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Evidence for Gut-Associated Serratia symbiotica in Wild Aphids and Ants Provides New Perspectives on the Evolution of Bacterial Mutualism in Insects

  • Invertebrate Microbiology
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Abstract

Many insects engage in symbiotic associations with diverse assemblages of bacterial symbionts that can deeply impact on their ecology and evolution. The intraspecific variation of symbionts remains poorly assessed while phenotypic effects and transmission behaviors, which are key processes for the persistence and evolution of symbioses, may differ widely depending on the symbiont strains. Serratia symbiotica is one of the most frequent symbiont species in aphids and a valuable model to assess this intraspecific variation since it includes both facultative and obligate symbiotic strains. Despite evidence that some facultative S. symbiotica strains exhibit a free-living capacity, the presence of these strains in wild aphid populations, as well as in insects with which they maintain regular contact, has never been demonstrated. Here, we examined the prevalence, diversity, and tissue tropism of S. symbiotica in wild aphids and associated ants. We found a high occurrence of S. symbiotica infection in ant populations, especially when having tended infected aphid colonies. We also found that the S. symbiotica diversity includes strains found located within the gut of aphids and ants. In the latter, this tissue tropism was found restricted to the proventriculus. Altogether, these findings highlight the extraordinary diversity and versatility of an insect symbiont and suggest the existence of novel routes for symbiont acquisition in insects.

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References

  1. McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci 110:3229–3236. https://doi.org/10.1073/pnas.1218525110

    Article  PubMed  PubMed Central  Google Scholar 

  2. Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55:247–266. https://doi.org/10.1146/annurev-ento-112408-085305

    Article  CAS  PubMed  Google Scholar 

  3. Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543. https://doi.org/10.1111/j.1365-2311.2011.01318.x

    Article  Google Scholar 

  4. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190. https://doi.org/10.1146/annurev.genet.41.110306.130119

    Article  CAS  PubMed  Google Scholar 

  5. Ferrari J, Vavre F (2011) Bacterial symbionts in insects or the story of communities affecting communities. Philos Trans R Soc B Biol Sci 366:1389–1400. https://doi.org/10.1098/rstb.2010.0226

    Article  Google Scholar 

  6. Sandström JP, Russell JA, White JP, Moran NA (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 10:217–228. https://doi.org/10.1046/j.1365-294X.2001.01189.x

    Article  PubMed  Google Scholar 

  7. Duron O, Wilkes TE, Hurst GDD (2010) Interspecific transmission of a male-killing bacterium on an ecological timescale. Ecol Lett 13:1139–1148. https://doi.org/10.1111/j.1461-0248.2010.01502.x

    Article  PubMed  Google Scholar 

  8. Gehrer L, Vorburger C (2012) Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Lett rsbl20120144. https://doi.org/10.1098/rsbl.2012.0144

  9. Jousselin E, Cœur d’Acier A, Vanlerberghe-Masutti F, Duron O (2013) Evolution and diversity of Arsenophonus endosymbionts in aphids. Mol Ecol 22:260–270. https://doi.org/10.1111/mec.12092

    Article  PubMed  Google Scholar 

  10. Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T, Matsumoto S, Simon JC, Fukatsu T (2010) Symbiotic bacterium modifies aphid body color. Science 330:1102–1104. https://doi.org/10.1126/science.1195463

    Article  CAS  PubMed  Google Scholar 

  11. Dion E, Polin SE, Simon J-C, Outreman Y (2011) Symbiont infection affects aphid defensive behaviours. Biol Lett 7:743–746. https://doi.org/10.1098/rsbl.2011.0249

    Article  PubMed  PubMed Central  Google Scholar 

  12. Simon J-C, Boutin S, Tsuchida T, Koga R, le Gallic JF, Frantz A, Outreman Y, Fukatsu T (2011) Facultative symbiont infections affect aphid reproduction. PLoS One 6:e21831. https://doi.org/10.1371/journal.pone.0021831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Oliver KM, Smith AH, Russell JA (2014) Defensive symbiosis in the real world – advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct Ecol 28:341–355. https://doi.org/10.1111/1365-2435.12133

