1932

Abstract

All insects are colonized by microorganisms on the insect exoskeleton, in the gut and hemocoel, and within insect cells. The insect microbiota is generally different from microorganisms in the external environment, including ingested food. Specifically, certain microbial taxa are favored by the conditions and resources in the insect habitat, by their tolerance of insect immunity, and by specific mechanisms for their transmission. The resident microorganisms can promote insect fitness by contributing to nutrition, especially by providing essential amino acids, B vitamins, and, for fungal partners, sterols. Some microorganisms protect their insect hosts against pathogens, parasitoids, and other parasites by synthesizing specific toxins or modifying the insect immune system. Priorities for future research include elucidation of microbial contributions to detoxification, especially of plant allelochemicals in phytophagous insects, and resistance to pathogens; as well as their role in among-insect communication; and the potential value of manipulation of the microbiota to control insect pests.

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2015-01-07
2024-04-26
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Literature Cited

  1. Adams AS, Aylward FO, Adams SM, Erbilgin N, Aukema BH. 1.  et al. 2013. Mountain pine beetles colonizing historical and naive host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl. Environ. Microbiol. 79:3468–75 [Google Scholar]
  2. Adams AS, Six DL. 2.  2008. Detection of host habitat by parasitoids using cues associated with mycangial fungi of the mountain pine beetle, Dendroctonua ponderosae. Can. Entomol. 140:124–27 [Google Scholar]
  3. Aharon Y, Pasternak Z, Ben Yosef M, Behar A, Lauzon C. 3.  et al. 2013. Phylogenetic, metabolic, and taxonomic diversities shape Mediterranean fruit fly microbiotas during ontogeny. Appl. Environ. Microbiol. 79:303–13 [Google Scholar]
  4. Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T. 4.  et al. 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32:402–7 [Google Scholar]
  5. Andert J, Marten A, Brandl R, Brune A. 5.  2010. Inter- and intraspecific comparison of the bacterial assemblages in the hindgut of humivorous scarab beetle larvae (Pachnoda spp.). FEMS Microbiol. Ecol. 74:439–49 [Google Scholar]
  6. Anselme C, Vallier A, Balmand S, Fauvarque MO, Heddi A. 6.  2006. Host PGRP gene expression and bacterial release in endosymbiosis of the weevil Sitophilus zeamais. Appl. Environ. Microbiol. 72:6766–72 [Google Scholar]
  7. Bansal R, Hulbert S, Schemerhorn B, Reese JC, Whitworth RJ. 7.  et al. 2011. Hessian fly-associated bacteria: transmission, essentiality, and composition. PLOS ONE 6:e23170 [Google Scholar]
  8. Berenbaum M. 8.  1980. Adaptive significance of midgut pH in larval Lepidoptera. Am. Nat. 115:138–46 [Google Scholar]
  9. Bian G, Joshi D, Dong Y, Lu P, Zhou G. 9.  et al. 2013. Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 340:748–51 [Google Scholar]
  10. Braendle C, Miura T, Bickel R, Shingleton AW, Kambhampati S, Stern DL. 10.  2003. Developmental origin and evolution of bacteriocytes in the aphid-Buchnera symbiosis. PLoS Biol. 1:E21 [Google Scholar]
  11. Bright M, Bulgheresi S. 11.  2010. A complex journey: transmission of microbial symbionts. Nat. Rev. Microbiol. 8:218–30 [Google Scholar]
  12. Brown AM, Huynh LY, Bolender CM, Nelson KG, McCutcheon JP. 12.  2014. Population genomics of a symbiont in the early stages of a pest invasion. Mol. Ecol. 23:1516–30 [Google Scholar]
  13. Brucker RM, Bordenstein SR. 13.  2012. The roles of host evolutionary relationships (genus: Nasonia) and development in structuring microbial communities. Evolution 66:349–62 [Google Scholar]
  14. Brune A. 14.  2006. Symbiotic associations between termites and prokaryotes. The Prokaryotes M Dworkin, S Falkow, E Rosenberg, K-H Schleifer, E Stackebrandt 439–74 1 New York: Springer [Google Scholar]
