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Front Microbiol. 2021 Dec 15;12:782673. doi: 10.3389/fmicb.2021.782673. eCollection 2021.

Secretion Systems in Gram-Negative Bacterial Fish Pathogens.

Frontiers in microbiology

Sophanit Mekasha, Dirk Linke

Affiliations

  1. Section for Genetics and Evolutionary Biology, Department of Biosciences, University of Oslo, Oslo, Norway.

PMID: 34975803 PMCID: PMC8714846 DOI: 10.3389/fmicb.2021.782673

Abstract

Bacterial fish pathogens are one of the key challenges in the aquaculture industry, one of the fast-growing industries worldwide. These pathogens rely on arsenal of virulence factors such as toxins, adhesins, effectors and enzymes to promote colonization and infection. Translocation of virulence factors across the membrane to either the extracellular environment or directly into the host cells is performed by single or multiple dedicated secretion systems. These secretion systems are often key to the infection process. They can range from simple single-protein systems to complex injection needles made from dozens of subunits. Here, we review the different types of secretion systems in Gram-negative bacterial fish pathogens and describe their putative roles in pathogenicity. We find that the available information is fragmented and often descriptive, and hope that our overview will help researchers to more systematically learn from the similarities and differences between the virulence factors and secretion systems of the fish-pathogenic species described here.

Copyright © 2021 Mekasha and Linke.

Keywords: Gram-negative; aquaculture; fish disease; fish pathogen; secretion system; virulence factor

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Fish Shellfish Immunol. 2010 Apr;28(4):672-7 - PubMed
  2. Appl Environ Microbiol. 2005 Dec;71(12):8434-41 - PubMed
  3. BMC Genomics. 2017 Jul 12;18(1):528 - PubMed
  4. Microbiol Spectr. 2016 Apr;4(2): - PubMed
  5. BMC Genomics. 2008 Sep 18;9:427 - PubMed
  6. Infect Immun. 2004 Mar;72(3):1248-56 - PubMed
  7. J Appl Bacteriol. 1990 Jul;69(1):1-16 - PubMed
  8. PLoS One. 2013 Nov 20;8(11):e80943 - PubMed
  9. Biol Met. 1989;2(3):155-60 - PubMed
  10. Curr Opin Cell Biol. 2000 Aug;12(4):420-30 - PubMed
  11. Syst Appl Microbiol. 2003 Mar;26(1):127-31 - PubMed
  12. J Bacteriol. 2005 Apr;187(8):2628-37 - PubMed
  13. Res Microbiol. 2012 Sep-Oct;163(8):557-66 - PubMed
  14. Fish Shellfish Immunol. 2009 Dec;27(6):721-8 - PubMed
  15. Appl Environ Microbiol. 2017 Nov 16;83(23): - PubMed
  16. Infect Immun. 2015 Apr;83(4):1650-60 - PubMed
  17. J Appl Microbiol. 2008 Apr;104(4):944-51 - PubMed
  18. Biochim Biophys Acta. 2010 Jun;1798(6):1073-80 - PubMed
  19. Curr Opin Microbiol. 2015 Dec;28:72-7 - PubMed
  20. Appl Environ Microbiol. 2011 Nov;77(21):7656-62 - PubMed
  21. Microbiology (Reading). 2010 Sep;156(Pt 9):2864-2872 - PubMed
  22. Infect Immun. 1998 Jul;66(7):3134-41 - PubMed
