1932

Abstract

Symbiotic associations with microorganisms represent major sources of ecological and evolutionary innovations in insects. Multiple insect taxa engage in symbioses with bacteria of the genus a diverse group that is widespread across different environments and whose members can be mutualistic or pathogenic to plants, fungi, and animals. symbionts provide nutritional benefits and resistance against insecticides to stinkbugs, defend beetle eggs against pathogenic fungi, and may be involved in nitrogen metabolism in ants. In contrast to many other insect symbioses, the known associations with are characterized by environmental symbiont acquisition or mixed-mode transmission, resulting in interesting ecological and evolutionary dynamics of symbiont strain composition. Insect– symbioses present valuable model systems from which to derive insights into general principles governing symbiotic interactions because they are often experimentally and genetically tractable and span a large fraction of the diversity of functions, localizations, and transmission routes represented in insect symbioses.

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2020-01-07
2024-04-14
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Literature Cited

  1. 1. 
    Angus AA, Agapakis CM, Fong S, Yerrapragada S, Estrada-de los Santos P et al. 2014. Plant-associated aymbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis. PLOS ONE 9:e83779
    [Google Scholar]
  2. 2. 
    Bennett GM, Moran NA. 2013. Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a phloem-feeding insect. Genome Biol. Evol. 5:1675–88
    [Google Scholar]
  3. 3. 
    Beukes CW, Palmer M, Manyaka P, Chan WY, Avontuur JR et al. 2017. Genome data provides high support for generic boundaries in Burkholderia sensu lato. Front. Microbiol. 8:1154
    [Google Scholar]
  4. 4. 
    Bochkareva OO, Moroz EV, Davydov II, Gelfand MS 2018. Genome rearrangements and selection in multi-chromosome bacteria Burkholderia spp. BMC Genom 19:965
    [Google Scholar]
  5. 5. 
    Bongrand C, Ruby EG. 2018. Achieving a multi-strain symbiosis: strain behavior and infection dynamics. ISME J 13:698–706
    [Google Scholar]
  6. 6. 
    Boucias DG, Garcia-Maruniak A, Cherry R, Lu HJ, Maruniak JE, Lietze VU 2012. Detection and characterization of bacterial symbionts in the Heteropteran, Blissus insularis. FEMS Microbiol. Ecol. 82:629–41
    [Google Scholar]
  7. 7. 
    Brader G, Compant S, Vescio K, Mitter B, Trognitz F et al. 2017. Ecology and genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Annu. Rev. Phytopathol. 55:61–83
    [Google Scholar]
  8. 8. 
    Brune A. 2014. Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 12:168–80
    [Google Scholar]
  9. 9. 
    Buchner P. 1953. Endosymbiose der Tiere mit pflanzlichen Mikroorganismen Basel: Birkhäuser
  10. 10. 
    Byeon JH, Seo ES, Lee JB, Lee MJ, Kim JK et al. 2015. A specific cathepsin-L-like protease purified from an insect midgut shows antibacterial activity against gut symbiotic bacteria. Dev. Comp. Immunol. 53:79–84
    [Google Scholar]
  11. 11. 
    Cafaro MJ, Currie CR. 2005. Phylogenetic analysis of mutualistic filamentous bacteria associated with fungus-growing ants. Can. J. Microbiol. 51:441–46
    [Google Scholar]
  12. 12. 
    Carlier A, Fehr L, Pinto-Carbó M, Schäberle T, Reher R et al. 2016. The genome analysis of CandidatusBurkholderia crenata reveals that secondary metabolism may be a key function of the Ardisia crenata leaf nodule symbiosis. Environ. Microbiol. 18:2507–22
    [Google Scholar]
  13. 13. 
    Chevrette MG, Carlson CM, Ortega HE, Thomas C, Ananiev GE et al. 2019. The antimicrobial potential of Streptomyces from insect microbiomes. Nat. Commun. 10:516
    [Google Scholar]
  14. 14. 
    Chewapreecha C, Holden MTG, Vehkala M, Välimäki N, Yang Z et al. 2017. Global and regional dissemination and evolution of Burkholderia pseudomallei. Nat. Microbiol 2:16263
    [Google Scholar]
  15. 15. 
    Choudhary KS, Hudaiberdiev S, Gelencsér Z, Gonçalves Coutinho B, Venturi V, Pongor S 2013. The organization of the quorum sensing luxI/R family genes in Burkholderia. Int. J. Mol. Sci 14:13727–47
    [Google Scholar]
  16. 16. 
    Coenye T, Vandamme P. 2003. Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ. Microbiol. 5:719–29
    [Google Scholar]
  17. 17. 
    Compant S, Nowak J, Coenye T, Clément C, Ait Barka E 2008. Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol. Rev. 32:607–26
    [Google Scholar]
  18. 18. 
    Cotter PA, Stibitz S. 2007. c-di-GMP-mediated regulation of virulence and biofilm formation. Curr. Opin. Microbiol. 10:17–23
    [Google Scholar]
  19. 19. 
    de Leon AVP, Ormeno-Orrillo E, Ramirez-Puebla ST, Rosenblueth M, Esposti MD et al. 2017. Candidatus Dactylopiibacterium carminicum, a nitrogen-fixing symbiont of Dactylopius cochineal insects (Hemiptera: Coccoidea: Dactylopiidae). Genome Biol. Evol. 9:2237–50
    [Google Scholar]
  20. 20. 
