OpenLB
Open Library of Bioscience
Advanced Search
Toxins
08 12, 2020;12 (8):

The Tripartite Interaction of Host Immunity- Infection-Gut Microbiota.

Shuzhong Li, Surajit De Mandal, Xiaoxia Xu, Fengliang Jin
Author Information
  1. Shuzhong Li: Laboratory of Bio-Pesticide Innovation and Application of Guangdong Province, College of Agriculture, South China Agricultural University, Guangzhou 510642, China.
  2. Surajit De Mandal: Laboratory of Bio-Pesticide Innovation and Application of Guangdong Province, College of Agriculture, South China Agricultural University, Guangzhou 510642, China.
  3. Xiaoxia Xu: Laboratory of Bio-Pesticide Innovation and Application of Guangdong Province, College of Agriculture, South China Agricultural University, Guangzhou 510642, China.
  4. Fengliang Jin: Laboratory of Bio-Pesticide Innovation and Application of Guangdong Province, College of Agriculture, South China Agricultural University, Guangzhou 510642, China.
PMID: 32806491 DOI: 10.3390/toxins12080514

Abstract

(Bt) is an important cosmopolitan bacterial entomopathogen, which produces various protein toxins that have been expressed in transgenic crops. The evolved molecular interaction between the insect immune system and gut microbiota is changed during the Bt infection process. The host immune response, such as the expression of induced antimicrobial peptides (AMPs), the melanization response, and the production of reactive oxygen species (ROS), varies with different doses of Bt infection. Moreover, infection changes the abundance and structural composition of the intestinal bacteria community. The activated immune response, together with dysbiosis of the gut microbiota, also has an important effect on Bt pathogenicity and insect resistance to Bt. In this review, we attempt to clarify this tripartite interaction of host immunity, Bt infection, and gut microbiota, especially the important role of key immune regulators and symbiotic bacteria in the Bt killing activity. Increasing the effectiveness of biocontrol agents by interfering with insect resistance and controlling symbiotic bacteria can be important steps for the successful application of microbial biopesticides.

