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

Volumn 10, Issue 3, 2015, Pages

  Renoz, François ^a   Noël, Christine ^a   Errachid, Abdelmounaim ^b   Foray, Vincent ^a   Hance, Thierry ^a  

^a EARTH AND LIFE INSTITUTE   (Belgium)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

STRESS ACTIVATED PROTEIN KINASE;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COLONIZATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; IMMUNE RESPONSE; INTESTINE; LYSOSOME; NONHUMAN; PEA APHID; SERRATIA; SERRATIA INFECTION; SERRATIA MARCESCENS; SERRATIA SYMBIOTICA; SIGNAL TRANSDUCTION; SURVIVAL; SYMBIOSIS; ANIMAL; APHID; BACTERIUM; GENE; GENE EXPRESSION PROFILING; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INTESTINE FLORA; MICROBIOLOGY; TIME FACTOR;

ACYRTHOSIPHON PISUM; APHIDIDAE; BACTERIA (MICROORGANISMS); BUCHNERA APHIDICOLA; CANDIDATUS SERRATIA SYMBIOTICA; INVERTEBRATA; PISUM; SERRATIA MARCESCENS;

ANIMALS; APHIDS; BACTERIA; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION PROFILING; GENES, INSECT; HOST-PATHOGEN INTERACTIONS; SYMBIOSIS; TIME FACTORS;

EID: 84926318672     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122099     Document Type: Article

References (78)