  15. Brune A. 15.  2010. Methanogenesis in the digestive tracts of insects. Handbook of Hydrocarbon and Lipid Microbiology KN Timmis 706–28 Berlin: Springer-Verlag [Google Scholar]
  16. Buchner P. 16.  1965. Endosymbioses of Animals with Plant Microorganisms Chichester, UK: Wiley
  17. Calderon-Cortes N, Quesada M, Watanabe H, Cano-Camacho H, Oyama K. 17.  2012. Endogenous plant cell wall digestion: a key mechanism in insect evolution. Annu. Rev. Ecol. Evol. Syst. 43:45–71 [Google Scholar]
  18. Capuzzo C, Firrao G, Mazzon L, Squartini A, Girolami V. 18.  2005. ‘Candidatus Erwinia dacicola’, a coevolved symbiotic bacterium of the olive fly Bactrocera oleae (Gmelin). Int. J. Syst. Evol. Microbiol. 55:1641–47 [Google Scholar]
  19. Cardoza YJ, Klepzig KD, Raffa KF. 19.  2006. Bacteria in oral secretions of an endophytic insect inhibit antagonistic fungi. Ecol. Entomol. 31:636–45 [Google Scholar]
  20. Chandler JA, James PM. 20.  2013. Discovery of trypanosomatid parasites in globally distributed Drosophila species. PLOS ONE 8:e61937 [Google Scholar]
  21. Chandler JA, Lang JM, Bhatnagar S, Eisen JA, Kopp A. 21.  2011. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLOS Genet. 7:e1002272 [Google Scholar]
  22. Cirimotich CM, Dong Y, Clayton AM, Sandiford SL, Souza-Neto JA. 22.  et al. 2011. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 332:855–58 [Google Scholar]
  23. Conrad C, Despres L, Vallier A, Balmand S, Miquel C. 23.  et al. 2008. Long-term evolutionary stability of bacterial endosymbiosis in Curculionoidea: additional evidence of symbiont replacement in the Dryophthoridae family. Mol. Biol. Evol. 25:859–68 [Google Scholar]
  24. 24. Consort. Hum. Microb 2012. A framework for human microbiome research. Nature 486:215–21 [Google Scholar]
  25. Crotti E, Rizzi A, Chouaia B, Ricci I, Favia G. 25.  et al. 2010. Acetic acid bacteria, newly emerging symbionts of insects. Appl. Environ. Microbiol. 76:6963–70 [Google Scholar]
  26. Currie CR, Poulsen M, Mendenhall J, Boomsma JJ, Billen J. 26.  2006. Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311:81–83 [Google Scholar]
  27. Currie CR, Scott JA, Summerbell RC, Malloch D. 27.  1999. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701–4 [Google Scholar]
  28. Currie CR, Wong B, Stuart AE, Schultz TR, Rehner SA. 28.  et al. 2003. Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 299:386–88 [Google Scholar]
  29. Daffre S, Kylsten P, Samakovlis C, Hultmark D. 29.  1994. The lysozyme locus in Drosophila melanogaster: an expanded gene family adapted for expression in the digestive tract. Mol. Gen. Genet. 242:152–62 [Google Scholar]
  30. De Fine Licht HH, Schiøtt M, Rogowska-Wrzesinska A, Nygaard S, Roepstorff P, Boomsma JJ. 30.  2013. Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts. Proc. Natl. Acad. Sci. USA 110:583–87 [Google Scholar]
  31. Degnan PH, Moran NA. 31.  2008. Diverse phage-encoded toxins in a protective insect endosymbiont. Appl. Environ. Microbiol. 74:6782–91 [Google Scholar]
  32. Diaz-Albiter H, Sant'Anna MR, Genta FA, Dillon RJ. 32.  2012. Reactive oxygen species-mediated immunity against Leishmania mexicana and Serratia marcescens in the sand phlebotomine fly Lutzomyia longipalpis. J. Biol. Chem. 287:23995–4003 [Google Scholar]
  33. Dillon R, Charnley K. 33.  2002. Mutualism between the desert locust Schistocerca gregaria and its gut microbiota. Res. Microbiol. 153:503–9 [Google Scholar]
  34. Dostálová A, Volf P. 34.  2012. Leishmania development in sand flies: parasite-vector interactions overview. Parasites Vectors 5:276 [Google Scholar]
  35. Douglas AE. 35.  1989. Mycetocyte symbiosis in insects. Biol. Rev. 64:409–34 [Google Scholar]
  36. Douglas AE. 36.  2006. Phloem-sap feeding by animals: problems and solutions. J. Exp. Bot. 57:747–54 [Google Scholar]