  23. PLoS One. 2012;7(3):e33725 - PubMed
  24. Front Microbiol. 2011 May 30;2:93 - PubMed
  25. Vet Res. 2013 Apr 24;44:27 - PubMed
  26. Cell Rep. 2012 May 31;1(5):453-60 - PubMed
  27. J Nat Toxins. 2000 Aug;9(3):281-97 - PubMed
  28. Int J Med Microbiol. 2015 Feb;305(2):276-82 - PubMed
  29. FEMS Microbiol Lett. 1993 Aug 1;111(2-3):275-80 - PubMed
  30. FEMS Microbiol Lett. 1996 Jun 1;139(2-3):97-101 - PubMed
  31. Proc Natl Acad Sci U S A. 2011 Jul 12;108(28):11614-9 - PubMed
  32. J Appl Microbiol. 2008 Nov;105(5):1441-51 - PubMed
  33. Environ Microbiol. 2007 Feb;9(2):370-82 - PubMed
  34. Appl Microbiol Biotechnol. 2014 Jun;98(11):4937-48 - PubMed
  35. Biochem J. 1992 Feb 1;281 ( Pt 3):703-8 - PubMed
  36. Microb Pathog. 2021 Aug;157:104965 - PubMed
  37. Appl Environ Microbiol. 2003 Sep;69(9):5275-80 - PubMed
  38. Front Cell Infect Microbiol. 2017 Jul 25;7:342 - PubMed
  39. Nature. 1991 May 30;351(6325):371-7 - PubMed
  40. Mol Microbiol. 2001 Jul;41(2):439-50 - PubMed
  41. Microb Pathog. 2006 May;40(5):198-210 - PubMed
  42. J Appl Microbiol. 2007 Aug;103(2):289-96 - PubMed
  43. Front Microbiol. 2019 May 31;10:1163 - PubMed
  44. J Gen Microbiol. 1993 Feb;139(2):245-9 - PubMed
  45. J Fish Dis. 2016 May;39(5):565-76 - PubMed
  46. Mol Microbiol. 1996 Feb;19(3):625-37 - PubMed
  47. Nat Biotechnol. 2007 Jul;25(7):763-9 - PubMed
  48. J Fish Dis. 2005 Jul;28(7):391-8 - PubMed
  49. Int J Biochem Cell Biol. 2007;39(10):1771-5 - PubMed
  50. Infect Immun. 2006 Jan;74(1):765-8 - PubMed
  51. Microb Pathog. 2020 Feb 10;142:104053 - PubMed
  52. Front Cell Infect Microbiol. 2019 Mar 29;9:81 - PubMed
  53. World J Microbiol Biotechnol. 2018 May 11;34(5):68 - PubMed
  54. Microbiology (Reading). 2006 Jun;152(Pt 6):1847-1856 - PubMed
  55. Cold Spring Harb Perspect Biol. 2010 May;2(5):a000414 - PubMed
  56. J Appl Microbiol. 2003;94(6):1120-7 - PubMed
  57. FEMS Microbiol Lett. 1992 Nov 15;78(1):65-71 - PubMed
  58. Microbiology (Reading). 2007 Feb;153(Pt 2):483-489 - PubMed
  59. Infect Immun. 1992 Aug;60(8):3072-8 - PubMed
  60. EMBO Rep. 2001 May;2(5):376-81 - PubMed
  61. J Am Chem Soc. 2014 Apr 16;136(15):5615-8 - PubMed
  62. Proc Natl Acad Sci U S A. 2018 Apr 17;115(16):E3779-E3787 - PubMed
  63. Nat Rev Microbiol. 2020 Jan;18(1):47-59 - PubMed
  64. Front Microbiol. 2016 Dec 20;7:2003 - PubMed
  65. Dis Aquat Organ. 2009 Mar 9;84(1):25-33 - PubMed
  66. Curr Top Microbiol Immunol. 2001;257:35-52 - PubMed
  67. Dis Aquat Organ. 2010 Jun 11;90(2):121-7 - PubMed
  68. J Fish Dis. 2006 Jun;29(6):339-46 - PubMed
  69. Appl Environ Microbiol. 2015 Sep 1;81(17):5867-79 - PubMed
  70. Infect Immun. 2009 May;77(5):1723-33 - PubMed
  71. Appl Environ Microbiol. 2008 Apr;74(8):2341-8 - PubMed
  72. Infect Immun. 2008 Jun;76(6):2620-32 - PubMed
  73. Microbiology (Reading). 2013 Sep;159(Pt 9):1937-1945 - PubMed
  74. Microbiologyopen. 2013 Feb;2(1):182-94 - PubMed
  75. Sci Rep. 2015 May 27;5:9833 - PubMed
