Lessons from studying insect symbioses

Cell Host and Microbe

Volumn 10, Issue 4, 2011, Pages 359-367

  Douglas, Angela E ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; HOST PATHOGEN INTERACTION; INSECT; MAMMAL; MICROORGANISM; NONHUMAN; PRIORITY JOURNAL; SYMBIOSIS;

HEXAPODA; MAMMALIA;

EID: 80054932118     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2011.09.001     Document Type: Review

References (77)

1. D.K. Aanen, and R.F. Hoekstra The evolution of obligate mutualism: if you can't beat 'em, join 'em Trends Ecol. Evol. (Amst.) 22 2007 506 509 (Pubitemid 47562148)
2. E. Akman Gündüz, and A.E. Douglas Symbiotic bacteria enable insect to use a nutritionally inadequate diet Proc. Biol. Sci. 276 2009 987 991
3. M. Bakula The persistence of a microbial flora during postembryogenesis of Drosophila melanogaster J. Invertebr. Pathol. 14 1969 365 374
4. G. Brugerolle, and R. Radek Symbiotic protozoa of termites H. König, A. Varma, Intestinal Microorganisms of Soil Invertebrates 2006 Springer-Verlag Berlin 243 269
5. T. Brummel, A. Ching, L. Seroude, A.F. Simon, and S. Benzer Drosophila lifespan enhancement by exogenous bacteria Proc. Natl. Acad. Sci. USA 101 2004 12974 12979 (Pubitemid 39167568)
6. K.E. Burnum, S.J. Callister, C.D. Nicora, S.O. Purvine, P. Hugenholtz, F. Warnecke, R.H. Scheffrahn, R.D. Smith, and M.S. Lipton Proteome insights into the symbiotic relationship between a captive colony of Nasutitermes corniger and its hindgut microbiome ISME J. 5 2011 161 164
7. S.M. Chandler, T.L. Wilkinson, and A.E. Douglas Impact of plant nutrients on the relationship between a herbivorous insect and its symbiotic bacteria Proc. Biol. Sci. 275 2008 565 570 (Pubitemid 351156532)
8. C.M. Cirimotich, Y. Dong, L.S. Garver, S. Sim, and G. Dimopoulos Mosquito immune defenses against Plasmodium infection Dev. Comp. Immunol. 34 2010 387 395
9. J.H. Connell Diversity in tropical rain forests and coral reefs Science 199 1978 1302 1310
10. C.R. Cox, and M.S. Gilmore Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis Infect. Immun. 75 2007 1565 1576 (Pubitemid 46559420)
11. C. Dale, and N.A. Moran Molecular interactions between bacterial symbionts and their hosts Cell 126 2006 453 465 (Pubitemid 44163611)
12. L. Dethlefsen, M. McFall-Ngai, and D.A. Relman An ecological and evolutionary perspective on human-microbe mutualism and disease Nature 449 2007 811 818 (Pubitemid 47598621)
13. R.J. Dillon, and V.M. Dillon The gut bacteria of insects: nonpathogenic interactions Annu. Rev. Entomol. 49 2004 71 92 (Pubitemid 38192417)
14. Y. Dong, F. Manfredini, and G. Dimopoulos Implication of the mosquito midgut microbiota in the defense against malaria parasites PLoS Pathog. 5 2009 e1000423
15. A.E. Douglas Symbiotic microorganisms: untapped resources for insect pest control Trends Biotechnol. 25 2007 338 342 (Pubitemid 47042920)
16. A.E. Douglas The microbial dimension in insect nutritional ecology Funct. Ecol. 23 2009 38 47
17. J. Duan, H. Chung, E. Troy, and D.L. Kasper Microbial colonization drives expansion of IL-1 receptor 1-expressing and IL-17-producing gamma/delta T cells Cell Host Microbe 7 2010 140 150
18. P.W. Ewald Evolution of Infectious Diseases 1994 Oxford University Press Oxford, UK
19. P.G. Falk, L.V. Hooper, T. Midtvedt, and J.I. Gordon Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology Microbiol. Mol. Biol. Rev. 62 1998 1157 1170 (Pubitemid 28558295)