    Depoorter E, Bull MJ, Peeters C, Coenye T, Vandamme P, Mahenthiralingam E 2016. Burkholderia: an update on taxonomy and biotechnological potential as antibiotic producers. Appl. Microbiol. Biotechnol. 100:5215–29
    [Google Scholar]
  21. 21. 
    Dereeper A, Guignon V, Blanc G, Audic S, Buffet S et al. 2008. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465–69
    [Google Scholar]
  22. 22. 
    Dobritsa AP, Samadpour M. 2016. Transfer of eleven species of the genus Burkholderia to the genus Paraburkholderia and proposal of Caballeronia gen. nov. to accommodate twelve species of the genera Burkholderia and Paraburkholderia. Int. J. Syst. Evol. Microbiol 66:2836–46
    [Google Scholar]
  23. 23. 
    Dose B, Niehs SP, Scherlach K, Flórez LV, Kaltenpoth M, Hertweck C 2018. Unexpected bacterial origin of the antibiotic icosalide: two-tailed depsipeptide assembly in multifarious Burkholderia symbionts. ACS Chem. Biol. 13:2414–20
    [Google Scholar]
  24. 24. 
    Douglas AE. 2009. The microbial dimension in insect nutritional ecology. Funct. Ecol. 23:38–47
    [Google Scholar]
  25. 25. 
    Douglas AE. 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60:17–34
    [Google Scholar]
  26. 26. 
    Drevinek P, Mahenthiralingam E. 2010. Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin. Microbiol. Infect. 16:821–30
    [Google Scholar]
  27. 27. 
    Eberl L. 2006. Quorum sensing in the genus Burkholderia. Int. J. Med. Microbiol 296:103–10
    [Google Scholar]
  28. 28. 
    Eberl L, Vandamme P. 2016. Members of the genus Burkholderia: good and bad guys. F1000Research 5:1007
    [Google Scholar]
  29. 29. 
    Eilmus S, Heil M. 2009. Bacterial associates of arboreal ants and their putative functions in an obligate ant-plant mutualism. Appl. Environ. Microbiol. 75:4324–32
    [Google Scholar]
  30. 30. 
    Engl T, Kroiss J, Kai M, Nechitaylo T, Svatoš A, Kaltenpoth M 2018. Evolutionary stability of antibiotic protection in a defensive symbiosis. PNAS 115:E2020–29
    [Google Scholar]
  31. 31. 
    Enomoto S, Chari A, Clayton AL, Dale C 2017. Quorum sensing attenuates virulence in Sodalis praecaptivus. Cell Host Microbe 21:629–36
    [Google Scholar]
  32. 32. 
    Estrada-De Los Santos P, Bustillos-Cristales R, Caballero-Mellado J 2001. Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl. Environ. Microbiol. 67:2790–98
    [Google Scholar]
  33. 33. 
    Estrada-de Los Santos P, Palmer M, Chávez-Ramírez B, Beukes C, Steenkamp ET et al. 2018. Whole genome analyses suggests that Burkholderia sensu lato contains two additional novel genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae. Genes 9:E389
    [Google Scholar]
  34. 34. 
    Estrada-de Los Santos P, Vinuesa P, Martínez-Aguilar L, Hirsch AM, Caballero-Mellado J 2013. Phylogenetic analysis of Burkholderia species by multilocus sequence analysis. Curr. Microbiol. 67:51–60
    [Google Scholar]
  35. 35. 
    Faulde M, Spiesberger M. 2013. Role of the moth fly Clogmia albipunctata (Diptera: Psychodinae) as a mechanical vector of bacterial pathogens in German hospitals. J. Hosp. Infect. 83:51–60
    [Google Scholar]
  36. 36. 
    Feldhaar H, Gross R. 2008. Immune reactions of insects on bacterial pathogens and mutualists. Microbes Infect 10:1082–88
    [Google Scholar]
  37. 37. 
    Feldhaar H, Straka J, Krischke M, Berthold K, Stoll S et al. 2007. Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol 5:48
    [Google Scholar]
  38. 38. 
    Flórez LV, Biedermann PHW, Engl T, Kaltenpoth M 2015. Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat. Prod. Rep. 32:904–36
    [Google Scholar]
  39. 39. 
    Flórez LV, Kaltenpoth M. 2017. Symbiont dynamics and strain diversity in the defensive mutualism between Lagria beetles and Burkholderia. Environ. Microbiol 19:3674–88
    [Google Scholar]
  40. 40. 
    Flórez LV, Scherlach K, Gaube P, Ross C, Sitte E et al. 2017. Antibiotic-producing symbionts dynamically transition between plant pathogenicity and insect-defensive mutualism. Nat. Commun. 8:15172
    [Google Scholar]
  41. 41. 
    Flórez LV, Scherlach K, Miller IJ, Rodrigues A, Kwan JC et al. 2018. An antifungal polyketide associated with horizontally acquired genes supports symbiont-mediated defense in Lagria villosa beetles. Nat. Commun. 9:2478
    [Google Scholar]
  42. 42. 
    Fürstenberg-Hägg J, Zagrobelny M, Bak S 2013. Plant defense against insect herbivores. Int. J. Mol. Sci. 14:10242–97
    [Google Scholar]
  43. 43. 
    Futahashi R, Tanaka K, Matsuura Y, Tanahashi M, Kikuchi Y, Fukatsu T 2011. Laccase2 is required for cuticular pigmentation in stinkbugs. Insect Biochem. Mol. Biol. 41:191–96
    [Google Scholar]
  44. 44. 
