Accessing the Hidden Microbial Diversity of Aphids: an Illustration of How Culture-Dependent Methods Can Be Used to Decipher the Insect Microbiota

Invertebrate Microbiology

Abstract

Microorganism communities that live inside insects can play critical roles in host development, nutrition, immunity, physiology, and behavior. Over the past decade, high-throughput sequencing reveals the extraordinary microbial diversity associated with various insect species and provides information independent of our ability to culture these microbes. However, their cultivation in the laboratory remains crucial for a deep understanding of their physiology and the roles they play in host insects. Aphids are insects that received specific attention because of their ability to form symbiotic associations with a wide range of endosymbionts that are considered as the core microbiome of these sap-feeding insects. But, if the functional diversity of obligate and facultative endosymbionts has been extensively studied in aphids, the diversity of gut symbionts and other associated microorganisms received limited consideration. Herein, we present a culture-dependent method that allowed us to successfully isolate microorganisms from several aphid species. The isolated microorganisms were assigned to 24 bacterial genera from the Actinobacteria, Firmicutes, and Proteobacteria phyla and three fungal genera from the Ascomycota and Basidiomycota phyla. In our study, we succeeded in isolating already described bacteria found associated to aphids (e.g., the facultative symbiont Serratia symbiotica), as well as microorganisms that have never been described in aphids before. By unraveling a microbial community that so far has been ignored, our study expands our current knowledge on the microbial diversity associated with aphids and illustrates how fast and simple culture-dependent approaches can be applied to insects in order to capture their diverse microbiota members.

Keywords

Insect Aphid microbiota Culture-dependent method Molecular phylogeny Symbiotic bacteria 

Supplementary material

248_2017_1092_MOESM1_ESM.docx (16 kb)
Table S1(DOCX 15 kb)
248_2017_1092_MOESM2_ESM.docx (19 kb)
Table S2(DOCX 18 kb)
248_2017_1092_MOESM3_ESM.docx (64 kb)
Table S3(DOCX 64 kb)

References

  1. 1.
    Chu C-C, Spencer JL, Curzi MJ, et al. (2013) Gut bacteria facilitate adaptation to crop rotation in the western corn rootworm. Proc. Natl. Acad. Sci. U. S. A. 110:11917–11922. https://doi.org/10.1073/pnas.1301886110 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32:723–735. https://doi.org/10.1111/j.1574-6976.2008.00123.x CrossRefPubMedGoogle Scholar
  3. 3.
    Rosenberg E, Sharon G, Atad I, Zilber-Rosenberg I (2010) The evolution of animals and plants via symbiosis with microorganisms. Environ. Microbiol. Rep. 2:500–506. https://doi.org/10.1111/j.1758-2229.2010.00177.x CrossRefPubMedGoogle Scholar
  4. 4.
    Takeshita K, Matsuura Y, Itoh H, et al. (2015) Burkholderia of plant-beneficial group are symbiotically associated with bordered plant bugs (Heteroptera: Pyrrhocoroidea: Largidae). Microbes Environ. 30:321–329. https://doi.org/10.1264/jsme2.ME15153 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Buchner P (1965) Symbiosis in animals which suck plant juices.Endosymbiosis of animals with plant microorganisms. Interscience, New York, Google Scholar
  6. 6.
    Munson MA, Baumann P, Clark MA, et al. (1991) Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J. Bacteriol. 173:6321–6324CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    ACC W, Ashton PD, Calevro F, et al. (2010) Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol. Biol. 19(Suppl 2):249–258. https://doi.org/10.1111/j.1365-2583.2009.00942.x Google Scholar
  8. 8.
    Pérez-Brocal V, Gil R, Moya A, Latorre A (2011) New insights on the evolutionary history of aphids and their primary endosymbiont Buchnera aphidicola. Int. J. Evol. Biol. https://doi.org/10.4061/2011/250154
  9. 9.
