA gene located outside the acinetobactin cluster is critical for siderophore production, iron acquisition and virulence. PLoS One 7:e36493

    Article  CAS  Google Scholar 

  33. Balado M, Souto A, Vences A, Careaga VP, Valderrama K, Segade Y, Rodríguez J, Osorio CR, Jiménez C, Lemos ML (2015) Two catechol siderophores, acinetobactin and amonabactin, are simultaneously produced by Aeromonas salmonicida subsp. salmonicida sharing part of the biosynthetic pathway. ACS Chem Biol 10:2850–2860

    Article  CAS  Google Scholar 

  34. McRose DL, Baars O, Seyedsayamdost MR, Morel FMM (2018) Quorum sensing and iron regulate a two-for-one siderophore gene cluster in Vibrio harveyi. Proc Natl Acad Sci USA (in press). https://doi.org/10.1073/pnas.1805791115

    Article  Google Scholar 

  35. Wyckoff EE, Allred BE, Raymond KN, Payne SM (2015) Catechol siderophore transport by Vibrio cholerae. J Bacteriol 197:2840–2849

    Article  CAS  Google Scholar 

  36. Sandy M, Butler A (2009) Microbial iron acquisition: marine and terrestrial siderophores. Chem Rev 109:4580–4595

    Article  CAS  Google Scholar 

  37. Vraspir JM, Butler A (2009) Chemistry of marine ligands and siderophores. Ann Rev Mar Sci 1:43–63

    Article  Google Scholar 

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Acknowledgements

The research reported here made use of the shared facilities of the UCSB MRSEC (NSF DMR 1720256). We would like to thank the late Professor Jorge Crosa for his valuable suggestions. This work was supported by NSF CHE-171076 (AB).

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Correspondence to Margo G. Haygood.

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Naka, H., Reitz, Z.L., Jelowicki, A.L. et al. Amphi-enterobactin commonly produced among Vibrio campbellii and Vibrio harveyi strains can be taken up by a novel outer membrane protein FapA that also can transport canonical Fe(III)-enterobactin. J Biol Inorg Chem 23, 1009–1022 (2018). https://doi.org/10.1007/s00775-018-1601-5

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  • DOI: https://doi.org/10.1007/s00775-018-1601-5

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