1. Schmid-Hempel P. Evolutionary ecology of insect immune defenses. Annu Rev Entomol. 2005; 50: 529-551. doi: 10.1146/annurev.ento.50.071803.130420 PMID: 15471530
2. Ferrandon D, Imler J-L, Hetru C, Hoffmann JA. The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol. 2007; 7: 862-874. doi: 10.1038/nri2194 PMID: 17948019
3. Christophides GK, Vlachou D, Kafatos FC. Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae. Immunol Rev. 2004; 198: 127-148. PMID: 15199960
4. Altincicek B, Vilcinskas A. Identification of immune-related genes from an apterygote insect, the firebrat Thermobia domestica. Insect Biochem Mol Biol. 2007; 37: 726-731. doi: 10.1016/j.ibmb.2007.03.012 PMID: 17550828
5. Evans JD, Aronstein K, Chen YP, Hetru C, Imler J-L, Jiang H, et al. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol. 2006; 15: 645-656. doi: 10.1111/j.1365-2583.2006.00682.x PMID: 17069638
6. Anselme C, Pérez-Brocal V, Vallier A, Vincent-Monegat C, Charif D, Latorre A, et al. Identification of the Weevil immune genes and their expression in the bacteriome tissue. BMC Biol. 2008; 6: 43. doi: 10.1186/1741-7007-6-43 PMID: 18925938
7. Altincicek B, Knorr E, Vilcinskas A. Beetle immunity: Identification of immune-inducible genes from the model insect Tribolium castaneum. Dev Comp Immunol. 2008; 32: 585-595. doi: 10.1016/j.dci.2007.09.005 PMID: 17981328
8. Nappi AJ, Christensen BM. Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem Mol Biol. 2005; 35: 443-459. doi: 10.1016/j.ibmb.2005.01.014 PMID: 15804578
9. Jiravanichpaisal P, Lee BL, Söderhäll K. Cell-mediated immunity in arthropods: Hematopoiesis, coagulation, melanization and opsonization. Immunobiology. 2006; 211: 213-236. doi: 10.1016/j.imbio.2005. 10.015 PMID: 16697916
10. Lemaitre B, Hoffmann J. The host defense of Drosophila melanogaster. Annu Rev Immunol. 2007; 25: 697-743. doi: 10.1146/annurev.immunol.25.022106.141615 PMID: 17201680
11. Aguilar R, Jedlicka AE, Mintz M, Mahairaki V, Scott AL, Dimopoulos G. Global gene expression analysis of Anopheles gambiae responses to microbial challenge. Insect Biochem Mol Biol. 2005; 35: 709-719. doi: 10.1016/j.ibmb.2005.02.019 PMID: 15894188
12. De Morais Guedes S, Vitorino R, Domingues R, Tomer K, Correia AJF, Amado F, et al. Proteomics of immune-challenged Drosophila melanogaster larvae hemolymph. Biochem Biophys Res Commun. 2005; 328: 106-115. doi: 10.1016/j.bbrc.2004.12.135 PMID: 15670757
13. Rivero A. Nitric oxide: an antiparasitic molecule of invertebrates. Trends Parasitol. 2006; 22: 219-225. doi: 10.1016/j.pt.2006.02.014 PMID: 16545612
14. Vallet-Gely I, Lemaitre B, Boccard F. Bacterial strategies to overcome insect defences. Nat Rev Microbiol. 2008; 6: 302-313. doi: 10.1038/nrmicro1870 PMID: 18327270
15. Futahashi R, Tanaka K, Tanahashi M, Nikoh N, Kikuchi Y, Lee BL, et al. Gene Expression in Gut Symbiotic Organ of Stinkbug Affected by Extracellular Bacterial Symbiont. PLoS ONE. 2013; 8: e64557. doi: 10.1371/journal.pone.0064557 PMID: 23691247
16. Buchner P. Endosymbiosis of Animals with Plant Microorganisms. Revised edition. Interscience Publishers / John Wiley; 1965.
17. Douglas AE. Nutritional Interactions in Insect-Microbial Symbioses: Aphids and Their Symbiotic Bacteria Buchnera. Annu Rev Entomol. 1998; 43: 17-37. doi: 10.1146/annurev.ento.43.1.17 PMID: 15012383
18. Akman Gündüz E, Douglas AE. Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc Biol Sci. 2009; 276: 987-991. doi: 10.1098/rspb.2008.1476 PMID: 19129128
19. Snyder AK, Deberry JW, Runyen-Janecky L, Rio RVM. Nutrient provisioning facilitates homeostasis between tsetse fly (Diptera: Glossinidae) symbionts. Proc Biol Sci. 2010; 277: 2389-2397. doi: 10.1098/rspb.2010.0364 PMID: 20356887
20. Vigneron A, Masson F, Vallier A, Balmand S, Rey M, Vincent-Monégat C, et al. Insects Recycle Endosymbionts when the Benefit Is Over. Curr Biol. 2014; 24: 2267-2273. doi: 10.1016/j.cub.2014.07.065 PMID: 25242028