Keywords

Bacillus thuringiensis antimicrobial peptide gut microbiota

References

  1. Dev Comp Immunol. 2020 Jan;102:103468 [PMID: 31430488]
  2. Dev Comp Immunol. 2015 Jun;50(2):139-45 [PMID: 25684675]
  3. PLoS One. 2012;7(6):e39192 [PMID: 22761737]
  4. J Innate Immun. 2012;4(3):273-83 [PMID: 22237424]
  5. Mol Immunol. 2019 Feb;106:69-76 [PMID: 30590209]
  6. ISME J. 2016 May;10(5):1037-50 [PMID: 26565723]
  7. Nat Rev Microbiol. 2013 Sep;11(9):615-26 [PMID: 23893105]
  8. Antonie Van Leeuwenhoek. 2010 Jan;97(1):69-77 [PMID: 19876756]
  9. J Invertebr Pathol. 2010 Feb;103(2):124-31 [PMID: 20035766]
  10. Gene. 2018 Mar 20;647:21-30 [PMID: 29305978]
  11. Proc Natl Acad Sci U S A. 2011 Nov 29;108(48):19288-92 [PMID: 22084077]
  12. Trends Microbiol. 2010 May;18(5):189-94 [PMID: 20338765]
  13. Dev Comp Immunol. 2018 Sep;86:65-77 [PMID: 29715482]
  14. Microbiol Mol Biol Rev. 2007 Jun;71(2):255-81 [PMID: 17554045]
  15. J Insect Physiol. 2017 Apr;98:275-283 [PMID: 28167070]
  16. Nat Rev Immunol. 2010 Oct;10(10):735-44 [PMID: 20865020]
  17. J Appl Microbiol. 2003;94(6):981-7 [PMID: 12752805]
  18. Genes Dev. 2009 Oct 1;23(19):2333-44 [PMID: 19797770]
  19. Annu Rev Immunol. 2007;25:697-743 [PMID: 17201680]
  20. Mol Ecol. 2014 Mar;23(6):1225-37 [PMID: 24628935]
  21. Environ Microbiol. 2010 Oct;12(10):2730-7 [PMID: 20482744]
  22. PLoS One. 2014 Apr 14;9(4):e94729 [PMID: 24733183]
  23. FEMS Microbiol Rev. 2013 Jan;37(1):3-22 [PMID: 22540421]
  24. Int J Med Microbiol. 2000 Oct;290(4-5):463-9 [PMID: 11111927]
  25. Sci Rep. 2013;3:1641 [PMID: 23571408]
  26. J Invertebr Pathol. 2014 Jun;119:40-6 [PMID: 24735783]
  27. Bioeng Bugs. 2010 Jan-Feb;1(1):31-50 [PMID: 21327125]
  28. J Invertebr Pathol. 2008 Jul;98(3):360-2 [PMID: 18440019]
  29. Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):2696-9 [PMID: 14978282]
  30. Arch Insect Biochem Physiol. 1999 Sep;42(1):51-63 [PMID: 10467056]
  31. Science. 2010 Mar 26;327(5973):1644-8 [PMID: 20223948]
  32. Front Physiol. 2019 Oct 16;10:1303 [PMID: 31681013]
  33. Cell. 2014 Dec 4;159(6):1277-89 [PMID: 25480293]
  34. PLoS One. 2011 Mar 01;6(3):e17606 [PMID: 21390253]
  35. Insect Biochem Mol Biol. 2019 Apr;107:31-38 [PMID: 30710623]
  36. Science. 2012 Jun 8;336(6086):1262-7 [PMID: 22674330]
  37. Front Microbiol. 2017 Jul 07;8:1261 [PMID: 28736550]
  38. Sci Rep. 2015 Nov 23;5:16823 [PMID: 26592948]
  39. Pest Manag Sci. 2017 Dec;73(12):2495-2503 [PMID: 28627124]
  40. Parasit Vectors. 2018 Mar 2;11(1):121 [PMID: 29499735]
  41. PLoS Pathog. 2013;9(5):e1003379 [PMID: 23717206]
  42. Science. 2005 Nov 4;310(5749):847-50 [PMID: 16272120]
  43. PLoS One. 2013 Dec 02;8(12):e81927 [PMID: 24312604]
  44. J Agric Food Chem. 2019 Aug 14;67(32):8896-8904 [PMID: 31339308]
  45. Proc Natl Acad Sci U S A. 2016 Aug 23;113(34):9486-91 [PMID: 27506800]
  46. Pestic Biochem Physiol. 2019 Oct;160:79-86 [PMID: 31519260]
  47. Virulence. 2016 Nov 16;7(8):860-870 [PMID: 27029421]
  48. Cell Metab. 2011 Sep 7;14(3):403-14 [PMID: 21907145]
  49. Biochem Soc Symp. 2004;(71):85-96 [PMID: 15777014]
  50. Front Microbiol. 2019 Jul 18;10:1580 [PMID: 31379768]
  51. Toxins (Basel). 2019 Sep 14;11(9): [PMID: 31540044]
  52. Mol Ecol. 2017 May;26(9):2576-2590 [PMID: 28207182]
  53. Toxins (Basel). 2014 Dec 11;6(12):3296-325 [PMID: 25514092]
  54. Trends Ecol Evol. 2004 Feb;19(2):58-60 [PMID: 16701227]
  55. Insect Biochem Mol Biol. 2011 Jul;41(7):423-31 [PMID: 21376122]
  56. Invertebrate Surviv J. 2009 Jun 1;6(2):163-174 [PMID: 21625362]
  57. Dev Comp Immunol. 2020 Sep;110:103732 [PMID: 32423863]
  58. Biochem Biophys Res Commun. 1994 Feb 15;198(3):940-7 [PMID: 8117300]
  59. Parasitol Res. 2013 Sep;112(9):3283-8 [PMID: 23820604]
  60. Insect Biochem Mol Biol. 2018 Nov;102:59-66 [PMID: 30278206]
  61. J Agric Food Chem. 2017 Mar 15;65(10):2048-2055 [PMID: 28231709]
  62. mBio. 2014 May 27;5(3):e01117-14 [PMID: 24865556]
  63. Appl Environ Microbiol. 2017 Apr 17;83(9): [PMID: 28213547]
  64. J Immunol. 2008 Apr 15;180(8):5413-22 [PMID: 18390723]
  65. Science. 2008 Feb 8;319(5864):777-82 [PMID: 18218863]
  66. PLoS One. 2010 Sep 17;5(9): [PMID: 20862260]
  67. PLoS Genet. 2015 Apr 13;11(4):e1005124 [PMID: 25875245]