    Futahashi R, Tanaka K, Tanahashi M, Nikoh N, Kikuchi Y et al. 2013. Gene expression in gut symbiotic organ of stinkbug affected by extracellular bacterial symbiont. PLOS ONE 8:e64557
    [Google Scholar]
  45. 45. 
    Galyov EE, Brett PJ, DeShazer D 2010. Molecular insights into Burkholderia pseudomallei and Burkholderia mallei pathogenesis. Annu. Rev. Microbiol. 64:495–517
    [Google Scholar]
  46. 46. 
    Garcia JR, Laughton AM, Malik Z, Parker BJ, Trincot C et al. 2014. Partner associations across sympatric broad-headed bug species and their environmentally acquired bacterial symbionts. Mol. Ecol. 23:1333–47
    [Google Scholar]
  47. 47. 
    Gonçalves Coutinho B, Das M, Suárez-Moreno ZR, Gonzalez CF, Venturi V 2014. The Phytopathogenic Burkholderia Poole, UK: Caister Academic
  48. 48. 
    Gonzalez-Teuber M, Kaltenpoth M, Boland W 2014. Mutualistic ants as an indirect defence against leaf pathogens. New Phytol 202:640–50
    [Google Scholar]
  49. 49. 
    Gordon ERL, McFrederick Q, Weirauch C 2016. Phylogenetic evidence for ancient and persistent environmental symbiont reacquisition in Largidae (Hemiptera: Heteroptera). Appl. Environ. Microbiol. 82:7123–33
    [Google Scholar]
  50. 50. 
    Hardoim PR, van Overbeek LS, Berg G, Pirttila AM, Compant S et al. 2015. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 79:293–320
    [Google Scholar]
  51. 51. 
    Hopwood DA. 2007. Streptomyces in Nature and Medicine Oxford, UK: Oxford Univ. Press
  52. 52. 
    Hosokawa T, Ishii Y, Nikoh N, Fujie M, Satoh N, Fukatsu T 2016. Obligate bacterial mutualists evolving from environmental bacteria in natural insect populations. Nat. Microbiol. 1:15011
    [Google Scholar]
  53. 53. 
    Hu Y, Sanders JG, Łukasik P, D'Amelio CL, Millar JS et al. 2018. Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome. Nat. Commun. 9:964
    [Google Scholar]
  54. 54. 
    Huber B, Riedel K, Hentzer M, Heydorn A, Gotschlich A et al. 2001. The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147:2517–28
    [Google Scholar]
  55. 55. 
    Irschik H, Schummer D, Höfle G, Reichenbach H, Steinmetz H, Jansen R 2007. Etnangien, a macrolide-polyene antibiotic from Sorangium cellulosum that inhibits nucleic acid polymerases. J. Nat. Prod. 70:1060–63
    [Google Scholar]
  56. 56. 
    Ishii Y, Matsuura Y, Kakizawa S, Nikoh N, Fukatsu T 2013. Diversity of bacterial endosymbionts associated with Macrosteles leafhoppers vectoring phytopathogenic phytoplasmas. Appl. Environ. Microbiol. 79:5013–22
    [Google Scholar]
  57. 57. 
    Itoh H, Aita M, Nagayama A, Meng XY, Kamagata Y et al. 2014. Evidence of environmental and vertical transmission of Burkholderia symbionts in the Oriental chinch cug, Cavelerius saccharivorus (Heteroptera: Blissidae). Appl. Environ. Microbiol. 80:5974–83
    [Google Scholar]
  58. 58. 
    Itoh H, Hori T, Sato Y, Nagayama A, Tago K et al. 2018. Infection dynamics of insecticide-degrading symbionts from soil to insects in response to insecticide spraying. ISME J 12:909–20
    [Google Scholar]
  59. 59. 
    Itoh H, Tago K, Hayatsu M, Kikuchi Y 2018. Detoxifying symbiosis: microbe-mediated detoxification of phytotoxins and pesticides in insects. Nat. Prod. Rep. 35:434–54
    [Google Scholar]
  60. 60. 
    Jang HA, Seo ES, Seong MY, Lee BL 2017. A midgut lysate of the Riptortus pedestris has antibacterial activity against LPS O-antigen-deficient Burkholderia mutants. Dev. Comp. Immunol. 67:97–106
    [Google Scholar]
  61. 61. 
    Jang SH, Jang HA, Lee J, Kim JU, Lee SA et al. 2017. PhaR, a negative regulator of PhaP, modulates the colonization of a Burkholderia gut symbiont in the midgut of the host insect, Riptortus pedestris. Appl. Environ. Microbiol. 83:e00459–17
    [Google Scholar]
  62. 62. 
    Jeong Y, Kim J, Kim S, Kang Y, Nagamatsu T, Hwang I 2003. Toxoflavin produced by Burkholderia glumae causing rice grain rot is responsible for inducing bacterial wilt in many field crops. Plant Dis 87:890–95
    [Google Scholar]
  63. 63. 
    Johansson H, Dhaygude K, Lindström S, Helanterä H, Sundström L, Trontti K 2013. A metatranscriptomic approach to the identification of microbiota associated with the ant Formica exsecta. PLOS ONE 8:e79777
    [Google Scholar]
  64. 64. 
    Johnston-Monje D, Raizada MN. 2011. Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLOS ONE 6:e20396
    [Google Scholar]
  65. 65. 