    Article  Google Scholar 

  14. Leclair M, Pons I, Mahéo F, Morlière S, Simon JC, Outreman Y (2016) Diversity in symbiont consortia in the pea aphid complex is associated with large phenotypic variation in the insect host. Evol Ecol 30:925–941. https://doi.org/10.1007/s10682-016-9856-1

    Article  Google Scholar 

  15. Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA (2007) From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5:e114. https://doi.org/10.1371/journal.pbio.0050114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Teixeira L, Ferreira Á, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6:e1000002. https://doi.org/10.1371/journal.pbio.1000002

    Article  CAS  PubMed Central  Google Scholar 

  17. Min K-T, Benzer S (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci 94:10792–10796. https://doi.org/10.1073/pnas.94.20.10792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230. https://doi.org/10.1038/nrmicro2262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Egan S, Thomas T (2015) Microbial symbiosis of marine sessile hosts - diversity, function and applications. Frontiers Media SA

    Google Scholar 

  20. Salem H, Florez L, Gerardo N, Kaltenpoth M (2015) An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects. Proc R Soc Lond B Biol Sci 282:20142957. https://doi.org/10.1098/rspb.2014.2957

    Article  Google Scholar 

  21. Clayton AL, Oakeson KF, Gutin M, Pontes A, Dunn DM, von Niederhausern AC, Weiss RB, Fisher M, Dale C (2012) A novel human-infection-derived bacterium provides insights into the evolutionary origins of mutualistic insect–bacterial symbioses. PLoS Genet 8:e1002990. https://doi.org/10.1371/journal.pgen.1002990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Zytynska SE, Meyer ST, Sturm S, Ullmann W, Mehrparvar M, Weisser WW (2015) Secondary bacterial symbiont community in aphids responds to plant diversity. Oecologia 180:1–13. https://doi.org/10.1007/s00442-015-3488-y

    Article  Google Scholar 

  23. Lamelas A, Gosalbes MJ, Manzano-Marín A, Peretó J, Moya A, Latorre A (2011) Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont. PLoS Genet 7:e1002357. https://doi.org/10.1371/journal.pgen.1002357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lamelas A, Gosalbes MJ, Moya A, Latorre A (2011) The genome of Buchnera aphidicola from the aphid Cinara tujafilina provides new clues about the evolutionary history of metabolic losses in bacterial endosymbionts. Appl Environ Microbiol AEM.00141–11. https://doi.org/10.1128/AEM.00141-11

  25. Manzano-Marín A, Simon J-C, Latorre A (2016) Reinventing the wheel and making it round again: evolutionary convergence in Buchnera–Serratia symbiotic consortia between the distantly related Lachninae aphids Tuberolachnus salignus and Cinara cedri. Genome Biol Evol 8:1440–1458. https://doi.org/10.1093/gbe/evw085

    Article  PubMed  PubMed Central  Google Scholar 

  26. Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195. https://doi.org/10.1046/j.1365-2311.2002.00393.x

    Article  Google Scholar 

  27. Burke G, Fiehn O, Moran N (2009) Effects of facultative symbionts and heat stress on the metabolome of pea aphids. ISME J 4:242–252. https://doi.org/10.1038/ismej.2009.114

    Article  PubMed  Google Scholar 

  28. Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci 100:1803–1807. https://doi.org/10.1073/pnas.0335320100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Foray V, Grigorescu AS, Sabri A, Haubruge E, Lognay G, Francis F, Fauconnier ML, Hance T, Thonart P (2014) Whole-genome sequence of Serratia symbiotica strain CWBI-2.3T, a free-living symbiont of the black bean aphid Aphis fabae. Genome Announc 2:e00767–e00714. https://doi.org/10.1128/genomeA.00767-14

    Article  PubMed  PubMed Central  Google Scholar 

  30. Sabri A, Leroy P, Haubruge E, Hance T, Frere I, Destain J, Thonart P (2011) Isolation, pure culture and characterization of Serratia symbiotica sp. nov., the R-type of secondary endosymbiont of the black bean aphid Aphis fabae. Int J Syst Evol Microbiol 61:2081–2088. https://doi.org/10.1099/ijs.0.024133-0

    Article  CAS  PubMed  Google Scholar 

  31. Grigorescu AS, Renoz F, Sabri A, et al (2017) Accessing the hidden microbial diversity of aphids: an illustration of how culture-dependent methods can be used to decipher the insect microbiota. Microb Ecol 1–14. https://doi.org/10.1007/s00248-017-1092-x