  68. Nat Rev Immunol. 2011 Nov 11;11(12):837-51 [PMID: 22076558]
  69. Parasite Immunol. 2006 Apr;28(4):121-30 [PMID: 16542314]
  70. Tissue Cell. 1991;23(3):411-22 [PMID: 18621170]
  71. Environ Microbiol. 2009 Oct;11(10):2556-63 [PMID: 19555371]
  72. Front Microbiol. 2020 May 25;11:846 [PMID: 32523559]
  73. Front Microbiol. 2016 Jan 06;6:1383 [PMID: 26779124]
  74. Cell Host Microbe. 2015 Feb 11;17(2):191-204 [PMID: 25639794]
  75. PLoS Genet. 2011 Aug;7(8):e1002168 [PMID: 21829386]
  76. Dev Comp Immunol. 2016 Nov;64:65-74 [PMID: 26872544]
  77. Appl Environ Microbiol. 2009 Aug;75(15):5094-9 [PMID: 19525273]
  78. Plant Biotechnol J. 2011 Apr;9(3):283-300 [PMID: 21375687]
  79. Sci Rep. 2017 Nov 24;7(1):16245 [PMID: 29176692]
  80. Trends Immunol. 2005 Apr;26(4):193-8 [PMID: 15797509]
  81. BMB Rep. 2008 Feb 29;41(2):93-101 [PMID: 18315943]
  82. J Environ Biol. 2008 Sep;29(5):641-53 [PMID: 19295059]
  83. Dev Comp Immunol. 2010 Oct;34(10):1119-28 [PMID: 20600279]
  84. Environ Entomol. 2014 Jun;43(3):612-6 [PMID: 24780240]
  85. Arch Insect Biochem Physiol. 2020 Apr;103(4):e21638 [PMID: 31702074]
  86. Appl Environ Microbiol. 2014 Sep;80(17):5254-64 [PMID: 24928884]
  87. PLoS One. 2014 Jan 27;9(1):e85948 [PMID: 24475063]
  88. PLoS Pathog. 2018 Feb 28;14(2):e1006899 [PMID: 29489896]
  89. mBio. 2013 Nov 05;4(6):e00860-13 [PMID: 24194543]
  90. Virulence. 2018;9(1):1625-1639 [PMID: 30257608]
  91. Cell Host Microbe. 2014 Nov 12;16(5):592-604 [PMID: 25525791]
  92. Dev Comp Immunol. 2010 Apr;34(4):369-76 [PMID: 19958789]
  93. Nat Chem Biol. 2014 Jun;10(6):416-24 [PMID: 24838170]
  94. Gene. 2014 Jan 1;533(1):180-7 [PMID: 24120626]
  95. mBio. 2011 May 17;2(3):e00065-11 [PMID: 21586646]
  96. Cell Chem Biol. 2017 Jan 19;24(1):66-75 [PMID: 28107652]
  97. Nature. 2012 Jul 19;487(7407):362-5 [PMID: 22722864]
  98. Front Microbiol. 2016 Oct 06;7:1567 [PMID: 27766093]
  99. Curr Opin Immunol. 2014 Oct;30:48-53 [PMID: 24997434]
  100. Biochem Biophys Res Commun. 2006 Jan 27;339(4):1043-7 [PMID: 16337146]
  101. PLoS Pathog. 2007 Mar;3(3):e26 [PMID: 17352533]
  102. Crit Rev Biotechnol. 2016;36(2):317-26 [PMID: 25264571]
  103. Appl Environ Microbiol. 2014 Oct;80(20):6258-65 [PMID: 25002420]
  104. Proc Natl Acad Sci U S A. 2009 Nov 17;106(46):19521-6 [PMID: 19880743]
  105. Toxins (Basel). 2018 Sep 25;10(10): [PMID: 30257487]
  106. Insect Biochem Mol Biol. 2005 Jul;35(7):729-39 [PMID: 15894190]
  107. FEMS Microbiol Rev. 2013 Sep;37(5):699-735 [PMID: 23692388]
  108. Curr Opin Insect Sci. 2016 Jun;15:104-10 [PMID: 27436739]
  109. J Biol Chem. 2012 Apr 20;287(17):14270-9 [PMID: 22375003]
  110. Proc Biol Sci. 2017 Dec 20;284(1869): [PMID: 29237849]
  111. J Exp Biol. 2004 Jul;207(Pt 15):2551-63 [PMID: 15201288]
  112. PLoS Pathog. 2010 Sep 09;6(9):e1001097 [PMID: 20844578]
  113. Dev Comp Immunol. 2020 Jun;107:103661 [PMID: 32097696]
  114. Science. 2008 Oct 3;322(5898):63 [PMID: 18832638]
  115. Front Cell Infect Microbiol. 2014 Jan 10;3:116 [PMID: 24455491]
  116. Dev Comp Immunol. 2019 Aug;97:20-27 [PMID: 30914318]
  117. J Econ Entomol. 2017 Apr 1;110(2):362-377 [PMID: 28334065]
  118. PLoS Pathog. 2009 Dec;5(12):e1000694 [PMID: 20019799]
  119. Proc Natl Acad Sci U S A. 2006 Oct 10;103(41):15196-9 [PMID: 17005725]
  120. J Invertebr Pathol. 2000 Oct;76(3):222-6 [PMID: 11023751]
  121. Sci Rep. 2016 Mar 30;6:23861 [PMID: 27025647]
  122. R Soc Open Sci. 2017 Feb 8;4(2):170003 [PMID: 28386455]
  123. Annu Rev Genet. 2003;37:409-33 [PMID: 14616068]
  124. Nat Biotechnol. 2017 Oct 11;35(10):926-935 [PMID: 29020006]
  125. J Med Entomol. 2003 May;40(3):371-4 [PMID: 12943119]
  126. Int J Biol Macromol. 2018 May;111:822-831 [PMID: 29305214]
  127. Cell. 2013 May 9;153(4):797-811 [PMID: 23663779]
  128. Proc Biol Sci. 2009 Jan 7;276(1654):145-51 [PMID: 18796392]
  129. Pestic Biochem Physiol. 2020 Feb;163:200-208 [PMID: 31973858]
  130. Front Physiol. 2018 Nov 15;9:1478 [PMID: 30498450]
  131. PLoS One. 2015 May 18;10(5):e0125991 [PMID: 25993013]
  132. J Invertebr Pathol. 2007 Oct;96(2):125-32 [PMID: 17499761]
  133. Nat Rev Endocrinol. 2015 Oct;11(10):577-91 [PMID: 26260141]
  134. Microbiol Res. 2008;163(6):684-92 [PMID: 19216106]
  135. BMC Biol. 2010 Dec 22;8:152 [PMID: 21176204]