    Kaiwa N, Hosokawa T, Nikoh N, Tanahashi M, Moriyama M et al. 2014. Symbiont-supplemented maternal investment underpinning host's ecological adaptation. Curr. Biol. 24:2465–70
    [Google Scholar]
  66. 66. 
    Kaltenpoth M. 2009. Actinobacteria as mutualists: general healthcare for insects. ? Trends Microbiol 17:529–35
    [Google Scholar]
  67. 67. 
    Kaltenpoth M, Gottler W, Herzner G, Strohm E 2005. Symbiotic bacteria protect wasp larvae from fungal infestation. Curr. Biol. 15:475–79
    [Google Scholar]
  68. 68. 
    Kaltenpoth M, Roeser-Mueller K, Koehler S, Peterson A, Nechitaylo T et al. 2014. Partner choice and fidelity stabilize co-evolution in a Cretaceous-age defensive symbiosis. PNAS 111:6359–64
    [Google Scholar]
  69. 69. 
    Keller A, Grimmer G, Steffan-Dewenter I 2013. Diverse microbiota identified in whole intact nest chambers of the red mason bee Osmia bicornis (Linnaeus 1758). PLOS ONE 8:e78296
    [Google Scholar]
  70. 70. 
    Kikuchi Y, Fukatsu T. 2014. Live imaging of symbiosis: spatiotemporal infection dynamics of a GFP-labelled Burkholderia symbiont in the bean bug Riptortus pedestris. Mol. Ecol 23:1445–56
    [Google Scholar]
  71. 71. 
    Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T 2012. Symbiont-mediated insecticide resistance. PNAS 109:8618–22
    [Google Scholar]
  72. 72. 
    Kikuchi Y, Hosokawa T, Fukatsu T 2007. Insect-microbe mutualism without vertical transmission: A stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl. Environ. Microbiol. 73:4308–16
    [Google Scholar]
  73. 73. 
    Kikuchi Y, Hosokawa T, Fukatsu T 2011. An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J 5:446–60
    [Google Scholar]
  74. 74. 
    Kikuchi Y, Hosokawa T, Fukatsu T 2011. Specific developmental window for establishment of an insect-microbe gut symbiosis. Appl. Environ. Microbiol. 77:4075–81
    [Google Scholar]
  75. 75. 
    Kikuchi Y, Meng XY, Fukatsu T 2005. Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae). Appl. Environ. Microbiol. 71:4035–43
    [Google Scholar]
  76. 76. 
    Kikuchi Y, Yumoto I. 2013. Efficient colonization of the bean bug Riptortus pedestris by an environmentally transmitted Burkholderia symbiont. Appl. Environ. Microbiol. 79:2088–91
    [Google Scholar]
  77. 77. 
    Kim JK, Han SH, Kim CH, Jo YH, Futahashi R et al. 2014. Molting-associated suppression of symbiont population and up-regulation of antimicrobial activity in the midgut symbiotic organ of the Riptortus-Burkholderia symbiosis. Dev. Comp. Immunol. 43:10–14
    [Google Scholar]
  78. 78. 
    Kim JK, Jang HA, Kim MS, Cho JH, Lee J et al. 2017. The lipopolysaccharide core oligosaccharide of Burkholderia plays a critical role in maintaining a proper gut symbiosis with the bean bug Riptortus pedestris. J. Biol. Chem 292:19226–37
    [Google Scholar]
  79. 79. 
    Kim JK, Jang HA, Won YJ, Kikuchi Y, Han SH et al. 2014. Purine biosynthesis-deficient Burkholderia mutants are incapable of symbiotic accommodation in the stinkbug. ISME J 8:552–63
    [Google Scholar]
  80. 80. 
    Kim JK, Kim NH, Jang HA, Kikuchi Y, Kim CH et al. 2013. Specific midgut region controlling the symbiont population in an insect-microbe gut symbiotic association. Appl. Environ. Microbiol. 79:7229–33
    [Google Scholar]
  81. 81. 
    Kim JK, Kwon JY, Kim SK, Han SH, Won YJ et al. 2014. Purine biosynthesis, biofilm formation, and persistence of an insect-microbe gut symbiosis. Appl. Environ. Microbiol. 80:4374–82
    [Google Scholar]
  82. 82. 
    Kim JK, Lee BL. 2015. Symbiotic factors in Burkholderia essential for establishing an association with the bean bug, Riptortus pedestris. Arch. Insect Biochem. Physiol. 88:4–17
    [Google Scholar]
  83. 83. 
    Kim JK, Lee BL. 2017. Insect symbiosis and immunity: the bean bug-Burkholderia interaction as a case study. Adv. Insect Physiol. 52:179–97
    [Google Scholar]
  84. 84. 
    Kim JK, Lee HJ, Kikuchi Y, Kitagawa W, Nikoh N et al. 2013. Bacterial cell wall synthesis gene uppP is required for Burkholderia colonization of the stinkbug gut. Appl. Environ. Microbiol. 79:4879–86
    [Google Scholar]
  85. 85. 
    Kim JK, Lee JB, Huh YR, Jang HA, Kim CH et al. 2015. Burkholderia gut symbionts enhance the innate immunity of host Riptortus pedestris. Dev. Comp. Immunol 53:265–69
    [Google Scholar]
  86. 86. 