  76. J Biosci. 2007 Dec;32(7):1331-44 - PubMed
  77. Gene. 1997 Jun 11;192(1):141-7 - PubMed
  78. Front Cell Infect Microbiol. 2020 Jan 09;9:426 - PubMed
  79. Appl Environ Microbiol. 2015 Feb;81(3):1157-67 - PubMed
  80. J Bacteriol. 2003 Nov;185(22):6583-91 - PubMed
  81. J Biol Chem. 2017 Oct 13;292(41):17129-17143 - PubMed
  82. J Bacteriol. 2020 Nov 19;202(24): - PubMed
  83. J Appl Microbiol. 2007 Nov;103(5):1461-70 - PubMed
  84. Microbiol Res. 2019 May;222:43-51 - PubMed
  85. Vet Microbiol. 2013 Oct 25;166(3-4):659-63 - PubMed
  86. Biochim Biophys Acta. 2014 Aug;1843(8):1568-77 - PubMed
  87. Mol Microbiol. 2011 Jun;80(6):1420-38 - PubMed
  88. Fish Shellfish Immunol. 2008 Jan;24(1):134-41 - PubMed
  89. FEMS Microbiol Lett. 2008 Nov;288(2):216-20 - PubMed
  90. J Fish Dis. 2006 Nov;29(11):683-90 - PubMed
  91. Arch Microbiol. 2007 Oct;188(4):433-9 - PubMed
  92. Int J Evol Biol. 2012;2012:457264 - PubMed
  93. J Bacteriol. 2005 Oct;187(20):6943-52 - PubMed
  94. Infect Immun. 1998 May;66(5):1990-8 - PubMed
  95. J Aquat Anim Health. 2007 Mar;19(1):35-40 - PubMed
  96. Mol Microbiol. 2021 Mar;115(3):345-355 - PubMed
  97. Vet Microbiol. 2009 May 12;136(3-4):326-34 - PubMed
  98. Front Microbiol. 2019 Jan 09;9:3216 - PubMed
  99. Appl Environ Microbiol. 2007 Dec;73(24):7934-46 - PubMed
  100. Infect Immun. 1985 Apr;48(1):146-52 - PubMed
  101. FEMS Microbiol Lett. 1996 Jul 15;141(1):19-23 - PubMed
  102. Front Microbiol. 2017 Oct 12;8:1983 - PubMed
  103. J Exp Zool. 2002 Aug 1;293(3):284-301 - PubMed
  104. J Infect Dis. 2011 May 15;203(10):1369-77 - PubMed
  105. Fish Shellfish Immunol. 2009 Jun;26(6):877-84 - PubMed
  106. Chem Commun (Camb). 2008 Nov 7;(41):5119-21 - PubMed
  107. J Biol Chem. 2011 Nov 11;286(45):39417-30 - PubMed
  108. Arch Microbiol. 2008 Oct;190(4):439-49 - PubMed
  109. Vet Res. 2015 Jan 13;46:1 - PubMed
  110. Fish Shellfish Immunol. 2004 May;16(5):645-58 - PubMed
  111. Vet Res. 2019 Oct 2;50(1):76 - PubMed
  112. Annu Rev Microbiol. 2014;68:415-38 - PubMed
  113. Microbiology (Reading). 2008 Apr;154(Pt 4):1144-1151 - PubMed
  114. J Bacteriol. 2005 Jan;187(2):752-7 - PubMed
  115. Nat Rev Microbiol. 2021 Sep;19(9):567-584 - PubMed
  116. Microb Cell Fact. 2018 Dec 20;17(1):196 - PubMed
  117. J Appl Microbiol. 2013 Mar;114(3):644-54 - PubMed
  118. Microb Pathog. 2005 Oct;39(4):109-19 - PubMed
  119. J Bacteriol. 2012 May;194(10):2763-4 - PubMed
  120. Science. 2010 Sep 24;329(5999):1660-2 - PubMed
  121. Infect Immun. 2001 Apr;69(4):2569-79 - PubMed
  122. J Bacteriol. 2005 Apr;187(7):2257-60 - PubMed
  123. Mol Microbiol. 1998 Dec;30(5):933-41 - PubMed
  124. Microb Pathog. 2020 Feb;139:103900 - PubMed
  125. DNA Cell Biol. 2009 Aug;28(8):383-8 - PubMed
  126. Microb Biotechnol. 2014 Sep;7(5):381-400 - PubMed
  127. Vet Microbiol. 2016 Jun 30;189:68-74 - PubMed
  128. Microb Pathog. 2018 Dec;125:276-280 - PubMed