  32. Renoz F, Champagne A, Degand H, Faber AM, Morsomme P, Foray V, Hance T (2017) Toward a better understanding of the mechanisms of symbiosis: a comprehensive proteome map of a nascent insect symbiont. PeerJ 5:e3291. https://doi.org/10.7717/peerj.3291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Manzano-Marín A, Latorre A (2016) Snapshots of a shrinking partner: genome reduction in Serratia symbiotica. Sci Rep 6. https://doi.org/10.1038/srep32590

  34. Henry LM, Maiden MCJ, Ferrari J, Godfray HCJ (2015) Insect life history and the evolution of bacterial mutualism. Ecol Lett 18:516–525. https://doi.org/10.1111/ele.12425

    Article  PubMed  Google Scholar 

  35. Hajibabaei M, Janzen DH, Burns JM, Hallwachs W, Hebert PDN (2006) DNA barcodes distinguish species of tropical Lepidoptera. Proc Natl Acad Sci U S A 103:968–971. https://doi.org/10.1073/pnas.0510466103

    Article  PubMed  PubMed Central  Google Scholar 

  36. D’acier AC, Cruaud A, Artige E et al (2014) DNA barcoding and the associated PhylAphidB@se website for the identification of European aphids (Insecta: Hemiptera: Aphididae). PLoS One 9:e97620. https://doi.org/10.1371/journal.pone.0097620

    Article  CAS  Google Scholar 

  37. Fukatsu T, Nikoh N, Kawai R, Koga R (2000) The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta: Homoptera). Appl Environ Microbiol 66:2748–2758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Renoz F, Noël C, Errachid A, Foray V, Hance T (2015) Infection dynamic of symbiotic bacteria in the pea aphid Acyrthosiphon pisum gut and host immune response at the early steps in the infection process. PLoS One 10:e0122099. https://doi.org/10.1371/journal.pone.0122099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Burke GR, Moran NA (2011) Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol 3:195–208. https://doi.org/10.1093/gbe/evr002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Manzano-Marín A, Latorre A (2014) Settling down: the genome of Serratia symbiotica from the aphid Cinara tujafilina zooms in on the process of accommodation to a cooperative intracellular life. Genome Biol Evol 6:1683–1698. https://doi.org/10.1093/gbe/evu133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. R Development Core Team (2006) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed 15 Dec 2015

  42. Henry LM, Peccoud J, Simon J-C, Hadfield JD, Maiden MJC, Ferrari J, Godfray HCJ (2013) Horizontally transmitted symbionts and host colonization of ecological niches. Curr Biol 23:1713–1717. https://doi.org/10.1016/j.cub.2013.07.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Łukasik P, Guo H, van Asch M, Henry LM, Godfray HCJ, Ferrari J (2015) Horizontal transfer of facultative endosymbionts is limited by host relatedness. Evolution 69:2757–2766. https://doi.org/10.1111/evo.12767

    Article  PubMed  Google Scholar 

  44. Degnan PH, Moran NA (2008) Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage. Mol Ecol 17:916–929. https://doi.org/10.1111/j.1365-294X.2007.03616.x

    Article  CAS  PubMed  Google Scholar 

  45. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  46. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  47. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772. https://doi.org/10.1038/nmeth.2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581–583. https://doi.org/10.1093/bioinformatics/btm388

    Article  CAS  PubMed  Google Scholar 

  49. Ryuichi Koga TT (2009) Quenching autofluorescence of insect tissues for in situ detection of endosymbionts. Appl Entomol Zool - APPL ENTOMOL ZOOL 44:281–291. https://doi.org/10.1303/aez.2009.281

    Article  CAS  Google Scholar 

  50. Baumann P, Baumann L, Lai C-Y, Rouhbakhsh D, Moran NA, Clark MA (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu Rev Microbiol 49:55–94. https://doi.org/10.1146/annurev.mi.49.100195.000415

    Article  CAS  PubMed  Google Scholar 

  51. Simonet P, Duport G, Gaget K, et al (2016) Direct flow cytometry measurements reveal a fine-tuning of symbiotic cell dynamics according to the host developmental needs in aphid symbiosis. Sci Rep 6:srep19967. https://doi.org/10.1038/srep19967