    Kim JK, Lee JB, Jang HA, Han YS, Fukatsu T, Lee BL 2016. Understanding regulation of the host-mediated gut symbiont population and the symbiont-mediated host immunity in the Riptortus-Burkholderia symbiosis system. Dev. Comp. Immunol. 64:75–81
    [Google Scholar]
  87. 87. 
    Kim JK, Park HY, Lee BL 2016. The symbiotic role of O-antigen of Burkholderia symbiont in association with host Riptortus pedestris. Dev. Comp. Immunol 60:202–8
    [Google Scholar]
  88. 88. 
    Kim JK, Son DW, Kim CH, Cho JH, Marchetti R et al. 2015. Insect gut symbiont susceptibility to host antimicrobial peptides caused by alteration of the bacterial cell envelope. J. Biol. Chem. 290:21042–53
    [Google Scholar]
  89. 89. 
    Kim JK, Won YJ, Nikoh N, Nakayama H, Han SH et al. 2013. Polyester synthesis genes associated with stress resistance are involved in an insect-bacterium symbiosis. PNAS 110:E2381–89
    [Google Scholar]
  90. 90. 
    Kinosita Y, Kikuchi Y, Mikami N, Nakane D, Nishizaka T 2018. Unforeseen swimming and gliding mode of an insect gut symbiont, Burkholderia sp. RPE64, with wrapping of the flagella around its cell body. ISME J 12:838–48
    [Google Scholar]
  91. 91. 
    Koehler S, Gaedeke R, Thompson C, Bongrand C, Visick KL et al. 2019. The model squid-vibrio symbiosis provides a window into the impact of strain- and species-level differences during the initial stages of symbiont engagement. Environ. Microbiol. 21:3269–83
    [Google Scholar]
  92. 92. 
    Kost C, Lakatos T, Bottcher I, Arendholz WR, Redenbach M, Wirth R 2007. Non-specific association between filamentous bacteria and fungus-growing ants. Naturwissenschaften 94:821–28
    [Google Scholar]
  93. 93. 
    Kroiss J, Kaltenpoth M, Schneider B, Schwinger M-G, Hertweck C et al. 2010. Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat. Chem. Biol. 6:261–63
    [Google Scholar]
  94. 94. 
    Kuechler SM, Matsuura Y, Dettner K, Kikuchi Y 2016. Phylogenetically diverse Burkholderia associated with midgut crypts of spurge bugs, Dicranocephalus spp. (Heteroptera: Stenocephalidae). Microbes Environ 31:145–53
    [Google Scholar]
  95. 95. 
    Kuechler SM, Renz P, Dettner K, Kehl S 2012. Diversity of symbiotic organs and bacterial endosymbionts of lygaeoid bugs of the families Blissidae and Lygaeidae (Hemiptera: Heteroptera: Lygaeoidea). Appl. Environ. Microbiol. 78:2648–59
    [Google Scholar]
  96. 96. 
    Lackner G, Moebius N, Partida-Martinez L, Hertweck C 2011. Complete genome sequence of Burkholderia rhizoxinica, an endosymbiont of Rhizopus microsporus. J. Bacteriol 193:783–84
    [Google Scholar]
  97. 97. 
    Lee J, Park J, Kim S, Park I, Seo YS 2016. Differential regulation of toxoflavin production and its role in the enhanced virulence of Burkholderia gladioli. Mol. Plant Pathol 17:65–76
    [Google Scholar]
  98. 98. 
    Lee JB, Byeon JH, Jang HA, Kim JK, Yoo JW et al. 2015. Bacterial cell motility of Burkholderia gut symbiont is required to colonize the insect gut. FEBS Lett 589:2784–90
    [Google Scholar]
  99. 99. 
    Lee JB, Park KE, Lee SA, Jang SH, Eo HJ et al. 2017. Gut symbiotic bacteria stimulate insect growth and egg production by modulating hexamerin and vitellogenin gene expression. Dev. Comp. Immunol. 69:12–22
    [Google Scholar]
  100. 100. 
    Liu X, Cheng YQ. 2014. Genome-guided discovery of diverse natural products from Burkholderia sp. J. Ind. Microbiol. Biot. 41:275–84
    [Google Scholar]
  101. 101. 
    Lundgren JG, Lehman RM, Chee-Sanford J 2007. Bacterial communities within digestive tracts of ground beetles (Coleoptera: Carabidae). Ann. Entomol. Soc. Am. 100:275–82
    [Google Scholar]
  102. 102. 
    Mahenthiralingam E, Urban TA, Goldberg JB 2005. The multifarious, multireplicon Burkholderia cepacia complex. Nat. Rev. Microbiol. 3:144–56
    [Google Scholar]
  103. 103. 
    Martinez-Cano DJ, Reyes-Prieto M, Martinez-Romero E, Partida-Martinez LP, Latorre A et al. 2015. Evolution of small prokaryotic genomes. Front. Microbiol. 5:742
    [Google Scholar]
  104. 104. 
    Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA 2011. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol. Ecol. 20:619–28
    [Google Scholar]
  105. 105. 
    Michalik K, Szklarzewicz T, Kalandyk-Kołodziejczyk M, Jankowska W, Michalik A 2016. Bacteria belonging to the genus Burkholderia are obligatory symbionts of the eriococcids Acanthococcus aceris Signoret, 1875 and Gossyparia spuria (Modeer, 1778) (Insecta, Hemiptera, Coccoidea). Arthropod Struct. Dev. 45:265–72
    [Google Scholar]
  106. 106. 