  129. Cell Tissue Res. 2004 Nov;318(2):305-11 - PubMed
  130. Dis Aquat Organ. 2013 Oct 11;106(2):129-38 - PubMed
  131. Dis Aquat Organ. 2005 Apr 18;64(2):107-19 - PubMed
  132. Can J Microbiol. 1981 Oct;27(10):1114-22 - PubMed
  133. Int J Med Microbiol. 2013 Dec;303(8):563-73 - PubMed
  134. FEMS Microbiol Lett. 1996 Jan 15;135(2-3):265-70 - PubMed
  135. Microbes Infect. 2002 Mar;4(3):279-83 - PubMed
  136. FEMS Microbiol Lett. 1997 Sep 1;154(1):1-7 - PubMed
  137. Arch Microbiol. 1996 Jan;165(1):9-17 - PubMed
  138. Vet Res. 2012 Oct 04;43:67 - PubMed
  139. Mol Microbiol. 1996 Dec;22(5):991-1003 - PubMed
  140. FEMS Microbiol Lett. 2002 Mar 5;208(2):245-51 - PubMed
  141. FEMS Microbiol Lett. 2020 Nov 5;367(20): - PubMed
  142. Infect Immun. 1996 Jul;64(7):2643-8 - PubMed
  143. Infect Immun. 2003 Jun;71(6):3329-36 - PubMed
  144. Lett Appl Microbiol. 2008 Jun;46(6):605-12 - PubMed
  145. J Fish Dis. 2003 Oct;26(10):563-74 - PubMed
  146. Infect Immun. 1998 Dec;66(12):5731-42 - PubMed
  147. Mol Microbiol. 1991 Feb;5(2):401-7 - PubMed
  148. Appl Environ Microbiol. 1998 Nov;64(11):4269-75 - PubMed
  149. J Bacteriol. 2002 Apr;184(7):1851-8 - PubMed
  150. Front Cell Infect Microbiol. 2019 Feb 27;9:38 - PubMed
  151. J Bacteriol. 2003 Nov;185(22):6648-57 - PubMed
  152. Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):13001-6 - PubMed
  153. Curr Genet. 2016 May;62(2):379-82 - PubMed
  154. J Fish Dis. 2013 Aug;36(8):703-9 - PubMed
  155. Int J Syst Bacteriol. 1992 Jan;42(1):120-6 - PubMed
  156. Vet Microbiol. 2013 Mar 23;162(2-4):858-865 - PubMed
  157. Infect Immun. 1993 Jun;61(6):2486-92 - PubMed
  158. Front Immunol. 2015 Jun 02;6:262 - PubMed
  159. J Bacteriol. 2005 Sep;187(17):5984-95 - PubMed
  160. BMC Res Notes. 2013 Jul 26;6:297 - PubMed
  161. Infect Immun. 1990 Jul;58(7):2127-32 - PubMed
  162. Lett Appl Microbiol. 2007 Aug;45(2):115-20 - PubMed
  163. J Bacteriol. 2002 Feb;184(4):936-46 - PubMed
  164. Annu Rev Microbiol. 2002;56:289-314 - PubMed
  165. J Fish Dis. 2006 Oct;29(10):601-9 - PubMed
  166. Microb Pathog. 2020 Dec;149:104503 - PubMed
  167. Vet Microbiol. 2015 Jun 12;177(3-4):332-40 - PubMed
  168. Fish Shellfish Immunol. 2012 Sep;33(3):514-21 - PubMed
  169. Appl Environ Microbiol. 2005 Nov;71(11):6947-53 - PubMed
  170. J Appl Microbiol. 2005;98(5):1011-9 - PubMed
  171. J Fish Dis. 2017 Jan;40(1):73-82 - PubMed
  172. Nat Commun. 2020 Jan 13;11(1):241 - PubMed
  173. Infect Immun. 2017 Apr 21;85(5): - PubMed
  174. Virulence. 2019 Dec;10(1):839-848 - PubMed
  175. Appl Environ Microbiol. 2001 Jun;67(6):2436-44 - PubMed
  176. Biometals. 2002 Jun;15(2):153-60 - PubMed
  177. Front Microbiol. 2015 Jul 28;6:763 - PubMed
  178. Front Cell Infect Microbiol. 2013 Apr 30;3:15 - PubMed
  179. J Biol Inorg Chem. 2018 Oct;23(7):1009-1022 - PubMed
  180. Immunobiology. 2006;211(4):283-93 - PubMed
  181. Appl Environ Microbiol. 1986 Jan;51(1):101-4 - PubMed