  37. Douglas AE. 37.  2009. The microbial dimension in insect nutritional ecology. Funct. Ecol. 23:38–47 [Google Scholar]
  38. Douglas AE, Dobson AJ. 38.  2013. New synthesis: animal communication mediated by microbes: fact or fantasy?. J. Chem. Ecol. 39:1149 [Google Scholar]
  39. Douglas AE, Minto LB, Wilkinson TL. 39.  2001. Quantifying nutrient production by the microbial symbionts in an aphid. J. Exp. Biol. 204:349–58 [Google Scholar]
  40. Dowd PF, Shen SK. 40.  1990. The contribution of symbiotic yeast to toxin resistance of the cigarette beetle (Lasioderma serricorne). Entomol. Exp. Appl. 56:241–48 [Google Scholar]
  41. Durvasula RV, Gumbs A, Panackal A, Kruglov O, Aksoy S. 41.  et al. 1997. Prevention of insect-borne disease: an approach using transgenic symbiotic bacteria. Proc. Natl. Acad. Sci. USA 94:3274–78 [Google Scholar]
  42. Engel P, Martinson VG, Moran NA. 42.  2012. Functional diversity within the simple gut microbiota of the honey bee. Proc. Natl. Acad. Sci. USA 109:11002–7 [Google Scholar]
  43. Ezenwa VO, Gerardo NM, Inouye DW, Medina M, Xavier JB. 43.  2012. Microbiology: animal behavior and the microbiome. Science 338:198–99 [Google Scholar]
  44. Febvay G, Rahbe Y, Rynkiewicz M, Guillaud J, Bonnot G. 44.  1999. Fate of dietary sucrose and neosynthesis of amino acids in the pea aphid, Acyrthosiphon pisum, reared on different diets. J. Exp. Biol. 202:2639–52 [Google Scholar]
  45. Feldhaar H, Straka J, Krischke M, Berthold K, Stoll S. 45.  et al. 2007. Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol. 5:48 [Google Scholar]
  46. Findley K, Yang J, Conlan S, Deming C. 46.  et al. 2013. Topographic diversity of fungal and bacterial communities in human skin. Nature 498:367–70 [Google Scholar]
  47. Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM. 47.  et al. 2010. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol. 11:R21 [Google Scholar]
  48. Gill EE, Brinkman FS. 48.  2011. The proportional lack of archaeal pathogens: Do viruses/phages hold the key?. BioEssays 33:248–54 [Google Scholar]
  49. Ha EM, Oh CT, Bae YS, Lee WJ. 49.  2005. A direct role for dual oxidase in Drosophila gut immunity. Science 310:847–50 [Google Scholar]
  50. Hansen AK, Moran NA. 50.  2014. The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol. Ecol. 23:1473–96 [Google Scholar]
  51. Harrison JF. 51.  2001. Insect acid-base physiology. Annu. Rev. Entomol. 46:221–50 [Google Scholar]
  52. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE. 52.  et al. 2011. Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254–56 [Google Scholar]
  53. Hosokawa T, Kikuchi Y, Meng XY, Fukatsu T. 53.  2005. The making of symbiont capsule in the plataspid stinkbug Megacopta punctatissima. FEMS Microbiol. Ecol. 54:471–77 [Google Scholar]
  54. Huang S-W, Zhang H-Y, Marshall S, Jackson TA. 54.  2010. The scarab gut: a potential bioreactor for bio-fuel production. Insect. Sci. 17:175–83 [Google Scholar]
  55. Hughes GL, Koga R, Xue P, Fukatsu T, Rasgon JL. 55.  2011. Wolbachia infections are virulent and inhibit the human malaria parasite Plasmodium falciparum in Anopheles gambiae. PLoS Pathog. 7:e1002043 [Google Scholar]
  56. Hulcr J, Rountree NR, Diamond SE, Stelinski LL, Fierer N, Dunn RR. 56.  2012. Mycangia of ambrosia beetles host communities of bacteria. Microb. Ecol. 64:784–93 [Google Scholar]
  57. Hurwitz I, Fieck A, Read A, Hillesland H, Klein N. 57.  et al. 2011. Paratransgenic control of vector borne diseases. Int. J. Biol. Sci. 7:1334–44 [Google Scholar]
  58. Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ. 58.  2010. Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212–15 [Google Scholar]
  59. Jakubowska AK, Vogel H, Herrero S. 59.  2013. Increase in gut microbiota after immune suppression in baculovirus-infected larvae. PLOS Pathog. 9:e1003379 [Google Scholar]