21. Moran NA, McCutcheon JP, Nakabachi A. Genomics and Evolution of Heritable Bacterial Symbionts. Annu Rev Genet. 2008; 42: 165-190. doi: 10.1146/annurev.genet.41.110306.130119 PMID: 18983256
22. Oliver KM, Degnan PH, Burke GR, Moran NA. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol. 2010; 55: 247-266. doi: 10.1146/annurev-ento-112408-085305 PMID: 19728837
23. van Ham RCHJ, Kamerbeek J, Palacios C, Rausell C, Abascal F, Bastolla U, et al. Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci. 2003; 100: 581-586. doi: 10.1073/pnas.0235981100 PMID: 12522265
24. Oliver KM, Russell JA, Moran NA, Hunter MS. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci. 2003; 100: 1803-1807. doi: 10.1073/pnas.0335320100 PMID: 12563031
25. Scarborough CL, Ferrari J, Godfray HCJ. Aphid protected from pathogen by endosymbiont. Science. 2005; 310: 1781. doi: 10.1126/science.1120180 PMID: 16357252
26. Tsuchida T, Koga R, Fukatsu T. Host Plant Specialization Governed by Facultative Symbiont. Science. 2004; 303: 1989-1989. doi: 10.1126/science.1094611 PMID: 15044797
27. Burke G, Fiehn O, Moran N. Effects of facultative symbionts and heat stress on the metabolome of pea aphids. ISME J. 2009; 4: 242-252. doi: 10.1038/ismej.2009.114 PMID: 19907504
28. Montllor CB, Maxmen A, Purcell AH. Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol. 2002; 27: 189-195. doi: 10.1046/j.1365-2311.2002.00393.x
29. Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T, Matsumoto S, et al. Symbiotic bacterium modifies aphid body color. Science. 2010; 330: 1102-1104. doi: 10.1126/science.1195463 PMID: 21097935
30. Jousselin E, Coeur d'Acier A, Vanlerberghe-Masutti F, Duron O. Evolution and diversity of Arsenophonus endosymbionts in aphids. Mol Ecol. 2013; 22: 260-270. doi: 10.1111/mec.12092 PMID: 23106652
31. Sandström JP, Russell JA, White JP, Moran NA. Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol. 2001; 10: 217-228. doi: 10.1046/j.1365-294X.2001.01189.x PMID: 11251800
32. Kikuchi Y, Hosokawa T, Fukatsu T. Insect-Microbe Mutualism without Vertical Transmission: a Stinkbug Acquires a Beneficial Gut Symbiont from the Environment Every Generation. Appl Environ Microbiol. 2007; 73: 4308-4316. doi: 10.1128/AEM.00067-07 PMID: 17483286
33. Clayton AL, Oakeson KF, Gutin M, Pontes A, Dunn DM, von Niederhausern AC, et al. A Novel Human-Infection-Derived Bacterium Provides Insights into the Evolutionary Origins of Mutualistic Insect - Bacterial Symbioses. PLoS Genet. 2012; 8: e1002990. doi: 10.1371/journal.pgen.1002990 PMID: 23166503
34. Caspi-Fluger A, Inbar M, Mozes-Daube N, Katzir N, Portnoy V, Belausov E, et al. Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc R Soc B Biol Sci. 2011; rspb20112095. doi: 10.1098/rspb.2011.2095
35. Gehrer L, Vorburger C. Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Lett. 2012; rsbl20120144. doi: 10.1098/rsbl.2012.0144
36. Dale C, Moran NA. Molecular Interactions between Bacterial Symbionts and Their Hosts. Cell. 2006; 126: 453-465. doi: 10.1016/j.cell.2006.07.014 PMID: 16901780
37. Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA. Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci. 2009; 106: 9063-9068. doi: 10.1073/pnas.0900194106 PMID: 19451630
38. The International Aphid Genomics Consortium. Genome Sequence of the Pea Aphid Acyrthosiphon pisum. PLoS Biol. 2010; 8: e1000313. doi: 10.1371/journal.pbio.1000313 PMID: 20186266
39. Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM, de Vos M, et al. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol. 2010; 11: R21. doi: 10.1186/gb-2010-11-2-r21 PMID: 20178569
40. Laughton AM, Garcia JR, Altincicek B, Strand MR, Gerardo NM. Characterisation of immune responses in the pea aphid, Acyrthosiphon pisum. J Insect Physiol. 2011; 57: 830-839. doi: 10.1016/j.jinsphys.2011.03.015 PMID: 21439291
41. Schmitz A, Anselme C, Ravallec M, Rebuf C, Simon J-C, Gatti J-L, et al. The Cellular Immune Response of the Pea Aphid to Foreign Intrusion and Symbiotic Challenge. PLoS ONE. 2012; 7: e42114. doi: 10.1371/journal.pone.0042114 PMID: 22848726