    Mitter B, Petric A, Shin MW, Chain PSG, Hauberg-Lotte L et al. 2013. Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front. Plant Sci. 4:120
    [Google Scholar]
  107. 107. 
    Moebius N, Üzüm Z, Dijksterhuis J, Lackner G, Hertweck C 2014. Active invasion of bacteria into living fungal cells. eLife 3:e03007
    [Google Scholar]
  108. 108. 
    Morales-Jiménez J, Vera-Ponce de León A, García-Domínguez A, Martínez-Romero E, Zúñiga G, Hernández-Rodríguez C 2013. Nitrogen-fixing and uricolytic bacteria associated with the gut of Dendroctonus rhizophagus and Dendroctonus valens (Curculionidae: Scolytinae). Microb. Ecol. 66:200–10
    [Google Scholar]
  109. 109. 
    Moran NA, McCutcheon JP, Nakabachi A 2008. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42:165–90
    [Google Scholar]
  110. 110. 
    Naughton LM, An SQ, Hwang I, Chou SH, He YQ et al. 2016. Functional and genomic insights into the pathogenesis of Burkholderia species to rice. Environ. Microbiol. 18:780–90
    [Google Scholar]
  111. 111. 
    Nazir R, Hansen MA, Sørensen S, van Elsas JD 2012. Draft genome sequence of the soil bacterium Burkholderia terrae strain BS001, which interacts with fungal surface structures. J. Bacteriol. 194:4480–81
    [Google Scholar]
  112. 112. 
    Nickzad A, Lepine F, Deziel E 2015. Quorum sensing controls swarming motility of Burkholderia glumae through regulation of rhamnolipids. PLOS ONE 10:e0128509
    [Google Scholar]
  113. 113. 
    Nishiguchi MK, Nair VS. 2003. Evolution of symbiosis in the Vibroonaceae: a combined approach using molecules and physiology. Int. J. Syst. Evol. Microbiol. 53:2019–26
    [Google Scholar]
  114. 114. 
    Nyholm SV, Stabb EV, Ruby EG, McFall-Ngai MJ 2000. Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. PNAS 97:10231–35
    [Google Scholar]
  115. 115. 
    Ohbayashi T, Takeshita K, Kitagawa W, Nikoh N, Koga R et al. 2015. Insect's intestinal organ for symbiont sorting. PNAS 112:E5179–88
    [Google Scholar]
  116. 116. 
    Olivier-Espejel S, Sabree ZL, Noge K, Becerra JX 2011. Gut microbiota in nymph and adults of the giant mesquite bug (Thasus neocalifornicus) (Heteroptera: Coreidae) is dominated by Burkholderia acquired de novo every generation. Environ. Entomol. 40:1102–10
    [Google Scholar]
  117. 117. 
    Paganin P, Tabacchioni S, Chiarini L 2011. Pathogenicity and biotechnological applications of the genus Burkholderia. Centr. Eur. J. Biol 6:997–1005
    [Google Scholar]
  118. 118. 
    Park KE, Jang SH, Lee J, Lee SA, Kikuchi Y et al. 2018. The roles of antimicrobial peptide, rip-thanatin, in the midgut of Riptortus pedestris. Dev. Comp. Immunol 78:83–90
    [Google Scholar]
  119. 119. 
    Partida-Martinez LP, de Looß CF, Ishida K 2007. Rhizonin, the first mycotoxin isolated from the zygomycota, is not a fungal metabolite but is produced by bacterial endosymbionts. Appl. Environ. Microbiol. 73:793–97
    [Google Scholar]
  120. 120. 
    Partida-Martinez LP, Hertweck C. 2005. Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884–88
    [Google Scholar]
  121. 121. 
    Partida-Martinez LP, Monajembashi S, Greulich KO, Hertweck C 2007. Endosymbiont-dependent host reproduction maintains bacterial-fungal mutualism. Curr. Biol. 17:773–77
    [Google Scholar]
  122. 122. 
    Peeters C, Cooper VS, Hatcher PJ, Verheyde B, Carlier A, Vandamme P 2017. Comparative genomics of Burkholderia multivorans, a ubiquitous pathogen with a highly conserved genomic structure. PLOS ONE 12:e0176191
    [Google Scholar]
  123. 123. 
    Pérez-Pantoja D, Donoso R, Agulló L, Córdova M, Seeger M et al. 2012. Genomic analysis of the potential for aromatic compounds biodegradation in Burkholderiales. Environ. Microbiol. 14:1091–117
    [Google Scholar]
  124. 124. 
    Perlman SJ, Hunter MS, Zchori-Fein E 2006. The emerging diversity of Rickettsia. Proc. R. Soc. B 273:2097–106
    [Google Scholar]
  125. 125. 
    Pidot SJ, Coyne S, Kloss F, Hertweck C 2014. Antibiotics from neglected bacterial sources. Int. J. Med. Microbiol. 304:14–22
    [Google Scholar]
  126. 126. 
    Pinto-Carbó M, Gademann K, Eberl L, Carlier A 2018. Leaf nodule symbiosis: function and transmission of obligate bacterial endophytes. Curr. Opin. Plant Biol. 44:23–31
    [Google Scholar]
  127. 127. 
    Pinto-Carbó M, Sieber S, Dessein S, Wicker T, Verstraete B et al. 2016. Evidence of horizontal gene transfer between obligate leaf nodule symbionts. ISME J 10:2092–105
    [Google Scholar]
  128. 128. 