  52. Eisner T, Wilson EO (1952) The morphology of the proventriculus of a formicine ant. Psyche J Entomol 59:47–60. https://doi.org/10.1155/1952/14806

    Article  Google Scholar 

  53. Lanan MC, Rodrigues PAP, Agellon A, Jansma P, Wheeler DE (2016) A bacterial filter protects and structures the gut microbiome of an insect. ISME J 10:1866–1876. https://doi.org/10.1038/ismej.2015.264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Moran NA, Russell JA, Koga R, Fukatsu T (2005) Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl Environ Microbiol 71:3302–3310. https://doi.org/10.1128/AEM.71.6.3302-3310.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Koga R, Meng X-Y, Tsuchida T, Fukatsu T (2012) Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte–embryo interface. Proc Natl Acad Sci 109:E1230–E1237. https://doi.org/10.1073/pnas.1119212109

    Article  PubMed  PubMed Central  Google Scholar 

  56. Manzano-Marín A, Szabó G, Simon J-C, Horn M, Latorre A (2017) Happens in the best of subfamilies: establishment and repeated replacements of co-obligate secondary endosymbionts within Lachninae aphids. Environ Microbiol 19:393–408. https://doi.org/10.1111/1462-2920.13633

    Article  CAS  PubMed  Google Scholar 

  57. Leroy PD, Sabri A, Heuskin S, Thonart P, Lognay G, Verheggen FJ, Francis F, Brostaux Y, Felton GW, Haubruge E (2011) Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies. Nat Commun 2:348. https://doi.org/10.1038/ncomms1347

    Article  CAS  PubMed  Google Scholar 

  58. Fischer CY, Lognay GC, Detrain C, Heil M, Grigorescu A, Sabri A, Thonart P, Haubruge E, Verheggen FJ (2015) Bacteria may enhance species association in an ant–aphid mutualistic relationship. Chemoecology 25:223–232. https://doi.org/10.1007/s00049-015-0188-3

    Article  CAS  Google Scholar 

  59. Darby AC, Douglas AE (2003) Elucidation of the transmission patterns of an insect-borne bacterium. Appl Environ Microbiol 69:4403–4407. https://doi.org/10.1128/AEM.69.8.4403-4407.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Sabri A, Vandermoten S, Leroy PD, Haubruge E, Hance T, Thonart P, de Pauw E, Francis F (2013) Proteomic investigation of aphid honeydew reveals an unexpected diversity of proteins. PLoS One 8:e74656. https://doi.org/10.1371/journal.pone.0074656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Buckley RC (1987) Interactions involving plants, Homoptera, and ants. Annu Rev Ecol Syst 18:111–135

    Article  Google Scholar 

  62. Katayama N, Suzuki N (2003) Bodyguard effects for aphids of Aphis craccivora Koch (Homoptera: Aphididae) as related to the activity of two ant species, Tetramorium caespitum Linnaeus (Hymenoptera: Formicidae) and Lasius niger L. (Hymenoptera: Formicidae). Appl Entomol Zool 38:427–433. https://doi.org/10.1303/aez.2003.427

    Article  Google Scholar 

  63. Stadler B (1997) The relative importance of host plants, natural enemies and ants in the evolution of life-history characters in aphids. In: Dettner PDK, Bauer PDG, Völkl DW (eds) Vertical food web interactions. Springer, Berlin Heidelberg, pp 241–256

    Chapter  Google Scholar 

  64. Portha S, Deneubourg J-L, Detrain C (2004) How food type and brood influence foraging decisions of Lasius niger scouts. Anim Behav 68:115–122. https://doi.org/10.1016/j.anbehav.2003.10.016

    Article  Google Scholar 

  65. Liebig J, Heinze J, Hölldobler B (1997) Trophallaxis and aggression in the ponerine ant, Ponera coarctata: implications for the evolution of liquid food exchange in the Hymenoptera. Ethology 103:707–722. https://doi.org/10.1111/j.1439-0310.1997.tb00180.x

    Article  Google Scholar 

  66. Sirviö A, Pamilo P (2010) Multiple endosymbionts in populations of the ant Formica cinerea. BMC Evol Biol 10:335. https://doi.org/10.1186/1471-2148-10-335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. He H, Chen Y, Zhang Y, Wei C (2011) Bacteria associated with gut lumen of Camponotus japonicus Mayr. Environ Entomol 40:1405–1409. https://doi.org/10.1603/EN11157