    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 CrossRefGoogle Scholar
  10. 10.
    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 CrossRefPubMedGoogle Scholar
  11. 11.
    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 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Schmitz A, Anselme C, Ravallec M, et al. (2012) The cellular immune response of the pea aphid to foreign intrusion and symbiotic challenge. PLoS One 7:e42114. https://doi.org/10.1371/journal.pone.0042114 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Łukasik P, Guo H, van Asch M, et al. (2013) Protection against a fungal pathogen conferred by the aphid facultative endosymbionts Rickettsia and Spiroplasma is expressed in multiple host genotypes and species and is not influenced by co-infection with another symbiont. J. Evol. Biol. 26:2654–2661. https://doi.org/10.1111/jeb.12260 CrossRefPubMedGoogle Scholar
  14. 14.
    Costopoulos K, Kovacs JL, Kamins A, Gerardo NM (2014) Aphid facultative symbionts reduce survival of the predatory lady beetle Hippodamia convergens. BMC Ecol. 14:5. https://doi.org/10.1186/1472-6785-14-5 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Leonardo TE, Muiru GT (2003) Facultative symbionts are associated with host plant specialization in pea aphid populations. Proc. Biol. Sci. 270(Suppl):S209–S212. https://doi.org/10.1098/rsbl.2003.0064 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989–1989. https://doi.org/10.1126/science.1094611 CrossRefPubMedGoogle Scholar
  17. 17.
    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 CrossRefGoogle Scholar
  18. 18.
    Tsuchida T, Koga R, Fujiwara A, Fukatsu T (2014) Phenotypic effect of “Candidatus Rickettsiella viridis,” a facultative symbiont of the pea aphid (Acyrthosiphon pisum), and its interaction with a coexisting symbiont. Appl. Environ. Microbiol. 80:525–533. https://doi.org/10.1128/AEM.03049-13 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Grenier A-M, Nardon C, Rahbé Y (1994) Observations on the micro-organisms occurring in the gut of the pea aphid Acyrthosiphon pisum. Entomol Exp Appl 70:91–96. https://doi.org/10.1111/j.1570-7458.1994.tb01762.x CrossRefGoogle Scholar
  20. 20.
    Harada HHO, Ishikawa AH (1996) A consideration about the origin of aphid intracellular symbiont in connection with gut bacterial flora. J. Gen. Appl. Microbiol. 42:17–26. https://doi.org/10.2323/jgam.42.17 CrossRefGoogle Scholar
  21. 21.
    Harada H, Oyaizu H, Kosako Y, Ishikawa H (1997) Erwinia aphidicola, a new species isolated from pea aphid, Acyrthosiphon pisum. J Gen Appl Microbiol 43:349–354. https://doi.org/10.2323/jgam.43.349 CrossRefPubMedGoogle Scholar
  22. 22.
    Degnan PH, Yu Y, Sisneros N, et al. (2009) Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc. Natl. Acad. Sci. U. S. A. 106:9063–9068. https://doi.org/10.1073/pnas.0900194106 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Burke GR, N a M (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 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Haynes S, Darby AC, Daniell TJ, et al. (2003) Diversity of bacteria associated with natural aphid populations diversity of bacteria associated with natural aphid populations. Appl. Environ. Microbiol. 69:7216–7223. https://doi.org/10.1128/AEM.69.12.7216 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Jones RT, Bressan A, Greenwell AM, Fierer N (2011) Bacterial communities of two parthenogenetic aphid species cocolonizing two host plants across the Hawaiian Islands. Appl. Environ. Microbiol. 77:8345–8349. https://doi.org/10.1128/AEM.05974-11 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Jing X, Wong AC-N, Chaston JM, et al. (2014) The bacterial communities in plant phloem-sap-feeding insects. Mol. Ecol. 23:1433–1444. https://doi.org/10.1111/mec.12637 CrossRefPubMedGoogle Scholar
  27. 27.