    Powell JE, Leonard SP, Kwong WK, Engel P, Moran NA 2016. Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont. PNAS 113:13887–92
    [Google Scholar]
  129. 129. 
    Pruesse E, Peplies J, Gloeckner FO 2012. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–29
    [Google Scholar]
  130. 130. 
    Reid NM, Addison SL, Macdonald LJ, Lloyd-Jones G 2011. Biodiversity of active and inactive bacteria in the gut flora of wood-feeding huhu beetle larvae (Prionoplus reticularis). Appl. Environ. Microbiol. 77:7000–6
    [Google Scholar]
  131. 131. 
    Rizvi SA, Courson DS, Keller VA, Rock RS, Kozmin SA 2008. The dual mode of action of bistramide A entails severing of filamentous actin and covalent protein modification. PNAS 105:4088–92
    [Google Scholar]
  132. 132. 
    Ruiu L. 2015. Insect pathogenic bacteria in integrated pest management. Insects 6:352–67
    [Google Scholar]
  133. 133. 
    Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE 2009. Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. PNAS 106:21236–41
    [Google Scholar]
  134. 134. 
    Sabree ZL, Kambhampati S, Moran NA 2009. Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. PNAS 106:19521–26
    [Google Scholar]
  135. 135. 
    Salem H, Bauer E, Kirsch R, Berasategui A, Cripps M et al. 2017. Drastic genome reduction in an herbivore's pectinolytic symbiont. Cell 171:1520–31
    [Google Scholar]
  136. 136. 
    Salem H, Bauer E, Strauss AS, Vogel H, Marz M, Kaltenpoth M 2014. Vitamin supplementation by gut symbionts ensures metabolic homeostasis in an insect host. Proc. R. Soc. B 281:20141838
    [Google Scholar]
  137. 137. 
    Salem H, Flórez L, Gerardo NM, Kaltenpoth M 2015. An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects. Proc. R. Soc. B 282:20142957
    [Google Scholar]
  138. 138. 
    Salem H, Kreutzer E, Sudakaran S, Kaltenpoth M 2013. Actinobacteria as essential symbionts in firebugs and cotton stainers (Hemiptera, Pyrrhocoridae). Environ. Microbiol. 15:1956–68
    [Google Scholar]
  139. 139. 
    Santos AV, Dillon RJ, Dillon VM, Reynolds SE, Samuels RI 2004. Ocurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa. FEMS Microbiol. Lett 239:319–23
    [Google Scholar]
  140. 140. 
    Sawana A, Adeolu M, Gupta RS 2014. Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov harboring environmental species. Front. Genet. 5:429
    [Google Scholar]
  141. 141. 
    Schoenian I, Spiteller M, Ghaste M, Wirth R, Herz H, Spiteller D 2011. Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. PNAS 108:1955–60
    [Google Scholar]
  142. 142. 
    Scott JJ, Oh DC, Yuceer MC, Klepzig KD, Clardy J, Currie CR 2008. Bacterial protection of beetle-fungus mutualism. Science 322:63
    [Google Scholar]
  143. 143. 
    Seed KD, Dennis JJ. 2008. Development of Galleria mellonella as an alternative infection model for the Burkholderia cepacia complex. Infect. Immun. 76:1267–75
    [Google Scholar]
  144. 144. 
    Segers F, Kesnerova L, Kosoy M, Engel P 2017. Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen. ISME J 11:1232–44
    [Google Scholar]
  145. 145. 
    Seipke RF, Kaltenpoth M, Hutchings MI 2012. Streptomyces as symbionts: an emerging and widespread theme. ? FEMS Microbiol. Rev. 36:862–76
    [Google Scholar]
  146. 146. 
    Seo J-S, Keum Y-S, Li QX 2009. Bacterial degradation of aromatic compounds. Int. J. Environ. Res. Public Health 6:278–309
    [Google Scholar]
  147. 147. 
    Seo Y-S, Lim JY, Park J, Kim S, Lee H-H et al. 2015. Comparative genome analysis of rice-pathogenic Burkholderia provides insight into capacity to adapt to different environments and hosts. BMC Genom 16:349
    [Google Scholar]
  148. 148. 
    Shehata HR, Lyons EM, Jordan KS, Raizada MN 2016. Bacterial endophytes from wild and ancient maize are able to suppress the fungal pathogen Sclerotinia homoeocarpa. J. Appl. Microbiol 120:756–69
    [Google Scholar]
  149. 149. 
    Shibata TF, Maeda T, Nikoh N, Yamaguchi K, Oshima K et al. 2013. Complete genome sequence of Burkholderia sp. strain RPE64, bacterial symbiont of the bean bug Riptortus pedestris. Genome Announc 1:e00441–13
    [Google Scholar]
  150. 150. 
    Speare L, Cecere AG, Guckes KR, Smith S, Wollenberg MS et al. 2018. Bacterial symbionts use a type VI secretion system to eliminate competitors in their natural host. PNAS 115:E8528–37
    [Google Scholar]
  151. 151. 
    Stammer HJ. 1929. Die Symbiose der Lagriiden (Coleoptera). Z. Morphol. Oekol. Tiere 15:1–34
    [Google Scholar]
  152. 152. 
    Stoll S, Gadau J, Gross R, Feldhaar H 2007. Bacterial microbiota associated with ants of the genus Tetraponera. Biol. J. Linn. Soc 90:399–412
    [Google Scholar]
  153. 153. 
