Endosymbiont Tolerance and Control within Insect Hosts.

Carolin Ratzka, Roy Gross, Heike Feldhaar
Author Information
  1. Carolin Ratzka: Department of Microbiology, Biocentre, University of Würzburg, 97074, Germany. carolin.ratzka@biozentrum.uni-wuerzburg.de.
  2. Roy Gross: Department of Microbiology, Biocentre, University of Würzburg, 97074, Germany. roy@biozentrum.uni-wuerzburg.de.
  3. Heike Feldhaar: Animal Ecology I, University of Bayreuth, 95440, Germany. feldhaar@uni-bayreuth.de.

Abstract

Bacterial endosymbioses are very common in insects and can range from obligate to facultative as well as from mutualistic to pathogenic associations. Several recent studies provide new insight into how endosymbionts manage to establish chronic infections of their hosts without being eliminated by the host immune system. Endosymbiont tolerance may be achieved either by specific bacterial adaptations or by host measurements shielding bacteria from innate defense mechanisms. Nevertheless, insect hosts also need to sustain control mechanisms to prevent endosymbionts from unregulated proliferation. Emerging evidence indicates that in some cases the mutual adaptations of the two organisms may have led to the integration of the endosymbionts as a part of the host immune system. In fact, endosymbionts may provide protective traits against pathogens and predators and may even be required for the proper development of the host immune system during host ontogeny. This review gives an overview of current knowledge of molecular mechanisms ensuring maintenance of chronic infections with mutualistic endosymbionts and the impact of endosymbionts on host immune competence.