    Gauthier J-P, Outreman Y, Mieuzet L, Simon J-C (2015) Bacterial communities associated with host-adapted populations of pea aphids revealed by deep sequencing of 16S ribosomal DNA. PLoS One 10:e0120664. https://doi.org/10.1371/journal.pone.0120664 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Najar-Rodríguez AJ, E a MG, Mensah RK, et al. (2009) The microbial flora of Aphis gossypii: patterns across host plants and geographical space. J. Invertebr. Pathol. 100:123–126. https://doi.org/10.1016/j.jip.2008.10.005 CrossRefPubMedGoogle Scholar
  29. 29.
    Lagier JC, Armougom F, Million M, et al. (2012) Microbial culturomics: paradigm shift in the human gut microbiome study. Clin. Microbiol. Infect. 18:1185–1193. https://doi.org/10.1111/1469-0691.12023 CrossRefPubMedGoogle Scholar
  30. 30.
    Leroy PD, Sabri A, Heuskin S, et al. (2011) Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies. Nat. Commun. 2:348. https://doi.org/10.1038/ncomms1347 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Fischer CY, Lognay GC, Detrain C, et al. (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 CrossRefGoogle Scholar
  32. 32.
    Foray V, Grigorescu a S, Sabri a, et al. (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:e00767-14–e00767-14. https://doi.org/10.1128/genomeA.00767-14 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Lagier J-C, Hugon P, Khelaifia S, et al. (2015) The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota. Clin. Microbiol. Rev. 28:237–264. https://doi.org/10.1128/CMR.00014-14 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Sabri A, Leroy P, Haubruge E, et al. (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 CrossRefPubMedGoogle Scholar
  35. 35.
    Sabri A, Vandermoten S, Leroy PD, et al. (2013) Proteomic investigation of aphid honeydew reveals an unexpected diversity of proteins. PLoS One 8:e74656. https://doi.org/10.1371/journal.pone.0074656 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Blackman RLEV (2000) Aphids on the world’s crops: an identification and information guide, 2nd edn. Wiley, Hoboken, Google Scholar
  37. 37.
    Altschul SF, Gish W, Miller W, et al. (1990) Basic local alignment search tool. J. Mol. Biol. 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2 CrossRefPubMedGoogle Scholar
  38. 38.
    Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406–425PubMedGoogle Scholar
  40. 40.
    Zimmer KR, Seixas a, Conceição JM, et al. (2013) Cattle tick-associated bacteria exert anti-biofilm and anti-Tritrichomonas foetus activities. Vet. Microbiol. 164:171–176. https://doi.org/10.1016/j.vetmic.2013.01.029 CrossRefPubMedGoogle Scholar
  41. 41.
    Kim H, Park DS, HW O, et al. (2012) Gryllotalpicola gen. nov., with descriptions of Gryllotalpicola koreensis sp. nov., Gryllotalpicola daejeonensis sp. nov. and Gryllotalpicola kribbensis sp. nov. from the gut of the African mole cricket, Gryllotalpa africana, and reclassification of Curto. Int. J. Syst. Evol. Microbiol. 62:2363–2370. https://doi.org/10.1099/ijs.0.034678-0 CrossRefPubMedGoogle Scholar
  42. 42.
    Clark EL, Daniell TJ, Wishart JH, KA SF (2012) How conserved are the bacterial communities associated with aphids? A detailed assessment of the Brevicoryne brassicae (Hemiptera: Aphididae) using 16S rDNA. Environ. Entomol. 41:1386–1397. https://doi.org/10.1603/EN12152 CrossRefPubMedGoogle Scholar
  43. 43.
    Boucias DG, Garcia-Maruniak A, Cherry R, et al. (2012) Detection and characterization of bacterial symbionts in the Heteropteran, Blissus insularis. FEMS Microbiol. Ecol. 82:629–641. https://doi.org/10.1111/j.1574-6941.2012.01433.x CrossRefPubMedGoogle Scholar
  44. 44.
    Matsuura Y, Kikuchi Y, Meng XY, et al. (2012) Novel clade of alphaproteobacterial endosymbionts associated with stinkbugs and other arthropods. Appl. Environ. Microbiol. 78:4149–4156. https://doi.org/10.1128/AEM.00673-12 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Chanbusarakum L, Ullman D (2008) Characterization of bacterial symbionts in Frankliniella occidentalis (Pergande), western flower thrips. J. Invertebr. Pathol. 99:318–325. https://doi.org/10.1016/j.jip.2008.09.001 CrossRefPubMedGoogle Scholar
  46. 46.
    Li T, Xiao JH, YQ W, Huang DW (2014) Diversity of bacterial symbionts in populations of Sitobion miscanthi (Hemiptera: Aphididae) in China. Environ. Entomol. 43:605–611. https://doi.org/10.1603/EN13229 CrossRefPubMedGoogle Scholar
  47. 47.
    Fukatsu T, Ishikawa H (1996) Phylogenetic position of yeast-like symbiont of Hamiltonaphis styraci (Homoptera, Aphididae) based on 18S rRNA gene sequeences. Insect Biochem. Mol. Biol. 26:383–388Google Scholar
  48. 48.
    Oliver KM, Degnan PH, Burke GR, N a M (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 CrossRefPubMedGoogle Scholar
  49. 49.
    Engel P, N a M (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 CrossRefPubMedGoogle Scholar
  50. 50.
    McFall-Ngai M, Hadfield MG, Bosch TCG, et al. (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 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    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 CrossRefPubMedGoogle Scholar
  52. 52.
    Kikuchi Y, Hayatsu M, Hosokawa T, et al. (2012) Symbiont-mediated insecticide resistance. Proc. Natl. Acad. Sci. 109:8618–8622. https://doi.org/10.1073/pnas.1200231109 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Kwong WK, Moran NA (2016) Gut microbial communities of social bees. Nat Rev Microbiol 14:374–384. https://doi.org/10.1038/nrmicro.2016.43 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Azambuja P, Garcia ES, Ratcliffe NA (2005) Gut microbiota and parasite transmission by insect vectors. Trends Parasitol. 21:568–572. https://doi.org/10.1016/j.pt.2005.09.011 CrossRefPubMedGoogle Scholar
  55. 55.
    Favia G, Ricci I, Damiani C, et al. (2007) Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc. Natl. Acad. Sci. 104:9047–9051. https://doi.org/10.1073/pnas.0610451104 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Boissière A, Tchioffo MT, Bachar D, et al. (2012) Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathog. 8:e1002742. https://doi.org/10.1371/journal.ppat.1002742 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Dillon RJ, Vennard CT, Charnley AK (2002) A note: gut bacteria produce components of a locust cohesion pheromone. J. Appl. Microbiol. 92:759–763. https://doi.org/10.1046/j.1365-2672.2002.01581.x CrossRefPubMedGoogle Scholar
  58. 58.
    Blackwood KS, He C, Gunton J, et al. (2000) Evaluation of recA sequences for identification of Mycobacterium species. J. Clin. Microbiol. 38:2846–2852PubMedPubMedCentralGoogle Scholar
  59. 59.
    Harada H, Ishikawa H (1997) Experimental pathogenicity of Erwinia aphidicola to pea aphid, Acyrthosiphon pisum. J. Gen. Appl. Microbiol. 43:363–367. https://doi.org/10.2323/jgam.43.363 CrossRefPubMedGoogle Scholar
  60. 60.
    Stavrinides J, McCloskey JK, Ochman H (2009) Pea aphid as both host and vector for the phytopathogenic bacterium Pseudomonas syringae. Appl. Environ. Microbiol. 75:2230–2235. https://doi.org/10.1128/AEM.02860-08 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Stavrinides J, No A, Ochman H (2010) A single genetic locus in the phytopathogen Pantoea stewartii enables gut colonization and pathogenicity in an insect host. Environ. Microbiol. 12:147–155. https://doi.org/10.1111/j.1462-2920.2009.02056.x CrossRefPubMedGoogle Scholar
  62. 62.
    Costechareyre D, Balmand S, Condemine G, Rahbé Y (2012) Dickeya dadantii, a plant pathogenic bacterium producing Cyt-like entomotoxins, causes septicemia in the pea aphid Acyrthosiphon pisum. PLoS One 7:e30702. https://doi.org/10.1371/journal.pone.0030702 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Renoz F, Noël C, Errachid A, et al. (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 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230. https://doi.org/10.1038/nrmicro2262 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Vorwerk S, Martinez-Torres D, Forneck A (2007) Pantoea agglomerans-associated bacteria in grape phylloxera (Daktulosphaira vitifoliae, Fitch). Agric. For. Entomol. 9:57–64. https://doi.org/10.1111/j.1461-9563.2006.000319.x CrossRefGoogle Scholar
  66. 66.
    Cruz AT, Cazacu AC, Allen CH (2007) Pantoea agglomerans, a plant pathogen causing human disease. J. Clin. Microbiol. 45:1989–1992. https://doi.org/10.1128/JCM.00632-07 CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Miller SH, Mark GL, Franks A, O’Gara F (2008) Pseudomonas–plant interactions. In: Rehm BHA (ed) Pseudomonas. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, pp. 353–376CrossRefGoogle Scholar
  68. 68.
    Gulati A, Vyas P, Rahi P, Kasana RC (2009) Plant growth-promoting and rhizosphere-competent Acinetobacter rhizosphaerae strain BIHB 723 from the cold deserts of the Himalayas. Curr. Microbiol. 58:371–377. https://doi.org/10.1007/s00284-008-9339-x CrossRefPubMedGoogle Scholar
  69. 69.
    Lebreton F, Willems RJL, Gilmore MS (2014) Enterococcus diversity, origins in nature, and gut colonization. In: Gilmore MS, Clewell DB, Ike Y, et al. (eds) Enterococci: from commensals to leading causes of drug resistant infection. Massachusetts Eye and Ear Infirmary, Boston, https://www.ncbi.nlm.nih.gov/books/NBK190427/
  70. 70.
    Fang H, Lv W, Huang Z, et al. (2015) Gryllotalpicola reticulitermitis sp. nov., isolated from a termite gut. Int. J. Syst. Evol. Microbiol. 65:85–89. https://doi.org/10.1099/ijs.0.062984-0 CrossRefPubMedGoogle Scholar
  71. 71.
    Mason KL, Stepien TA, Blum JE, et al. (2011) From commensal to pathogen: translocation of Enterococcus faecalis from the midgut to the hemocoel of Manduca sexta. mBio 2:e00065-11. https://doi.org/10.1128/mBio.00065-11 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Caspi-Fluger A, Inbar M, Mozes-Daube N, et al (2011) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc R Soc B Biol Sci rspb20112095. https://doi.org/10.1098/rspb.2011.2095
  73. 73.
    Xu Y, Buss EA, Boucias DG (2016) Environmental transmission of the gut symbiont Burkholderia to phloem-feeding Blissus insularis. PLoS One 11:e0161699. https://doi.org/10.1371/journal.pone.0161699 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Gerardo NM, Altincicek B, Anselme C, et al. (2010) Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol. 11:R21. https://doi.org/10.1186/gb-2010-11-2-r21 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Kaltenpoth M (2009) Actinobacteria as mutualists: general healthcare for insects? Trends Microbiol. 17:529–535. https://doi.org/10.1016/j.tim.2009.09.006 CrossRefPubMedGoogle Scholar
  76. 76.
    Pineda A, Soler R, Weldegergis BT, et al. (2013) Non-pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid-induced plant volatiles via jasmonic acid signalling. Plant Cell Environ. 36:393–404. https://doi.org/10.1111/j.1365-3040.2012.02581.x CrossRefPubMedGoogle Scholar
  77. 77.
    Fischer CY, Lognay GC, Detrain C, et al (2015) Bacteria may enhance species association in an ant–aphid mutualistic relationship. Chemoecology. https://doi.org/10.1007/s00049-015-0188-3
  78. 78.
    Halpern M, Fridman S, Atamna-Ismaeel N, Izhaki I (2013) Rosenbergiella nectarea gen. nov., sp. nov., in the family Enterobacteriaceae, isolated from floral nectar. Int. J. Syst. Evol. Microbiol. 63:4259–4265. https://doi.org/10.1099/ijs.0.052217-0 CrossRefPubMedGoogle Scholar
  79. 79.
    Lenaerts M, Álvarez-Pérez S, de Vega C, et al (2014) Rosenbergiella australoborealis sp. nov., Rosenbergiella collisarenosi sp. nov. and Rosenbergiella epipactidis sp. nov., three novel bacterial species isolated from floral nectar. Syst Appl Microbiol. https://doi.org/10.1016/j.syapm.2014.03.002
  80. 80.
    Samuni-Blank M, Izhaki I, Laviad S, et al (2014) The role of abiotic environmental conditions and herbivory in shaping bacterial community composition in floral nectar. PLoS One. https://doi.org/10.1371/journal.pone.0099107
  81. 81.
    Pérez-Brocal V, Latorre A, Moya A (2011) Symbionts and pathogens: what is the difference? In: Dobrindt U, Hacker JH, Svanborg C (eds) Between pathogenicity and commensalism. Springer, Berlin, pp. 215–243Google Scholar
  82. 82.
    Duron O, Noël V, McCoy KD, et al. (2015) The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii. PLoS Pathog. 11:e1004892. https://doi.org/10.1371/journal.ppat.1004892 CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Bordenstein SR, Paraskevopoulos C, Dunning Hotopp JC, et al. (2009) Parasitism and mutualism in Wolbachia: what the phylogenomic trees can and cannot say. Mol. Biol. Evol. 26:231–241. https://doi.org/10.1093/molbev/msn243 CrossRefPubMedGoogle Scholar
  84. 84.
    Newton AC, Fitt BDL, Atkins SD, et al. (2010) Pathogenesis, parasitism and mutualism in the trophic space of microbe–plant interactions. Trends Microbiol. 18:365–373. https://doi.org/10.1016/j.tim.2010.06.002 CrossRefPubMedGoogle Scholar
  85. 85.
    Pineda A, Zheng SJ, JJ a v L, et al. (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci. 15:507–514. https://doi.org/10.1016/j.tplants.2010.05.007 CrossRefPubMedGoogle Scholar
  86. 86.
    Gosalbes MJ, Lamelas A, Moya A, Latorre A (2008) The striking case of tryptophan provision in the cedar aphid Cinara cedri. J. Bacteriol. 190:6026–6029. https://doi.org/10.1128/JB.00525-08 CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Oakeson KF, Gil R, Clayton AL, et al. (2014) Genome degeneration and adaptation in a nascent stage of symbiosis. Genome Biol Evol 6:76–93. https://doi.org/10.1093/gbe/evt210 CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Moriwaki NM, Atsushita KM, Ishina MN, Ono YK (2003) High concentrations of trehalose in aphid hemolymph. Appl. Entomol. Zool. 38:241–248CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Walloon Center of Industrial BiologyUniversité de LiègeLiègeBelgium
  2. 2.Earth and Life Institute, Biodiversity Research CenterUniversité Catholique de LouvainLouvain-la-NeuveBelgium
  3. 3.Artechno SAIsnesBelgium
  4. 4.Centre de Recherches de Biochimie Macromoléculaire (UMR-CNRS 5237)Montpellier Cedex 05France

Personalised recommendations