20. S. Fraune, R. Augustin, F. Anton-Erxleben, J. Wittlieb, C. Gelhaus, V.B. Klimovich, M.P. Samoilovich, and T.C. Bosch In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides Proc. Natl. Acad. Sci. USA 107 2010 18067 18072
21. T. Fukatsu, and T. Hosokawa Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima Appl. Environ. Microbiol. 68 2002 389 396 (Pubitemid 34031201)
22. L.S. Garver, Z. Xi, and G. Dimopoulos Immunoglobulin superfamily members play an important role in the mosquito immune system Dev. Comp. Immunol. 32 2008 519 531 (Pubitemid 351172447)
23. N.M. Gerardo, B. Altincicek, C. Anselme, H. Atamian, S.M. Barribeau, M. de Vos, E.J. Duncan, J.D. Evans, T. Gabaldón, and M. Ghanim Immunity and other defenses in pea aphids, Acyrthosiphon pisum Genome Biol. 11 2010 R21
24. A.K. Hansen, and N.A. Moran Aphid genome expression reveals host-symbiont cooperation in the production of amino acids Proc. Natl. Acad. Sci. USA 108 2011 2849 2854
25. L.M. Hedges, J.C. Brownlie, S.L. O'Neill, and K.N. Johnson Wolbachia and virus protection in insects Science 322 2008 702
26. T. Hosokawa, Y. Kikuchi, and T. Fukatsu How many symbionts are provided by mothers, acquired by offspring, and needed for successful vertical transmission in an obligate insect-bacterium mutualism? Mol. Ecol. 16 2007 5316 5325 (Pubitemid 350265267)
27. M. Hussain, F.D. Frentiu, L.A. Moreira, S.L. O'Neill, and S. Asgari Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti Proc. Natl. Acad. Sci. USA 108 2011 9250 9255
28. International Aphid Genomics Consortium Genome sequence of the pea aphid Acyrthosiphon pisum PLoS Biol. 8 2010 e1000313
29. J. Jaenike, R. Unckless, S.N. Cockburn, L.M. Boelio, and S.J. Perlman Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont Science 329 2010 212 215
30. M. Kaltenpoth, W. Göttler, G. Herzner, and E. Strohm Symbiotic bacteria protect wasp larvae from fungal infestation Curr. Biol. 15 2005 475 479 (Pubitemid 40323536)
31. R. Kerney, E. Kim, R.P. Hangarter, A.A. Heiss, C.D. Bishop, and B.K. Hall Intracellular invasion of green algae in a salamander host Proc. Natl. Acad. Sci. USA 108 2011 6497 6502
32. N. Kremer, D. Voronin, D. Charif, P. Mavingui, B. Mollereau, and F. Vavre Wolbachia interferes with ferritin expression and iron metabolism in insects PLoS Pathog. 5 2009 e1000630
33. J. Kroiss, M. Kaltenpoth, B. Schneider, M.G. Schwinger, C. Hertweck, R.K. Maddula, E. Strohm, and A. Svatos Symbiotic Streptomycetes provide antibiotic combination prophylaxis for wasp offspring Nat. Chem. Biol. 6 2010 261 263
34. Y.K. Lee, and S.K. Mazmanian Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330 2010 1768 1773
35. B. Lemaitre, and J. Hoffmann The host defense of Drosophila melanogaster Annu. Rev. Immunol. 25 2007 697 743 (Pubitemid 46697922)
36. S.J. MacDonald, G.H. Thomas, and A.E. Douglas Genetic and metabolic determinants of nutritional phenotype in an insect-bacterial symbiosis Mol. Ecol. 20 2011 2073 2084
37. J.P. McCutcheon, and N.A. Moran Parallel genomic evolution and metabolic interdependence in an ancient symbiosis Proc. Natl. Acad. Sci. USA 104 2007 19392 19397
38. J.P. McCutcheon, and N.A. Moran Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution Genome Biol Evol 2 2010 708 718