Keywords

References

  1. Proc Natl Acad Sci U S A. 1999 Jun 8;96(12):6814-9 [PMID: 10359795]
  2. Trends Biochem Sci. 1999 Aug;24(8):311-6 [PMID: 10431175]
  3. Annu Rev Microbiol. 1999;53:71-102 [PMID: 10547686]
  4. Parasitol Today. 2000 Mar;16(3):114-8 [PMID: 10689331]
  5. Ann N Y Acad Sci. 1975;266:260-75 [PMID: 1072598]
  6. Science. 2000 Apr 7;288(5463):146-9 [PMID: 10753120]
  7. J Biol Chem. 2000 Oct 20;275(42):32721-7 [PMID: 10827089]
  8. Insect Mol Biol. 2000 Dec;9(6):635-9 [PMID: 11122472]
  9. Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1883-8 [PMID: 11172045]
  10. Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12648-53 [PMID: 11592981]
  11. J Biol Chem. 2002 Mar 1;277(9):7059-65 [PMID: 11751856]
  12. Nat Genet. 2002 Nov;32(3):402-7 [PMID: 12219091]
  13. Dev Cell. 2002 Nov;3(5):711-22 [PMID: 12431377]
  14. Science. 2003 Jan 17;299(5605):386-8 [PMID: 12532015]
  15. Insect Mol Biol. 2003 Feb;12(1):93-7 [PMID: 12542640]
  16. Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1803-7 [PMID: 12563031]
  17. Mol Ecol. 2003 Apr;12(4):1061-75 [PMID: 12753224]
  18. Genetics. 1961 Dec;46:1665-76 [PMID: 14496145]
  19. PLoS Biol. 2003 Oct;1(1):E21 [PMID: 14551917]
  20. Mol Immunol. 2004 Feb;40(12):877-86 [PMID: 14698226]
  21. J Bacteriol. 2004 Mar;186(5):1280-6 [PMID: 14973122]
  22. Annu Rev Entomol. 1997;42:587-609 [PMID: 15012323]
  23. Annu Rev Entomol. 1998;43:17-37 [PMID: 15012383]
  24. PLoS Biol. 2004 Mar;2(3):E69 [PMID: 15024419]
  25. Nat Rev Microbiol. 2004 Apr;2(4):301-14 [PMID: 15031729]
  26. Curr Opin Microbiol. 2004 Feb;7(1):67-70 [PMID: 15036143]
  27. J Med Entomol. 2004 May;41(3):447-55 [PMID: 15185949]
  28. Microbiol Mol Biol Rev. 2004 Dec;68(4):745-70 [PMID: 15590782]
  29. Cell Microbiol. 2005 Feb;7(2):293-305 [PMID: 15659072]
  30. Insect Biochem Mol Biol. 2005 Feb;35(2):105-15 [PMID: 15681221]
  31. Curr Biol. 2005 Mar 8;15(5):475-9 [PMID: 15753044]
  32. Proc Natl Acad Sci U S A. 2005 Apr 12;102(15):5477-82 [PMID: 15800043]
  33. Insect Mol Biol. 2005 Jun;14(3):281-7 [PMID: 15926897]
  34. Appl Environ Microbiol. 2005 Jun;71(6):3302-10 [PMID: 15933033]
  35. Proc Natl Acad Sci U S A. 2005 Aug 9;102(32):11426-31 [PMID: 16061795]
  36. Proc Natl Acad Sci U S A. 2005 Sep 6;102(36):12795-800 [PMID: 16120675]
  37. Annu Rev Microbiol. 2005;59:155-89 [PMID: 16153167]
  38. Proc Natl Acad Sci U S A. 2005 Nov 22;102(47):16919-26 [PMID: 16195380]
  39. Science. 2005 Dec 16;310(5755):1781 [PMID: 16357252]
  40. Immunity. 2006 Apr;24(4):463-73 [PMID: 16618604]
  41. Proc Biol Sci. 2006 Apr 7;273(1588):805-14 [PMID: 16618673]
  42. Front Biosci. 2006 Sep 01;11:2983-3002 [PMID: 16720370]
  43. Proc Biol Sci. 2006 May 22;273(1591):1273-80 [PMID: 16720402]
  44. EMBO J. 2006 Jul 12;25(13):3068-77 [PMID: 16763552]
  45. Cell. 2006 Aug 11;126(3):453-65 [PMID: 16901780]
  46. J Biochem. 2006 Aug;140(2):161-6 [PMID: 16954534]
  47. Appl Environ Microbiol. 2006 Oct;72(10):6766-72 [PMID: 17021229]
  48. Proc Natl Acad Sci U S A. 2006 Oct 24;103(43):15800-5 [PMID: 17043235]
  49. Cell. 2006 Dec 29;127(7):1425-37 [PMID: 17190605]
  50. Annu Rev Immunol. 2007;25:697-743 [PMID: 17201680]
  51. Nat Rev Microbiol. 2007 Apr;5(4):264-77 [PMID: 17363965]
  52. PLoS Biol. 2007 May;5(5):e96 [PMID: 17425405]
  53. Immunol Rev. 2007 Oct;219:8-16 [PMID: 17850478]
  54. BMC Biol. 2007 Oct 30;5:48 [PMID: 17971224]
  55. Proc Biol Sci. 2008 Feb 7;275(1632):293-9 [PMID: 18029301]
  56. Biochem Soc Trans. 2007 Dec;35(Pt 6):1496-500 [PMID: 18031252]
  57. Proc Biol Sci. 2008 Feb 22;275(1633):353-61 [PMID: 18055391]
  58. BMC Genomics. 2008 Jan 02;9:1 [PMID: 18171476]
  59. Science. 2008 Feb 8;319(5864):777-82 [PMID: 18218863]
  60. Proc Biol Sci. 2008 May 7;275(1638):1089-94 [PMID: 18270153]
  61. Nature. 2008 Feb 28;451(7182):1069-75 [PMID: 18305538]
  62. FEMS Microbiol Lett. 2008 Apr;281(2):215-20 [PMID: 18312577]
  63. Science. 2008 Jun 20;320(5883):1651-4 [PMID: 18566289]
  64. Nat Immunol. 2008 Aug;9(8):908-16 [PMID: 18604211]
  65. J Insect Physiol. 2008 Aug;54(8):1236-42 [PMID: 18647605]
  66. Microbes Infect. 2008 Jul;10(9):1082-8 [PMID: 18672091]