42. Altincicek B, Gross J, Vilcinskas A. Wounding-mediated gene expression and accelerated viviparous reproduction of the pea aphid Acyrthosiphon pisum. Insect Mol Biol. 2008; 17: 711-716. doi: 10.1111/j.1365-2583.2008.00835.x PMID: 18823444
43. Petersen LM, Tisa LS. Friend or foe? A review of the mechanisms that drive Serratia towards diverse lifestyles. Can J Microbiol. 2013; 59: 627-640. doi: 10.1139/cjm-2013-0343 PMID: 24011346
44. Nehme NT, Liégeois S, Kele B, Giammarinaro P, Pradel E, Hoffmann JA, et al. A Model of Bacterial Intestinal Infections in Drosophila melanogaster. PLoS Pathog. 2007; 3: e173. doi: 10.1371/journal.ppat.0030173 PMID: 18039029
45. Gosalbes MJ, Lamelas A, Moya A, Latorre A. The Striking Case of Tryptophan Provision in the Cedar Aphid Cinara cedri. J Bacteriol. 2008; 190: 6026-6029. doi: 10.1128/JB.00525-08 PMID: 18586942
46. Lamelas A, Gosalbes MJ, Manzano-Marín A, Peretó J, Moya A, Latorre A. Serratia symbiotica from the Aphid Cinara cedri: A Missing Link from Facultative to Obligate Insect Endosymbiont. PLoS Genet. 2011; 7: e1002357. doi: 10.1371/journal.pgen.1002357 PMID: 22102823
47. Sabri A, Leroy P, Haubruge E, Hance T, Frère I, Destain J, et al. 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. 2011; 61: 2081-2088. doi: 10.1099/ijs.0.024133-0 PMID: 20870890
48. Dubreuil G, Deleury E, Crochard D, Simon J-C, Coustau C. Diversification of MIF immune regulators in aphids: link with agonistic and antagonistic interactions. BMC Genomics. 2014; 15: 762. doi: 10.1186/1471-2164-15-762 PMID: 25193628
49. Bright M, Bulgheresi S. A complex journey: transmission of microbial symbionts. Nat Rev Microbiol. 2010; 8: 218-230. doi: 10.1038/nrmicro2262 PMID: 20157340
50. Flyg C, Kenne K, Boman HG. Insect pathogenic properties of Serratia marcescens: phage-resistant mutants with a decreased resistance to Cecropia immunity and a decreased virulence to Drosophila. J Gen Microbiol. 1980; 120: 173-181. PMID: 7012273
51. Fukatsu T, Nikoh N, Kawai R, Koga R. The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta: homoptera). Appl Environ Microbiol. 2000; 66: 2748-2758. PMID: 10877764
52. Altincicek B, Ter Braak B, Laughton AM, Udekwu KI, Gerardo NM. Escherichia coli K-12 pathogenicity in the pea aphid, Acyrthosiphon pisum, reveals reduced antibacterial defense in aphids. Dev Comp Immunol. 2011; 35: 1091-1097. doi: 10.1016/j.dci.2011.03.017 PMID: 21527277
53. Crawley MJ. The R Book. 1 edition. Chichester, England; Hoboken, N.J: Wiley; 2007.
54. Ryuichi Koga TT. Quenching autofluorescence of insect tissues for in situ detection of endosymbionts. Appl Entomol Zool - APPL ENTOMOL ZOOL. 2009; 44: 281-291. doi: 10.1303/aez.2009.281 PMID: 17364819
55. Nishikori K, Morioka K, Kubo T, Morioka M. Age- and morph-dependent activation of the lysosomal system and Buchnera degradation in aphid endosymbiosis. J Insect Physiol. 2009; 55: 351-357. doi: 10.1016/j.jinsphys.2009.01.001 PMID: 19183557
56. Dunbar HE, Wilson ACC, Ferguson NR, Moran NA. Aphid Thermal Tolerance Is Governed by a Point Mutation in Bacterial Symbionts. PLoS Biol. 2007; 5: e96. doi: 10.1371/journal.pbio.0050096 PMID: 17425405
57. Foray V, Grigorescu AS, Sabri A, Haubruge E, Lognay G, Francis F, et al. Whole-Genome Sequence of Serratia symbiotica Strain CWBI-2.3T, a Free-Living Symbiont of the Black Bean Aphid Aphis fabae. Genome Announc. 2014; 2: e00767-14. doi: 10.1128/genomeA.00767-14 PMID: 25146134
58. Mekalanos JJ. Environmental signals controlling expression of virulence determinants in bacteria. J Bacteriol. 1992; 174: 1-7. PMID: 1729202
59. Petersen LM, Tisa LS. Influence of temperature on the physiology and virulence of the insect pathogen Serratia sp. Strain SCBI. Appl Environ Microbiol. 2012; 78: 8840-8844. doi: 10.1128/AEM.02580-12 PMID: 23042169