  182. Front Cell Infect Microbiol. 2018 Oct 30;8:373 - PubMed
  183. Front Microbiol. 2017 Jul 25;8:1375 - PubMed
  184. J Bacteriol. 2006 Dec;188(23):8272-82 - PubMed
  185. Infect Genet Evol. 2017 Oct;54:7-17 - PubMed
  186. J Exp Med. 2009 Dec 21;206(13):3073-88 - PubMed
  187. Appl Environ Microbiol. 2001 Jun;67(6):2430-5 - PubMed
  188. FEMS Microbiol Rev. 2014 Jul;38(4):660-97 - PubMed
  189. Trends Microbiol. 2007 Oct;15(10):456-61 - PubMed
  190. Infect Immun. 2010 Apr;78(4):1772-80 - PubMed
  191. Sci Rep. 2016 Mar 16;6:23080 - PubMed
  192. Mol Biol Cell. 2005 Sep;16(9):4108-23 - PubMed
  193. J Appl Bacteriol. 1973 Jun;36(2):227-32 - PubMed
  194. J Bacteriol. 2007 Mar;189(6):2575-9 - PubMed
  195. Dis Aquat Organ. 2003 Jul 8;55(2):101-7 - PubMed
  196. Nat Rev Microbiol. 2012 Jun 11;10(7):483-96 - PubMed
  197. Dev Comp Immunol. 1987 Summer;11(3):529-37 - PubMed
  198. N Engl J Med. 2001 Apr 5;344(14):1058-66 - PubMed
  199. Mol Microbiol. 2012 Jul;85(2):225-38 - PubMed
  200. Biochim Biophys Acta. 2014 Aug;1843(8):1629-41 - PubMed
  201. J Bacteriol. 1998 Feb;180(3):505-13 - PubMed
  202. PLoS One. 2019 Aug 29;14(8):e0221018 - PubMed
  203. Infect Immun. 2000 Jun;68(6):3233-41 - PubMed
  204. Microb Pathog. 1996 Sep;21(3):173-82 - PubMed
  205. Vet Microbiol. 2012 Aug 17;158(3-4):436-42 - PubMed
  206. Dis Aquat Organ. 1998 Nov 30;34(3):161-6 - PubMed
  207. J Bacteriol. 1992 Nov;174(22):7235-44 - PubMed
  208. J Fish Dis. 2003 Jan;26(1):55-8 - PubMed
  209. Microbiol Mol Biol Rev. 1998 Jun;62(2):379-433 - PubMed
  210. Vet Microbiol. 2016 Feb 29;184:94-101 - PubMed
  211. PLoS One. 2015 Jul 29;10(7):e0134098 - PubMed
  212. Inorg Chem. 1998 Sep 7;37(18):4578-4583 - PubMed
  213. Biochemistry. 2016 Feb 16;55(6):884-93 - PubMed
  214. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6332-6 - PubMed
  215. Microbiol Spectr. 2016 Feb;4(1): - PubMed
  216. Front Microbiol. 2018 Dec 13;9:2996 - PubMed
  217. J Biol Chem. 1991 Aug 15;266(23):15258-65 - PubMed
  218. Dis Aquat Organ. 1998 May 14;33(1):73-5 - PubMed
  219. Microbiology (Reading). 2005 Jul;151(Pt 7):2301-2313 - PubMed
  220. Microbiology (Reading). 2002 Jul;148(Pt 7):2233-2243 - PubMed
  221. J Bacteriol. 2004 Dec;186(23):8137-43 - PubMed
  222. Fish Shellfish Immunol. 2009 Sep;27(3):469-77 - PubMed
  223. Bioinformatics. 2007 Jan 1;23(1):127-8 - PubMed
  224. J Microbiol. 2012 Oct;50(5):719-25 - PubMed
  225. Biol Pharm Bull. 2006 May;29(5):911-8 - PubMed
  226. Infect Immun. 2011 Nov;79(11):4617-27 - PubMed
  227. PLoS One. 2009 Oct 29;4(10):e7646 - PubMed
  228. FEMS Microbiol Lett. 2003 Sep 26;226(2):273-9 - PubMed
  229. Front Immunol. 2017 Dec 07;8:1706 - PubMed
  230. Int J Syst Evol Microbiol. 2014 Feb;64(Pt 2):406-412 - PubMed
  231. Dis Aquat Organ. 2003 Aug 15;56(1):25-30 - PubMed
  232. J Bacteriol. 1989 Apr;171(4):1811-6 - PubMed
  233. Appl Environ Microbiol. 2004 Sep;70(9):5199-207 - PubMed
  234. Microbiol Mol Biol Rev. 1997 Jun;61(2):136-69 - PubMed