    Article  CAS  PubMed  Google Scholar 

  68. Li X, Nan X, Wei C, He H (2012) The gut bacteria associated with Camponotus japonicus Mayr with culture-dependent and DGGE methods. Curr Microbiol 65:610–616. https://doi.org/10.1007/s00284-012-0197-1

    Article  CAS  PubMed  Google Scholar 

  69. Engel P, Moran NA (2013) The gut microbiota of insects—diversity in structure and function. FEMS Microbiol Rev 37:699–735. https://doi.org/10.1111/1574-6976.12025

    Article  CAS  PubMed  Google Scholar 

  70. 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. Proc Natl Acad Sci 106:21236–21241. https://doi.org/10.1073/pnas.0907926106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Hu Y, Łukasik P, Moreau CS, Russell JA (2014) Correlates of gut community composition across an ant species (Cephalotes varians) elucidate causes and consequences of symbiotic variability. Mol Ecol 23:1284–1300. https://doi.org/10.1111/mec.12607

    Article  PubMed  Google Scholar 

  72. Koga R, Tsuchida T, Fukatsu T (2003) Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc R Soc Lond B Biol Sci 270:2543–2550. https://doi.org/10.1098/rspb.2003.2537

    Article  Google Scholar 

  73. Fakhour S, Ambroise J, Renoz F, Foray V, Gala JL, Hance T (2018) A large-scale field study of bacterial communities in cereal aphid populations across Morocco. FEMS Microbiol Ecol 94. https://doi.org/10.1093/femsec/fiy003

  74. Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92. https://doi.org/10.1146/annurev.ento.49.061802.123416

    Article  CAS  PubMed  Google Scholar 

  75. Hansen AK, Moran NA (2014) The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol Ecol 23:1473–1496. https://doi.org/10.1111/mec.12421

    Article  PubMed  Google Scholar 

  76. Meister S, Agianian B, Turlure F, Relógio A, Morlais I, Kafatos FC, Christophides GK (2009) Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathog 5:e1000542. https://doi.org/10.1371/journal.ppat.1000542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Cirimotich CM, Dong Y, Clayton AM, Sandiford SL, Souza-Neto JA, Mulenga M, Dimopoulos G (2011) Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 332:855–858. https://doi.org/10.1126/science.1201618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Koch H, Schmid-Hempel P (2011) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci 108:19288–19292. https://doi.org/10.1073/pnas.1110474108

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors thank deeply Abdelmounaim Errachid and Charles Hachez for technical support regarding confocal microscopy and Florence Hecq and Marianne Renoz for their helpful comments on the earlier version of the manuscript. This paper is publication BRC394 of the Biodiversity Research center (Université catholique de Louvain).

Funding

This work was supported by the Fonds de la Recherche Scientifique (FNRS) through a Fonds pour la Recherche en Industrie et en Agronomie (FRIA) (FRIA grant no. 1.E074.14). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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  1. Biodiversity Research Centre, Earth and Life Institute, Université catholique de Louvain, Croix du sud 4-5, 1348, Louvain-la-Neuve, Belgium

    François Renoz, Inès Pons, Gwennaël Bataille, Christine Noël, Valentin Pierson & Thierry Hance

  2. Department of Biology, Institute of Botany, University of Liège, B22 Sart Tilman, 4000, Liege, Belgium

    Alain Vanderpoorten

  3. Centre de Recherche de Biologie cellulaire de Montpellier, UMR CNRS 5237, 34293, Montpellier, France

    Vincent Foray

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FR conceived and designed the research; FR, IP, VP, and CN performed the research; FR, IP, GB, AV, CN, VF, and VP analyzed the data; FR wrote the paper; VF, IP, AV, and TH made manuscript revisions. All authors gave final approval for publication.

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Renoz, F., Pons, I., Vanderpoorten, A. et al. Evidence for Gut-Associated Serratia symbiotica in Wild Aphids and Ants Provides New Perspectives on the Evolution of Bacterial Mutualism in Insects. Microb Ecol 78, 159–169 (2019). https://doi.org/10.1007/s00248-018-1265-2

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  • DOI: https://doi.org/10.1007/s00248-018-1265-2

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