60. Burke GR, Moran NA. Responses of the pea aphid transcriptome to infection by facultative symbionts. Insect Mol Biol. 2011; 20: 357-365. doi: 10.1111/j.1365-2583.2011.01070.x PMID: 21382108
61. Hultmark D. Insect lysozymes. EXS. 1996; 75: 87-102. PMID: 8765296
62. Nakabachi A, Shigenobu S, Sakazume N, Shiraki T, Hayashizaki Y, Carninci P, et al. Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera. Proc Natl Acad Sci U S A. 2005; 102: 5477-5482. doi: 10.1073/pnas.0409034102 PMID: 15800043
63. Callewaert L, Michiels CW. Lysozymes in the animal kingdom. J Biosci. 2010; 35: 127-160. PMID: 20413917
64. Chevalier F, Herbinière-Gaboreau J, Charif D, Mitta G, Gavory F, Wincker P, et al. Feminizing Wolbachia: a transcriptomics approach with insights on the immune response genes in Armadillidium vulgare. BMC Microbiol. 2012; 12: S1. doi: 10.1186/1471-2180-12-S1-S1 PMID: 22375708
65. Islam D, Bandholtz L, Nilsson J, Wigzell H, Christensson B, Agerberth B, et al. Downregulation of bactericidal peptides in enteric infections: a novel immune escape mechanism with bacterial DNA as a potential regulator. Nat Med. 2001; 7: 180-185. doi: 10.1038/84627 PMID: 11175848
66. Turk V, Turk B, Turk D. Lysosomal cysteine proteases: facts and opportunities. EMBO J. 2001; 20: 4629-4633. doi: 10.1093/emboj/20.17.4629 PMID: 11532926
67. Cristofoletti PT, Ribeiro AF, Deraison C, Rahbé Y, Terra WR. Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. J Insect Physiol. 2003; 49: 11-24. PMID: 12770012
68. Tryselius Y, Hultmark D. Cysteine proteinase 1 (CP1), a cathepsin L-like enzyme expressed in the Drosophila melanogaster haemocyte cell line mbn-2. Insect Mol Biol. 1997; 6: 173-181. PMID: 9099581
69. Wang L-F, Chai L-Q, He H-J, Wang Q, Wang J-X, Zhao X-F. A cathepsin L-like proteinase is involved in moulting and metamorphosis in Helicoverpa armigera. Insect Mol Biol. 2010; 19: 99-111. doi: 10.1111/j.1365-2583.2009.00952.x PMID: 20167021
70. Sapountzis P, Duport G, Balmand S, Gaget K, Jaubert-Possamai S, Febvay G, et al. New insight into the RNA interference response against cathepsin-L gene in the pea aphid, Acyrthosiphon pisum: molting or gut phenotypes specifically induced by injection or feeding treatments. Insect Biochem Mol Biol. 2014; 51: 20-32. doi: 10.1016/j.ibmb.2014.05.005 PMID: 24859468
71. Kremer N, Philipp EER, Carpentier M-C, Brennan CA, Kraemer L, Altura MA, et al. Initial symbiont contact orchestrates host-organ-wide transcriptional changes that prime tissue colonization. Cell Host Microbe. 2013; 14: 183-194. doi: 10.1016/j.chom.2013.07.006 PMID: 23954157
72. Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM, de Vos M, et al. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol. 2010; 11: R21. doi: 10.1186/gb-2010-11-2-r21 PMID: 20178569
73. Kaiwa N, Hosokawa T, Kikuchi Y, Nikoh N, Meng XY, Kimura N, et al. Primary gut symbiont and secondary, Sodalis-allied symbiont of the Scutellerid stinkbug Cantao ocellatus. Appl Environ Microbiol. 2010; 76: 3486-3494. doi: 10.1128/AEM.00421-10 PMID: 20400564
74. Sirviö A, Pamilo P. Multiple endosymbionts in populations of the ant Formica cinerea. BMC Evol Biol. 2010; 10: 335. doi: 10.1186/1471-2148-10-335 PMID: 21040533
75. He H, Chen Y, Zhang Y, Wei C. Bacteria associated with gut lumen of Camponotus japonicus Mayr. Environ Entomol. 2011; 40: 1405-1409. doi: 10.1603/EN11157 PMID: 22217755
76. Li X, Nan X, Wei C, He H. The gut bacteria associated with Camponotus japonicus Mayr with culture-dependent and DGGE methods. Curr Microbiol. 2012; 65: 610-616. doi: 10.1007/s00284-012-0197-1 PMID: 22878556
77. Oakeson KF, Gil R, Clayton AL, Dunn DM, von Niederhausern AC, Hamil C, et al. Genome degeneration and adaptation in a nascent stage of symbiosis. Genome Biol Evol. 2014; 6: 76-93. doi: 10.1093/gbe/evt210 PMID: 24407854
78. Kikuchi Y. Endosymbiotic Bacteria in Insects: Their Diversity and Culturability. Microbes Environ. 2009; 24: 195-204. doi: 10.1264/jsme2.ME09140S PMID: 21566374