  235. Science. 2009 Jan 9;323(5911):269-72 - PubMed
  236. Fish Shellfish Immunol. 2019 Mar;86:143-151 - PubMed
  237. Infect Immun. 2015 Nov;83(11):4335-48 - PubMed
  238. Infect Immun. 1990 Nov;58(11):3731-6 - PubMed
  239. Arch Microbiol. 2012 Oct;194(10):827-35 - PubMed
  240. Arch Microbiol. 2006 Jul;186(1):11-20 - PubMed
  241. Microorganisms. 2019 Sep 03;7(9): - PubMed
  242. Infect Immun. 2000 Feb;68(2):526-34 - PubMed
  243. PLoS One. 2017 Jan 23;12(1):e0170770 - PubMed
  244. Nat Rev Microbiol. 2017 Jan;15(1):21-36 - PubMed
  245. Rev Physiol Biochem Pharmacol. 2004;152:65-77 - PubMed
  246. Fish Shellfish Immunol. 2019 Nov;94:58-65 - PubMed
  247. Mol Microbiol. 2009 Aug;73(4):639-49 - PubMed
  248. Int J Med Microbiol. 2007 Oct;297(6):401-15 - PubMed
  249. Mol Microbiol. 2002 Apr;44(1):217-31 - PubMed
  250. Appl Environ Microbiol. 2004 Nov;70(11):6914-9 - PubMed
  251. Infect Immun. 2011 Jul;79(7):2889-900 - PubMed
  252. Infect Immun. 2007 Nov;75(11):5079-84 - PubMed
  253. Vet Microbiol. 2003 Jul 30;94(4):325-33 - PubMed
  254. Microb Pathog. 1993 Oct;15(4):269-82 - PubMed
  255. Appl Environ Microbiol. 2021 Jul 27;87(16):e0081221 - PubMed
  256. Microbiology (Reading). 2008 May;154(Pt 5):1400-1413 - PubMed
  257. FEMS Microbiol Lett. 2001 Jan 15;194(2):239-43 - PubMed
  258. Infect Immun. 1998 Dec;66(12):5703-10 - PubMed
  259. Virulence. 2018 Dec 31;9(1):721-723 - PubMed
  260. J Fish Dis. 2007 May;30(5):257-68 - PubMed
  261. Proc Natl Acad Sci U S A. 2010 Jan 5;107(1):276-81 - PubMed
  262. Virulence. 2014 Jul 1;5(5):619-24 - PubMed
  263. Toxicon. 2018 Jul;149:45-53 - PubMed
  264. Cell Host Microbe. 2011 Oct 20;10(4):401-9 - PubMed
  265. Mol Membr Biol. 2005 Jan-Apr;22(1-2):29-39 - PubMed
  266. Microb Pathog. 2018 Apr;117:157-161 - PubMed
  267. FEMS Microbiol Lett. 2018 Jun 1;365(11): - PubMed
  268. Front Cell Infect Microbiol. 2020 Nov 05;10:599762 - PubMed
  269. Front Microbiol. 2018 Mar 26;9:525 - PubMed
  270. Microbiology (Reading). 2007 Feb;153(Pt 2):570-584 - PubMed
  271. Int J Med Microbiol. 2010 Dec;300(8):534-43 - PubMed
  272. J Bacteriol. 1990 Sep;172(9):5382-93 - PubMed
  273. Infect Immun. 2001 Sep;69(9):5538-45 - PubMed
  274. Annu Rev Microbiol. 2004;58:611-47 - PubMed
  275. Appl Environ Microbiol. 2009 May;75(9):2775-83 - PubMed
  276. EcoSal Plus. 2019 Mar;8(2): - PubMed
  277. Front Microbiol. 2018 Jan 23;9:18 - PubMed
  278. Virulence. 2015;6(5):417-8 - PubMed
  279. Infect Immun. 2004 Dec;72(12):7326-9 - PubMed
  280. Fish Shellfish Immunol. 2010 Dec;29(6):1082-91 - PubMed
  281. J Bacteriol. 2002 Nov;184(21):5966-70 - PubMed
  282. Infect Immun. 2006 Oct;74(10):6001-5 - PubMed
  283. Appl Environ Microbiol. 2019 Mar 6;85(6): - PubMed
  284. Org Biomol Chem. 2008 Apr 7;6(7):1278-87 - PubMed
  285. Infect Immun. 2007 Apr;75(4):1679-89 - PubMed
  286. J Biol Chem. 2007 Nov 23;282(47):34299-305 - PubMed