    Suárez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendonça-Previato L, James EK, Venturi V 2012. Common features of environmental and potentially beneficial plant-associated Burkholderia. Microb. Ecol 63:249–66
    [Google Scholar]
  154. 154. 
    Sudakaran S, Kost C, Kaltenpoth M 2017. Symbiont acquisition and replacement as a source of ecological innovation. Trends Microbiol 25:375–90
    [Google Scholar]
  155. 155. 
    Sudakaran S, Retz F, Kikuchi Y, Kost C, Kaltenpoth M 2015. Evolutionary transition in symbiotic syndromes enabled diversification of phytophagous insects on an imbalanced diet. ISME J 9:2587–604
    [Google Scholar]
  156. 156. 
    Sudakaran S, Salem H, Kost C, Kaltenpoth M 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]
  157. 157. 
    Suppiger A, Schmid N, Aguilar C, Pessi G, Eberl L 2013. Two quorum sensing systems control biofilm formation and virulence in members of the Burkholderia cepacia complex. Virulence 4:400–9
    [Google Scholar]
  158. 158. 
    Tabacchioni S, Bevivino A, Dalmastri C, Chiarini L 2002. Burkholderia cepacia complex in the rhizosphere: a minireview. Ann. Microbiol. 52:103–17
    [Google Scholar]
  159. 159. 
    Tago K, Kikuchi Y, Nakaoka S, Katsuyama C, Hayatsu M 2015. Insecticide applications to soil contribute to the development of Burkholderia mediating insecticide resistance in stinkbugs. Mol. Ecol. 24:3766–78
    [Google Scholar]
  160. 160. 
    Tago K, Okubo T, Itoh H, Kikuchi Y, Hori T et al. 2015. Insecticide-degrading Burkholderia symbionts of the stinkbug naturally occupy various environments of sugarcane fields in a southeast island of Japan. Microbes Environ 30:29–36
    [Google Scholar]
  161. 161. 
    Takeshita K, Kikuchi Y. 2017. Riptortus pedestris and Burkholderia symbiont: an ideal model system for insect-microbe symbiotic associations. Res. Microbiol. 168:175–87
    [Google Scholar]
  162. 162. 
    Takeshita K, Shibata TF, Nikoh N, Nishiyama T, Hasebe M et al. 2014. Whole-genome sequence of Burkholderia sp. strain RPE67, a bacterial gut symbiont of the bean bug Riptortus pedestris. Genome Announc 2:e00556–14
    [Google Scholar]
  163. 163. 
    Tian Y, Kong BH, Liu SL, Li CL, Yu R et al. 2013. Burkholderia grimmiae sp. nov., isolated from a xerophilous moss (Grimmia montana). Int. J. Syst. Evol. Microbiol. 63:2108–13
    [Google Scholar]
  164. 164. 
    van Borm S, Buschinger A, Boomsma JJ, Billen J 2002. Tetraponera ants have gut symbionts related to nitrogen-fixing root-nodule bacteria. Proc. R. Soc. B 269:2023–27
    [Google Scholar]
  165. 165. 
    Vanrhijn P, Vanderleyden J. 1995. The Rhizobium-plant symbiosis. Microbiol. Rev. 59:124–42
    [Google Scholar]
  166. 166. 
    Vial L, Chapalain A, Groleau MC, Deziel E 2011. The various lifestyles of the Burkholderia cepacia complex species: a tribute to adaptation. Environ. Microbiol. 13:1–12
    [Google Scholar]
  167. 167. 
    Vial L, Groleau MC, Dekimpe V, Déziel E 2007. Burkholderia diversity and versatility: an inventory of the extracellular products. J. Microbiol. Biotechnol. 17:1407–29
    [Google Scholar]
  168. 168. 
    Weiss BL, Wang JW, Aksoy S 2011. Tsetse immune system maturation requires the presence of obligate symbionts in larvae. PLOS Biol 9:e1000619
    [Google Scholar]
  169. 169. 
    Willcocks SJ, Denman CC, Atkins HS, Wren BW 2016. Intracellular replication of the well-armed pathogen Burkholderia pseudomallei. Curr. Opin. Microbiol 29:94–103
    [Google Scholar]
  170. 170. 
    Xu Y, Buss EA, Boucias DG 2016. Environmental transmission of the gut symbiont Burkholderia to phloem-feeding Blissus insularis. PLOS ONE 11:e0161699
    [Google Scholar]
  171. 171. 
    Xu Y, Buss EA, Boucias DG 2016. Impacts of antibiotic and bacteriophage treatments on the gut-symbiont-associated Blissus insularis (Hemiptera: Blissidae). Insects 7:E61
    [Google Scholar]
  172. 172. 
    Yabuuchi E, Kosako Y, Oyaizu H, Yano I, Hotta H et al. 1992. Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol. Immunol. 36:1251–75
    [Google Scholar]
  173. 173. 
    Yamada A, Inoue T, Noda S, Hongoh Y, Ohkuma M 2007. Evolutionary trend of phylogenetic diversity of nitrogen fixation genes in the gut community of wood-feeding termites. Mol. Ecol. 16:3768–77
    [Google Scholar]
  174. 174. 
    Ziganshina EE, Mohammed WS, Shagimardanova EI, Vankov PY, Gogoleva NE, Ziganshin AM 2018. Fungal, bacterial, and archaeal diversity in the digestive tract of several beetle larvae (Coleoptera). Biomed. Res. Int. 2018:6765438
    [Google Scholar]
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