  60. Kaltenpoth M, Gottler W, Herzner G, Strohm E. 60.  2005. Symbiotic bacteria protect wasp larvae from fungal infestation. Curr. Biol. 15:475–79 [Google Scholar]
  61. Kaltenpoth M, Yildirim E, Gürbüz MF, Herzner G, Strohm E. 61.  2012. Refining the roots of the beewolf-Streptomyces symbiosis: antennal symbionts in the rare genus Philanthinus (Hymenoptera, Crabronidae). Appl. Environ. Microbiol. 78:822–27 [Google Scholar]
  62. Kambris Z, Blagborough AM, Pinto SB, Blagrove MS, Godfray HC. 62.  et al. 2010. Wolbachia stimulates immune gene expression and inhibits Plasmodium development in Anopheles gambiae. PLoS Pathog. 6e1001143
  63. Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T. 63.  2012. Symbiont-mediated insecticide resistance. Proc. Natl. Acad. Sci. USA 109:8618–22 [Google Scholar]
  64. Koch H, Cisarovsky G, Schmid-Hempel P. 64.  2012. Ecological effects on gut bacterial communities in wild bumblebee colonies. J. Anim. Ecol. 81:1202–10 [Google Scholar]
  65. Koga R, Bennett GM, Cryan JR, Moran NA. 65.  2013. Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage. Environ. Microbiol. 15:2073–81 [Google Scholar]
  66. Koga R, Meng XY, Tsuchida T, Fukatsu T. 66.  2012. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. Proc. Natl. Acad. Sci. USA 109:E1230–37 [Google Scholar]
  67. Köhler T, Dietrich C, Scheffrahn RH, Brune A. 67.  2012. High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher termites (Nasutitermes spp.). Appl. Environ. Microbiol. 78:4691–701 [Google Scholar]
  68. Kuechler SM, Dettner K, Kehl S. 68.  2011. Characterization of an obligate intracellular bacterium in the midgut epithelium of the bulrush bug Chilacis typhae (Heteroptera, Lygaeidae, Artheneinae). Appl. Environ. Microbiol. 77:2869–76 [Google Scholar]
  69. Kwong WK, Moran NA. 69.  2013. Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order ‘Enterobacteriales’ of the Gammaproteobacteria. Int. J. Syst. Evol. Microbiol. 63:2008–18 [Google Scholar]
  70. Lemaitre B, Miguel-Aliaga I. 70.  2013. The digestive tract of Drosophila melanogaster. Annu. Rev. Genet. 47:377–404 [Google Scholar]
  71. Login FH, Balmand S, Vallier A, Vincent-Monegat C, Vigneron A. 71.  et al. 2011. Antimicrobial peptides keep insect endosymbionts under control. Science 334:362–65 [Google Scholar]
  72. Macdonald SJ, Lin GG, Russell CW, Thomas GH, Douglas AE. 72.  2012. The central role of the host cell in symbiotic nitrogen metabolism. Proc. R. Soc. Lond. B 279:2965–73 [Google Scholar]
  73. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA. 73.  2011. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol. Ecol. 20:619–28 [Google Scholar]
  74. Maslov DA, Votypka J, Yurchenko V, Lukes J. 74.  2013. Diversity and phylogeny of insect trypanosomatids: All that is hidden shall be revealed. Trends Parasitol. 29:43–52 [Google Scholar]
  75. McCutcheon JP, Moran NA. 75.  2007. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc. Natl. Acad. Sci. USA 104:19392–97 [Google Scholar]
  76. McCutcheon JP, Moran NA. 76.  2012. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10:13–26 [Google Scholar]
  77. McMeniman CJ, Lane RV, Cass BN, Fong AW, Sidhu M. 77.  et al. 2009. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323:141–44 [Google Scholar]
  78. Minard G, Tran FH, Raharimalala FN, Hellard E, Ravelonandro P. 78.  et al. 2013. Prevalence, genomic and metabolic profiles of Acinetobacter and Asaia associated with field-caught Aedes albopictus from Madagascar. FEMS Microbiol. Ecol. 83:63–73 [Google Scholar]
  79. Morales-Jiménez J, Zúñiga G, Villa-Tanaca L, Hernández-Rodríguez C. 79.  2009. Bacterial community and nitrogen fixation in the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Curculionidae: Scolytinae). Microb. Ecol. 58:879–91 [Google Scholar]
  80. Nakabachi A, Shigenobu S, Sakazume N, Shiraki T, Hayashizaki Y. 80.  et al. 2005. Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera. Proc. Natl. Acad. Sci. USA 102:5477–82 [Google Scholar]