  287. J Gen Microbiol. 1985 Jul;131(7):1603-9 - PubMed
  288. Front Cell Infect Microbiol. 2018 Mar 15;8:70 - PubMed
  289. Nat Rev Microbiol. 2017 Jun;15(6):323-337 - PubMed
  290. J Bacteriol. 1996 Mar;178(5):1310-9 - PubMed
  291. Mol Microbiol. 1997 May;24(4):851-6 - PubMed
  292. Infect Immun. 2012 Aug;80(8):2689-703 - PubMed
  293. Cell Host Microbe. 2014 Aug 13;16(2):227-236 - PubMed
  294. Nat Microbiol. 2019 May;4(5):781-788 - PubMed
  295. mBio. 2020 Jan 7;11(1): - PubMed
  296. mSphere. 2016 May 11;1(3): - PubMed
  297. Front Microbiol. 2018 May 25;9:1084 - PubMed
  298. Infect Immun. 2008 Sep;76(9):4019-37 - PubMed
  299. ACS Chem Biol. 2015 Dec 18;10(12):2850-60 - PubMed
  300. Appl Environ Microbiol. 2010 Aug;76(16):5335-43 - PubMed
  301. Front Cell Infect Microbiol. 2017 May 26;7:215 - PubMed
  302. Mol Microbiol. 1997 Apr;24(2):271-83 - PubMed
  303. Vet Microbiol. 2008 Apr 30;128(3-4):386-94 - PubMed
  304. J Appl Microbiol. 2000 May;88(5):897-906 - PubMed
  305. Front Microbiol. 2017 Aug 16;8:1542 - PubMed
  306. Fish Shellfish Immunol. 2019 Apr;87:744-754 - PubMed
  307. J Mol Biol. 2003 Oct 24;333(3):657-74 - PubMed
  308. J Bacteriol. 2004 Sep;186(18):6159-67 - PubMed
  309. Fish Shellfish Immunol. 2008 Nov;25(5):477-84 - PubMed
  310. FEMS Microbiol Rev. 1997 Jun;20(1-2):99-149 - PubMed
  311. Sci Rep. 2015 Sep 24;5:14449 - PubMed
  312. Mol Microbiol. 2003 May;48(3):737-51 - PubMed
  313. Microbiology (Reading). 2006 Sep;152(Pt 9):2809-2818 - PubMed
  314. Microorganisms. 2020 Aug 01;8(8): - PubMed
  315. Nat Rev Microbiol. 2019 Jul;17(7):429-440 - PubMed
  316. FEBS Lett. 2013 Jun 19;587(12):1823-8 - PubMed
  317. J Biol Inorg Chem. 2000 Feb;5(1):57-66 - PubMed
  318. Emerg Microbes Infect. 2016 Aug 03;5(8):e85 - PubMed
  319. J Bacteriol. 2000 Apr;182(8):2326-8 - PubMed
  320. Biochim Biophys Acta. 2014 Aug;1843(8):1578-91 - PubMed
  321. Biosci Biotechnol Biochem. 2015;80(1):135-44 - PubMed
  322. J Biol Chem. 1982 Mar 25;257(6):3320-5 - PubMed
  323. J Membr Biol. 1990 Apr;115(1):71-81 - PubMed
  324. Fish Shellfish Immunol. 2019 Nov;94:723-729 - PubMed
  325. ISME J. 2013 May;7(5):1026-37 - PubMed
  326. Environ Microbiol Rep. 2010 Feb;2(1):133-9 - PubMed
  327. Front Microbiol. 2017 Nov 30;8:2339 - PubMed
  328. Proteome Sci. 2010 Jun 04;8:26 - PubMed
  329. Microbiol Spectr. 2015 Jun;3(3): - PubMed
  330. Appl Environ Microbiol. 2006 Jun;72(6):4044-53 - PubMed
  331. J Bacteriol. 1988 Aug;170(8):3694-702 - PubMed
  332. J Biol Chem. 2003 Aug 29;278(35):32794-800 - PubMed
  333. Cell Tissue Res. 2011 Jan;343(1):227-35 - PubMed
  334. Environ Microbiol. 2010 Jun;12(6):1377-83 - PubMed
  335. Physiol Genomics. 2011 Nov 7;43(21):1241-54 - PubMed
  336. Nat Rev Microbiol. 2015 Jun;13(6):343-59 - PubMed
  337. Front Microbiol. 2017 Feb 28;8:282 - PubMed
  338. Front Cell Infect Microbiol. 2017 Sep 06;7:400 - PubMed
  339. Front Physiol. 2017 Dec 18;8:1066 - PubMed