  67. Appl Environ Microbiol. 2008 Oct;74(19):5965-74 [PMID: 18689507]
  68. Cell Mol Life Sci. 2008 Oct;65(19):3081-92 [PMID: 18726072]
  69. Appl Environ Microbiol. 2008 Nov;74(21):6782-91 [PMID: 18791000]
  70. Nat Rev Microbiol. 2008 Oct;6(10):741-51 [PMID: 18794912]
  71. Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15088-93 [PMID: 18815366]
  72. Insect Mol Biol. 2008 Dec;17(6):711-6 [PMID: 18823444]
  73. Science. 2008 Oct 3;322(5898):63 [PMID: 18832638]
  74. BMC Biol. 2008 Oct 16;6:43 [PMID: 18925938]
  75. Science. 2008 Oct 31;322(5902):702 [PMID: 18974344]
  76. Annu Rev Genet. 2008;42:165-90 [PMID: 18983256]
  77. Science. 2008 Nov 21;322(5905):1257-9 [PMID: 19023083]
  78. Environ Microbiol. 2009 Apr;11(4):877-88 [PMID: 19040455]
  79. J Insect Physiol. 2009 Apr;55(4):351-7 [PMID: 19183557]
  80. PLoS Biol. 2008 Dec 23;6(12):e2 [PMID: 19222304]
  81. Science. 2009 Apr 10;324(5924):258-61 [PMID: 19264986]
  82. Zoolog Sci. 2009 Jun;26(6):415-20 [PMID: 19583501]
  83. Proc Natl Acad Sci U S A. 2009 Jul 21;106(29):12133-8 [PMID: 19587241]
  84. Mol Microbiol. 2009 Sep;73(5):751-9 [PMID: 19656293]
  85. Trends Microbiol. 2009 Aug;17(8):348-54 [PMID: 19660955]
  86. Science. 2009 Aug 21;325(5943):992-4 [PMID: 19696350]
  87. Annu Rev Entomol. 2010;55:247-66 [PMID: 19728837]
  88. Biol Lett. 2010 Feb 23;6(1):109-11 [PMID: 19776066]
  89. Science. 2009 Oct 2;326(5949):134-6 [PMID: 19797660]
  90. Trends Microbiol. 2009 Dec;17(12):529-35 [PMID: 19853457]
  91. Cell. 2009 Dec 24;139(7):1268-78 [PMID: 20064373]
  92. Genome Biol. 2010;11(2):R21 [PMID: 20178569]
  93. PLoS Biol. 2010 Feb 23;8(2):e1000313 [PMID: 20186266]
  94. Insect Mol Biol. 2010 Aug;19(4):481-8 [PMID: 20456506]
  95. Science. 2010 Jul 9;329(5988):212-5 [PMID: 20616278]
  96. PLoS One. 2010 Aug 05;5(8):e11977 [PMID: 20700535]
  97. Proc Biol Sci. 2011 Feb 7;278(1704):333-8 [PMID: 20719775]
  98. PLoS One. 2010 Aug 13;5(8):e12149 [PMID: 20730104]
  99. PLoS Pathog. 2010 Oct 07;6(10):e1001143 [PMID: 20949079]
  100. BMC Microbiol. 2010 Dec 01;10:308 [PMID: 21122115]
  101. Ecol Lett. 2011 Feb;14(2):150-5 [PMID: 21155960]
  102. Mol Ecol. 2011 Mar;20(5):950-8 [PMID: 21255169]
  103. Insect Mol Biol. 2011 Jun;20(3):357-65 [PMID: 21382108]
  104. J Insect Physiol. 2011 Jun;57(6):830-9 [PMID: 21439291]
  105. Insect Biochem Mol Biol. 2011 Aug;41(8):529-36 [PMID: 21440063]
  106. PLoS Biol. 2011 May;9(5):e1000619 [PMID: 21655301]
  107. Cell Microbiol. 2011 Sep;13(9):1385-96 [PMID: 21740495]
  108. Science. 2011 Oct 21;334(6054):362-5 [PMID: 22021855]
  109. J Immunol. 2012 Apr 1;188(7):3395-403 [PMID: 22368278]
  110. BMC Microbiol. 2012 Jan 18;12 Suppl 1:S14 [PMID: 22375912]
  111. BMC Microbiol. 2012 Jan 18;12 Suppl 1:S7 [PMID: 22376153]
  112. Infect Immun. 1989 Sep;57(9):2628-33 [PMID: 2759705]
  113. Wilehm Roux Arch Dev Biol. 1980 Jun;188(2):91-99 [PMID: 28304971]
  114. Oecologia. 1996 Aug;107(3):293-300 [PMID: 28307257]
  115. J Insect Physiol. 1971 Oct;17(10):2035-50 [PMID: 4999588]
  116. Int J Syst Bacteriol. 1995 Oct;45(4):848-51 [PMID: 7547309]
  117. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7888-93 [PMID: 8755572]
  118. Genetics. 1998 Jan;148(1):221-31 [PMID: 9475734]
  119. J Gen Virol. 1998 Apr;79 ( Pt 4):731-40 [PMID: 9568968]
  120. J Mol Evol. 1998 Jul;47(1):52-61 [PMID: 9664696]

Word Cloud

Created with Highcharts 10.0.0endosymbiontshostimmunemaysystemmechanismsinsectsmutualisticprovidechronicinfectionshostsEndosymbiontadaptationsBacterialendosymbiosescommoncanrangeobligatefacultativewellpathogenicassociationsSeveralrecentstudiesnewinsightmanageestablishwithouteliminatedtoleranceachievedeitherspecificbacterialmeasurementsshieldingbacteriainnatedefenseNeverthelessinsectalsoneedsustaincontrolpreventunregulatedproliferationEmergingevidenceindicatescasesmutualtwoorganismsledintegrationpartfactprotectivetraitspathogenspredatorsevenrequiredproperdevelopmentontogenyreviewgivesoverviewcurrentknowledgemolecularensuringmaintenanceimpactcompetenceToleranceControlwithinInsectHostsendosymbiosisresponse

Similar Articles

Cited By