39. J.P. McCutcheon, B.R. McDonald, and N.A. Moran Convergent evolution of metabolic roles in bacterial co-symbionts of insects Proc. Natl. Acad. Sci. USA 106 2009 15394 15399
40. M.J. McFall-Ngai Unseen forces: the influence of bacteria on animal development Dev. Biol. 242 2002 1 14 (Pubitemid 34113666)
41. M. McFall-Ngai Adaptive immunity: care for the community Nature 445 2007 153 (Pubitemid 46095705)
42. E.A. McGraw, D.J. Merritt, J.N. Droller, and S.L. O'Neill Wolbachia density and virulence attenuation after transfer into a novel host Proc. Natl. Acad. Sci. USA 99 2002 2918 2923 (Pubitemid 34240561)
43. J. Morales-Jiménez, G. Zúñiga, L. Villa-Tanaca, and C. Hernández-Rodríguez Bacterial community and nitrogen fixation in the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Curculionidae: Scolytinae) Microb. Ecol. 58 2009 879 891
44. N.A. Moran, M.A. Munson, P. Baumann, and H. Ishikawa A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts Proc. Biol. Sci. 253 1993 167 171
45. N.A. Moran, P. Tran, and N.M. Gerardo Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes Appl. Environ. Microbiol. 71 2005 8802 8810 (Pubitemid 41804017)
46. U.G. Mueller, D. Dash, C. Rabeling, and A. Rodrigues Coevolution between attine ants and actinomycete bacteria: a reevaluation Evolution 62 2008 2894 2912
47. D.R. Nemergut, E.K. Costello, M. Hamady, C. Lozupone, L. Jiang, S.K. Schmidt, N. Fierer, A.R. Townsend, C.C. Cleveland, L. Stanish, and R. Knight Global patterns in the biogeography of bacterial taxa Environ. Microbiol. 13 2011 135 144
48. J.H. Niess, F. Leithäuser, G. Adler, and J. Reimann Commensal gut flora drives the expansion of proinflammatory CD4 T cells in the colonic lamina propria under normal and inflammatory conditions J. Immunol. 180 2008 559 568
49. D.C. Oh, M. Poulsen, C.R. Currie, and J. Clardy Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis Nat. Chem. Biol. 5 2009 391 393
50. P.L. Oh, A.K. Benson, D.A. Peterson, P.B. Patil, E.N. Moriyama, S. Roos, and J. Walter Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution ISME J. 4 2010 377 387
51. K.M. Oliver, P.H. Degnan, M.S. Hunter, and N.A. Moran Bacteriophages encode factors required for protection in a symbiotic mutualism Science 325 2009 992 994
52. K.M. Oliver, P.H. Degnan, G.R. Burke, and N.A. Moran Facultative symbionts in aphids and the horizontal transfer of ecologically important traits Annu. Rev. Entomol. 55 2010 247 266
53. B.A. Pannebakker, B. Loppin, C.P. Elemans, L. Humblot, and F. Vavre Parasitic inhibition of cell death facilitates symbiosis Proc. Natl. Acad. Sci. USA 104 2007 213 215 (Pubitemid 46068011)
54. A. Poliakov, C.W. Russell, L. Ponnala, H.J. Hoops, Q. Sun, A.E. Douglas, and K.J. van Wijk Large-scale label-free quantitative proteomics of the pea aphid-Buchnera symbiosis Mol. Cell Proteomics 10 2011 M110.007039
55. M. Pollard, and N. Sharon Responses of the Peyer's Patches in Germ-Free Mice to Antigenic Stimulation Infect. Immun. 2 1970 96 100
56. C. Ren, P. Webster, S.E. Finkel, and J. Tower Increased internal and external bacterial load during Drosophila aging without life-span trade-off Cell Metab. 6 2007 144 152 (Pubitemid 47163619)
57. N. Reymond, F. Calevro, J. Viñuelas, N. Morin, Y. Rahbé, G. Febvay, C. Laugier, A.E. Douglas, J.-M. Fayard, and H. Charles Different levels of transcriptional regulation due to trophic constraints in the reduced genome of Buchnera aphidicola APS Appl. Environ. Microbiol. 72 2006 7760 7766 (Pubitemid 44927682)