Grants

  1. 31972345/National Natural Science Foundation of China

MeSH Term

Animals
Bacillus thuringiensis
Bacterial Infections
Biological Control Agents
Dysbiosis
Gastrointestinal Microbiome
Host Microbial Interactions
Immunity
Insecta
Microbial Interactions
Pore Forming Cytotoxic Proteins

Chemicals

Biological Control Agents
Pore Forming Cytotoxic Proteins
Journal Article Research Support, Non-U.S. Gov't Review
Article has an altmetric score of 1

Word Cloud

Created with Highcharts 10.0.0BtimportantimmunegutmicrobiotainfectioninsectresponsebacteriainteractionhostantimicrobialresistancesymbioticcosmopolitanbacterialentomopathogenproducesvariousproteintoxinsexpressedtransgeniccropsevolvedmolecularsystemchangedprocessexpressioninducedpeptidesAMPsmelanizationproductionreactiveoxygenspeciesROSvariesdifferentdosesMoreoverchangesabundancestructuralcompositionintestinalcommunityactivatedtogetherdysbiosisalsoeffectpathogenicityreviewattemptclarifytripartiteimmunityespeciallyrolekeyregulatorskillingactivityIncreasingeffectivenessbiocontrolagentsinterferingcontrollingcanstepssuccessfulapplicationmicrobialbiopesticidesTripartiteInteractionHostImmunity-Infection-GutMicrobiotaBacillusthuringiensispeptide

Similar Articles

Cited By