Host and Symbiont Jointly Control Gut Microbiota during Complete Metamorphosis

PLoS Pathogens

Volumn 11, Issue 11, 2015, Pages

  Johnston, Paul R ^a   Rolff, Jens ^a,b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b BERLIN BRANDENBURG INSTITUTE OF ADVANCED BIODIVERSITY RESEARCH BBIB   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM COLONY; DISEASE CARRIER; GENE SEQUENCE; INTESTINE FLORA; METAMORPHOSIS; NONHUMAN; PLASMID; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; RNA INTERFERENCE; SEGREGATION ANALYSIS; SEQUENCE ANALYSIS; SURVIVAL; ANIMAL; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INSECT; LARVA; MICROBIOLOGY; MICROFLORA; SYMBIOSIS;

ANIMALS; GASTROINTESTINAL MICROBIOME; HOST-PATHOGEN INTERACTIONS; INSECTS; LARVA; METAMORPHOSIS, BIOLOGICAL; MICROBIOTA; SYMBIOSIS;

EID: 84948956933     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005246     Document Type: Article

References (56)

1. Misof B, Liu S, Meusemann K, Peters RS, Donath a, Mayer C, et al. Phylogenomics resolves the timing and pattern of insect evolution. Science. 2014; 346: 763–767. doi: 10.1126/science.1257570 25378627
2. Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B, How many species are there on Earth and in the ocean? PLoS Biol. 2011; 9: e1001127. doi: 10.1371/journal.pbio.1001127 21886479
3. Truman JW, Riddiford LM, The origins of insect metamorphosis. Nature. 1999; 401: 447–452. doi: 10.1038/46737 10519548
4. Grimaldi D, Engel M, Evolution of the Insects. Cambridge University Press; 2005.
5. Moran N, Adaptation and constraint in the complex life cycles of animals. Annu Rev Ecol Syst. 1994; 25: 573–600. Available: http://www.jstor.org/stable/2097325
6. Stansbury M, Moczek A, The evolvability of arthropods. Arthropod Biology and Evolution. Springer Berlin Heidelberg; 2013. pp. 479–493.
7. Leach JG, The method of survival of bacteria in the puparia of the seed-corn maggot (Hylernyia Cilicrura Rond.). Zeitschrift für Angew Entomol. 1934; 20: 150–161.
8. Bacot AW, On the Persistence of Bacilli in the Gut of an Insect during Metamorphosis. Trans Entomol Soc London. 1911; 497–500.
9. Bakula M, The persistence of a microbial flora during postembryogenesis of Drosophila melanogaster. J Invertebr Pathol. 1969;14: 365–374. doi: 10.1016/0022-2011(69)90163-3 4904970
10. Delalibera I, Vasanthakumar A, Burwitz B, Schloss PD, Klepzig KD, Handelsman J, et al. Composition of the bacterial community in the gut of the pine engraver, Ips pini (Say) (Coleoptera) colonizing red pine. Symbiosis. 2007; 43: 97–104.
11. Wong CNA, Ng P, Douglas AE, Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environ Microbiol. 2011; 13: 1889–1900. doi: 10.1111/j.1462-2920.2011.02511.x 21631690
12. Hammer TJ, McMillan WO, Fierer N, Metamorphosis of a butterfly-associated bacterial community. PLoS One. 2014;9: e86995. doi: 10.1371/journal.pone.0086995 24466308
13. Brucker RM, Bordenstein SR, The roles of host evolutionary relationships (genus: Nasonia) and development in structuring microbial communities. Evolution. 2012; 66: 349–362. doi: 10.1111/j.1558-5646.2011.01454.x 22276533
14. Greenberg B, Salmonella suppression by known populations of bacteria in flies. J Bacteriol. 1969; 99: 629–35. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=250072&tool=pmcentrez&rendertype=abstract 4984172
15. Greenberg B, Klowden M, Enteric Bacterial Interactions in Insects. Am J Clin Nutr. 1972; 25: 1459–1466. 4629542
16. Russell V, Dunn PE, Antibacterial proteins in the midgut of Manduca sexta during metamorphosis. J Insect Physiol. 1996;42: 65–71.
17. Tebbutt H, On the influence of metamorphosis of Musca domestica upon bacteria administered in the larval Stage. J Hyg (Lond). 1912;12: 516–526.
18. Buchon N, Broderick NA, Lemaitre B, Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat Rev Microbiol. 2013; 11: 615–626. doi: 10.1038/nrmicro3074 23893105
19. Wheeler D, Redding AJ, Werren JH, Characterization of an ancient lepidopteran lateral gene transfer. PLoS One. 2013; 8: e59262. doi: 10.1371/journal.pone.0059262 23533610
20. Van Frankenhuyzen K, Liu YH, Tonon A, Interactions between Bacillus thuringiensis subsp kurstaki HD-1 and midgut bacteria in larvae of gypsy moth and spruce budworm. J Invertebr Pathol. 2010;1 03: 124–131.
21. Hernández-Martínez P, Naseri B, Navarro-Cerrillo G, Escriche B, Ferré J, Herrero S, Increase in midgut microbiota load induces an apparent immune priming and increases tolerance to Bacillus thuringiensis. Environ Microbiol. 2010; 12: 2730–2737. doi: 10.1111/j.1462-2920.2010.02241.x 20482744
22. Broderick NA, Raffa KF, Goodman RM, Handelsman J, Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol. 2004; 70: 293–300. doi: 10.1128/AEM.70.1.293 14711655
23. Brooks MA, Steinhaus EA, The Microorganisms of Healthy Insects. In: Insect Pathology: An Advanced Treatise vol 1. London: Academic Press; 1963. pp. 215–250.
24. Martin JD, Mundt JO, Enterococci in insects. Appl Microbiol. 1972; 24: 575–80. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=380616&tool=pmcentrez&rendertype=abstract 4628796
25. Bucher GE, Survival of populations of Streptococcus faecalis Andrewes and Horder in the gut of Galleria mellonella (Linnaeus) during metamorphosis, and transmission of the bacteria to the filial generation of the host. J Insect Pathol. 1963; 5: 336–343.
26. Xiang H, Wei G, Jia S, Huang J, Miao X, Zhou Z, et al. Microbial communities in the larval midgut of laboratory and field populations of cotton bollworm (Helicoverpa armigera). Can J Microbiol. 2006; 52: 1085–1092. doi: 10.1139/W06-064 17215900
27. Raymond B, Johnston PR, Wright DJ, Ellis RJ, Crickmore N, Bonsall MB, A mid-gut microbiota is not required for the pathogenicity of Bacillus thuringiensis to diamondback moth larvae. Environ Microbiol. 2009; 11: 2556–2563. doi: 10.1111/j.1462-2920.2009.01980.x 19555371
28. