Vanderpoorten, Alain ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et de la conservation - aCREA-Ulg
Bataille, G.
Noël, C.
Foray, V.
Pierson, V.
Hance, T.
Language :
English
Title :
Evidence for Gut-Associated Serratia symbiotica in Wild Aphids and Ants Provides New Perspectives on the Evolution of Bacterial Mutualism in Insects
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. 10.1073/pnas.1218525110
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. 10.1146/annurev-ento-112408-085305
Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543. 10.1111/j.1365-2311.2011.01318.x
Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190. 10.1146/annurev.genet.41.110306.130119
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. 10.1098/rstb.2010.0226
Sandström JP, Russell JA, White JP, Moran NA (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 10:217–228. 10.1046/j.1365-294X.2001.01189.x
Duron O, Wilkes TE, Hurst GDD (2010) Interspecific transmission of a male-killing bacterium on an ecological timescale. Ecol Lett 13:1139–1148. 10.1111/j.1461-0248.2010.01502.x
Gehrer L, Vorburger C (2012) Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Lett rsbl20120144. 10.1098/rsbl.2012.0144
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. 10.1111/mec.12092
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. 10.1126/science.1195463
Dion E, Polin SE, Simon J-C, Outreman Y (2011) Symbiont infection affects aphid defensive behaviours. Biol Lett 7:743–746. 10.1098/rsbl.2011.0249
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. 10.1371/journal.pone.0021831
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. 10.1111/1365-2435.12133
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. 10.1007/s10682-016-9856-1
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. 10.1371/journal.pbio.0050114
Teixeira L, Ferreira Á, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6:e1000002. 10.1371/journal.pbio.1000002
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. 10.1073/pnas.94.20.10792
Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230. 10.1038/nrmicro2262
Egan S, Thomas T (2015) Microbial symbiosis of marine sessile hosts - diversity, function and applications. Frontiers Media SA
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. 10.1098/rspb.2014.2957
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. 10.1371/journal.pgen.1002990
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. 10.1007/s00442-015-3488-y
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. 10.1371/journal.pgen.1002357
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. 10.1128/AEM.00141-11
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. 10.1093/gbe/evw085
Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195. 10.1046/j.1365-2311.2002.00393.x
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. 10.1038/ismej.2009.114
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. 10.1073/pnas.0335320100
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. 10.1128/genomeA.00767-14
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. 10.1099/ijs.0.024133-0
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. 10.1007/s00248-017-1092-x
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. 10.7717/peerj.3291
Manzano-Marín A, Latorre A (2016) Snapshots of a shrinking partner: genome reduction in Serratia symbiotica. Sci Rep 6. 10.1038/srep32590
Henry LM, Maiden MCJ, Ferrari J, Godfray HCJ (2015) Insect life history and the evolution of bacterial mutualism. Ecol Lett 18:516–525. 10.1111/ele.12425
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. 10.1073/pnas.0510466103
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. 10.1371/journal.pone.0097620
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
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. 10.1371/journal.pone.0122099
Burke GR, Moran NA (2011) Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol 3:195–208. 10.1093/gbe/evr002
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. 10.1093/gbe/evu133
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
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. 10.1016/j.cub.2013.07.029
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. 10.1111/evo.12767
Degnan PH, Moran NA (2008) Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage. Mol Ecol 17:916–929. 10.1111/j.1365-294X.2007.03616.x
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. 10.1093/bioinformatics/bts199
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772. 10.1038/nmeth.2109
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. 10.1093/bioinformatics/btm388
Ryuichi Koga TT (2009) Quenching autofluorescence of insect tissues for in situ detection of endosymbionts. Appl Entomol Zool - APPL ENTOMOL ZOOL 44:281–291. 10.1303/aez.2009.281
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. 10.1146/annurev.mi.49.100195.000415
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. 10.1038/srep19967
Eisner T, Wilson EO (1952) The morphology of the proventriculus of a formicine ant. Psyche J Entomol 59:47–60. 10.1155/1952/14806
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. 10.1038/ismej.2015.264
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. 10.1128/AEM.71.6.3302-3310.2005
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. 10.1073/pnas.1119212109
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. 10.1111/1462-2920.13633
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. 10.1038/ncomms1347
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. 10.1007/s00049-015-0188-3
Darby AC, Douglas AE (2003) Elucidation of the transmission patterns of an insect-borne bacterium. Appl Environ Microbiol 69:4403–4407. 10.1128/AEM.69.8.4403-4407.2003
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. 10.1371/journal.pone.0074656
Buckley RC (1987) Interactions involving plants, Homoptera, and ants. Annu Rev Ecol Syst 18:111–135
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. 10.1303/aez.2003.427
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
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. 10.1016/j.anbehav.2003.10.016
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. 10.1111/j.1439-0310.1997.tb00180.x
Sirviö A, Pamilo P (2010) Multiple endosymbionts in populations of the ant Formica cinerea. BMC Evol Biol 10:335. 10.1186/1471-2148-10-335
He H, Chen Y, Zhang Y, Wei C (2011) Bacteria associated with gut lumen of Camponotus japonicus Mayr. Environ Entomol 40:1405–1409. 10.1603/EN11157
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. 10.1007/s00284-012-0197-1
Engel P, Moran NA (2013) The gut microbiota of insects—diversity in structure and function. FEMS Microbiol Rev 37:699–735. 10.1111/1574-6976.12025
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. 10.1073/pnas.0907926106
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. 10.1111/mec.12607
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. 10.1098/rspb.2003.2537
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. 10.1093/femsec/fiy003
Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92. 10.1146/annurev.ento.49.061802.123416
Hansen AK, Moran NA (2014) The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol Ecol 23:1473–1496. 10.1111/mec.12421
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. 10.1371/journal.ppat.1000542
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. 10.1126/science.1201618
Koch H, Schmid-Hempel P (2011) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci 108:19288–19292. 10.1073/pnas.1110474108