  81. Nakabachi A, Ueoka R, Oshima K, Teta R, Mangoni A. 81.  et al. 2013. Defensive bacteriome symbiont with a drastically reduced genome. Curr. Biol. 23:1478–84 [Google Scholar]
  82. Nardi JB, Mackie RI, Dawson JO. 82.  2002. Could microbial symbionts of arthropod guts contribute significantly to nitrogen fixation in terrestrial ecosystems?. J. Insect Physiol. 48:751–63 [Google Scholar]
  83. Nasir H, Noda H. 83.  2003. Yeast-like symbiotes as a sterol source in anobiid beetles (Coleoptera, Anobiidae): possible metabolic pathways from fungal sterols to 7-dehydrocholesterol. Arch. Insect Biochem. Physiol. 52:175–82 [Google Scholar]
  84. Newell PD, Douglas AE. 84.  2014. Interspecies interactions determine the impact of the gut microbiota on nutrient allocation in Drosophila melanogaster. Appl. Environ. Microbiol. 80:788–96 [Google Scholar]
  85. Newman KL, Almeida RP, Purcell AH, Lindow SE. 85.  2004. Cell-cell signaling controls Xylella fastidiosa interactions with both insects and plants. Proc. Natl. Acad. Sci. USA 101:1737–42 [Google Scholar]
  86. Noda H, Koizumi Y. 86.  2003. Sterol biosynthesis by symbiotes: cytochrome P450 sterol C-22 desaturase genes from yeastlike symbiotes of rice planthoppers and anobiid beetles. Insect Biochem. Mol. Biol. 33:649–58 [Google Scholar]
  87. Ohkuma M, Noda S, Kudo T. 87.  1999. Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl. Environ. Microbiol. 65:4926–34 [Google Scholar]
  88. Oliver KM, Moran NA, Hunter MS. 88.  2005. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc. Natl. Acad. Sci. USA 102:12795–800 [Google Scholar]
  89. Piel J. 89.  2002. A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of Paederus beetles. Proc. Natl. Acad. Sci. USA 99:14002–7 [Google Scholar]
  90. Potrikus CJ, Breznak JA. 90.  1981. Gut bacteria recycle uric acid nitrogen in termites: a strategy for nutrient conservation. Proc. Natl. Acad. Sci. USA 78:4601–5 [Google Scholar]
  91. Price DR, Feng H, Baker JD, Bavan S, Luetje CW, Wilson AC. 91.  2014. Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts. Proc. Natl. Acad. Sci. USA 111:320–25 [Google Scholar]
  92. Ren C, Webster P, Finkel SE, Tower J. 92.  2007. Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metab. 6:144–52 [Google Scholar]
  93. Russell CW, Bouvaine S, Newell PD, Douglas AE. 93.  2013. Shared metabolic pathways in a coevolved insect-bacterial symbiosis. Appl. Environ. Microbiol. 79:6117–23 [Google Scholar]
  94. Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE. 94.  2009. Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc. Natl. Acad. Sci. USA 106:21236–41 [Google Scholar]
  95. Sabree ZL, Kambhampati S, Moran NA. 95.  2009. Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc. Natl. Acad. Sci. USA 106:19521–26 [Google Scholar]
  96. Sachs JL, Skophammer RG, Regus JU. 96.  2011. Evolutionary transitions in bacterial symbiosis. Proc. Natl. Acad. Sci. USA 108:Suppl. 210800–7 [Google Scholar]
  97. Santo Domingo JW, Kaufman MG, Klug MJ, Holben WE, Harris D, Tiedje JM. 97.  1998. Influence of diet on the structure and function of the bacterial hindgut community of crickets. Mol. Ecol. 7:761–67 [Google Scholar]
  98. Sasaki T, Kawamura M, Ishikawa H. 98.  1996. Nitrogen recycling in the brown planthopper, Nilaparvata lugens: involvement of yeast-like endosymbionts in uric acid metabolism. J. Insect Physiol. 42:125–29 [Google Scholar]
  99. Scarborough CL, Ferrari J, Godfray HC. 99.  2005. Aphid protected from pathogen by endosymbiont. Science 310:1781 [Google Scholar]
  100. Schauer C, Thompson CL, Brune A. 100.  2012. The bacterial community in the gut of the cockroach Shelfordella lateralis reflects the close evolutionary relatedness of cockroaches and termites. Appl. Environ. Microbiol. 78:2758–67 [Google Scholar]