  340. Proc Natl Acad Sci U S A. 2012 Dec 26;109(52):21390-5 - PubMed
  341. PLoS One. 2018 Feb 14;13(2):e0191860 - PubMed
  342. Clin Microbiol Rev. 2007 Oct;20(4):535-49 - PubMed
  343. Pathogens. 2019 Nov 28;8(4): - PubMed
  344. Biometals. 2007 Jun;20(3-4):393-403 - PubMed
  345. J Fish Dis. 2013 Apr;36(4):371-88 - PubMed
  346. J Fish Dis. 2014 Mar;37(3):163-88 - PubMed
  347. Rev Physiol Biochem Pharmacol. 2004;152:79-92 - PubMed
  348. Science. 2015 May 22;348(6237):1261359 - PubMed
  349. Can J Microbiol. 1993 May;39(5):513-23 - PubMed
  350. Front Vet Sci. 2020 Sep 25;7:574113 - PubMed
  351. J Bacteriol. 2014 Dec;196(24):4245-52 - PubMed
  352. Vet Microbiol. 2011 Sep 28;152(3-4):394-400 - PubMed
  353. J Fish Dis. 2011 Sep;34(9):643-61 - PubMed
  354. Arch Immunol Ther Exp (Warsz). 2002;50(6):379-91 - PubMed
  355. Front Cell Infect Microbiol. 2021 Feb 03;10:591751 - PubMed
  356. Front Microbiol. 2018 Aug 02;9:1766 - PubMed
  357. ACS Chem Biol. 2017 Feb 17;12(2):479-493 - PubMed
  358. Microb Ecol. 2013 Nov;66(4):850-60 - PubMed
  359. Microb Pathog. 2009 Sep;47(3):134-42 - PubMed
  360. J Aquat Anim Health. 2019 Mar;31(1):3-22 - PubMed
  361. Appl Environ Microbiol. 2019 May 2;85(10): - PubMed
  362. J Bacteriol. 2002 Oct;184(20):5762-71 - PubMed
  363. Met Ions Biol Syst. 1998;35:67-145 - PubMed
  364. Mol Microbiol. 2017 Oct;106(1):35-53 - PubMed
  365. Dev Comp Immunol. 2014 Sep;46(1):96-107 - PubMed
  366. Genes (Basel). 2019 Sep 11;10(9): - PubMed
  367. Dis Aquat Organ. 2010 Oct 26;92(1):31-40 - PubMed
  368. ACS Infect Dis. 2019 Nov 8;5(11):1936-1951 - PubMed
  369. J Invertebr Pathol. 2018 Jun;155:25-31 - PubMed
  370. Nat Rev Microbiol. 2014 Feb;12(2):137-48 - PubMed
  371. J Exp Med. 1990 Sep 1;172(3):795-806 - PubMed
  372. J Biol Chem. 2003 Jul 4;278(27):24509-20 - PubMed
  373. Appl Environ Microbiol. 2020 Aug 3;86(16): - PubMed
  374. Microb Pathog. 2016 Nov;100:195-200 - PubMed
  375. J Bacteriol. 2011 Jul;193(13):3389-90 - PubMed
  376. PLoS Pathog. 2015 Aug 25;11(8):e1005128 - PubMed
  377. Crit Rev Microbiol. 2018 Nov;44(6):779-792 - PubMed
  378. J Biol Chem. 2002 Nov 8;277(45):42530-9 - PubMed
  379. J Bacteriol. 1996 Mar;178(5):1412-9 - PubMed
  380. J Bacteriol. 2003 Dec;185(23):6938-49 - PubMed
  381. Experientia. 1991 May 15;47(5):416-8 - PubMed
  382. Microb Pathog. 2010 Dec;49(6):369-75 - PubMed
  383. Fish Shellfish Immunol. 2019 Oct;93:871-878 - PubMed
  384. Appl Environ Microbiol. 2004 Jul;70(7):4193-204 - PubMed
  385. Dis Aquat Organ. 2014 May 13;109(2):117-26 - PubMed
  386. Dis Aquat Organ. 1999 Sep 14;37(3):165-72 - PubMed
  387. J Bacteriol. 2008 Oct;190(20):6589-97 - PubMed
  388. Microb Pathog. 2017 Oct;111:203-211 - PubMed
  389. Appl Environ Microbiol. 1999 Aug;65(8):3555-60 - PubMed
  390. Appl Environ Microbiol. 1986 Mar;51(3):668-70 - PubMed
  391. Infect Immun. 2001 Jun;69(6):3523-35 - PubMed

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