58. C.J. Robinson, P. Schloss, Y. Ramos, K. Raffa, and J. Handelsman Robustness of the bacterial community in the cabbage white butterfly larval midgut Microb. Ecol. 59 2010 199 211
59. S.W. Roh, Y.D. Nam, H.W. Chang, K.H. Kim, M.S. Kim, J.H. Ryu, S.H. Kim, W.J. Lee, and J.W. Bae Phylogenetic characterization of two novel commensal bacteria involved with innate immune homeostasis in Drosophila melanogaster Appl. Environ. Microbiol. 74 2008 6171 6177
60. J. Rolff Why did the acquired immune system of vertebrates evolve? Dev. Comp. Immunol. 31 2007 476 482 (Pubitemid 46109038)
61. J.L. Round, S.M. Lee, J. Li, G. Tran, B. Jabri, T.A. Chatila, and S.K. Mazmanian The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota Science 332 2011 974 977
62. J.H. Ryu, S.H. Kim, H.Y. Lee, J.Y. Bai, Y.D. Nam, J.W. Bae, D.G. Lee, S.C. Shin, E.M. Ha, and W.J. Lee Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila Science 319 2008 777 782
63. T.B. Sackton, B.P. Lazzaro, T.A. Schlenke, J.D. Evans, D. Hultmark, and A.G. Clark Dynamic evolution of the innate immune system in Drosophila Nat. Genet. 39 2007 1461 1468 (Pubitemid 350191353)
64. C.L. Scarborough, J. Ferrari, and H.C. Godfray Aphid protected from pathogen by endosymbiont Science 310 2005 1781
65. J.J. Scott, D.C. Oh, M.C. Yuceer, K.D. Klepzig, J. Clardy, and C.R. Currie Bacterial protection of beetle-fungus mutualism Science 322 2008 63
66. S. Shanbhag, and S. Tripathi Epithelial ultrastructure and cellular mechanisms of acid and base transport in the Drosophila midgut J. Exp. Biol. 212 2009 1731 1744
67. S. Shigenobu, H. Watanabe, M. Hattori, Y. Sakaki, and H. Ishikawa Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS Nature 407 2000 81 86
68. T.S. Stappenbeck, L.V. Hooper, and J.I. Gordon Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells Proc. Natl. Acad. Sci. USA 99 2002 15451 15455 (Pubitemid 35403955)
69. K.J. Vogel, and N.A. Moran Sources of variation in dietary requirements in an obligate nutritional symbiosis Proc. Biol. Sci. 278 2011 115 121
70. Z. Wang, E. Klipfell, B.J. Bennett, R. Koeth, B.S. Levison, B. Dugar, A.E. Feldstein, E.B. Britt, X. Fu, and Y.M. Chung Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease Nature 472 2011 57 63
71. F. Warnecke, P. Luginbühl, N. Ivanova, M. Ghassemian, T.H. Richardson, J.T. Stege, M. Cayouette, A.C. McHardy, G. Djordjevic, and N. Aboushadi Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite Nature 450 2007 560 565 (Pubitemid 350190243)
72. H. Watanabe, and G. Tokuda Cellulolytic systems in insects Annu. Rev. Entomol. 55 2010 609 632
73. J.H. Werren, L. Baldo, and M.E. Clark Wolbachia: master manipulators of invertebrate biology Nat. Rev. Microbiol. 6 2008 741 751
74. H. Wieczorek, K.W. Beyenbach, M. Huss, and O. Vitavska Vacuolar-type proton pumps in insect epithelia J. Exp. Biol. 212 2009 1611 1619
75. A.C. Wilson, H.E. Dunbar, G.K. Davis, W.B. Hunter, D.L. Stern, and N.A. Moran A dual-genome microarray for the pea aphid, Acyrthosiphon pisum, and its obligate bacterial symbiont, Buchnera aphidicola BMC Genomics 7 2006 50
76. C.N. Wong, P. Ng, and A.E. Douglas Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster Environ. Microbiol. 13 2011 1889 1900
77. J. Xie, I. Vilchez, and M. Mateos Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma PLoS ONE 5 2010 e12149