  101. Scott JJ, Oh DC, Yuceer MC, Klepzig KD, Clardy J, Currie CR. 101.  2008. Bacterial protection of beetle-fungus mutualism. Science 322:63 [Google Scholar]
  102. Shanbhag S, Tripathi S. 102.  2009. Epithelial ultrastructure and cellular mechanisms of acid and base transport in the Drosophila midgut. J. Exp. Biol. 212:1731–44 [Google Scholar]
  103. Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E. 103.  2010. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 107:20051–56 [Google Scholar]
  104. Shen SK, Dowd PF. 104.  1991. Detoxification spectrum of the cigarette beetle symbiont Symbiotaphrina kochii in culture. Entomol. Exp. Appl. 60:51–59 [Google Scholar]
  105. Shigenobu S, Stern DL. 105.  2013. Aphids evolved novel secreted proteins for symbiosis with bacterial endosymbiont. Proc. R. Soc. Lond. B 280:20121952 [Google Scholar]
  106. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H. 106.  2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81–86 [Google Scholar]
  107. Sudakaran S, Salem H, Kost C, Kaltenpoth M. 107.  2012. Geographical and ecological stability of the symbiotic mid-gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae). Mol. Ecol. 21:6134–51 [Google Scholar]
  108. Sun J, Lu M, Gillette NE, Wingfield MJ. 108.  2013. Red turpentine beetle: innocuous native becomes invasive tree killer in China. Annu. Rev. Entomol. 58:293–311 [Google Scholar]
  109. Taerum SJ, Duong TA, de Beer ZW, Gillette N, Sun JH. 109.  et al. 2013. Large shift in symbiont assemblage in the invasive red turpentine beetle. PLOS ONE 8:e78126 [Google Scholar]
  110. Tang X, Freitak D, Vogel H, Ping L, Shao Y. 110.  et al. 2012. Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. PLOS ONE 7:e36978 [Google Scholar]
  111. Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G. 111.  2011. Environmental and gut Bacteroidetes: the food connection. Front. Microbiol. 2:93 [Google Scholar]
  112. Thompson BM, Grebenok RJ, Behmer ST, Gruner DS. 112.  2013. Microbial symbionts shape the sterol profile of the xylem-feeding woodwasp, Sirex noctilio. J. Chem. Ecol. 39:129–39 [Google Scholar]
  113. Tokuda G, Elbourne LD, Kinjo Y, Saitoh S, Sabree Z. 113.  et al. 2013. Maintenance of essential amino acid synthesis pathways in the Blattabacterium cuenoti symbiont of a wood-feeding cockroach. Biol. Lett. 9:20121153 [Google Scholar]
  114. Tsai YL, Hayward RE, Langer RC, Fidock DA, Vinetz JM. 114.  2001. Disruption of Plasmodium falciparum chitinase markedly impairs parasite invasion of mosquito midgut. Infect. Immun. 69:4048–54 [Google Scholar]
  115. Valiente Moro C, Tran FH, Raharimalala FN, Ravelonandro P, Mavingui P. 115.  2013. Diversity of culturable bacteria including Pantoea in wild mosquito Aedes albopictus. BMC Microbiol. 13:70 [Google Scholar]
  116. Vallet-Gely I, Lemaitre B, Boccard F. 116.  2008. Bacterial strategies to overcome insect defences. Nat. Rev. Microbiol. 6:302–13 [Google Scholar]
  117. Vogel KJ, Moran NA. 117.  2013. Functional and evolutionary analysis of the genome of an obligate fungal symbiont. Genome Biol. Evol. 5:891–904 [Google Scholar]
  118. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD. 118.  et al. 2011. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476:450–53 [Google Scholar]
  119. Wang J, Wu Y, Yang G, Aksoy S. 119.  2009. Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Proc. Natl. Acad. Sci. USA 106:12133–38 [Google Scholar]
  120. Warnecke F, Luginbuhl P, Ivanova N, Ghassemian M, Richardson TH. 120.  et al. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–65 [Google Scholar]
  121. Wong AC, Chaston JM, Douglas AE. 121.  2013. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J. 7:1922–32 [Google Scholar]
  122. Yek SH, Mueller UG. 122.  2011. The metapleural gland of ants. Biol. Rev. 86:774–91 [Google Scholar]
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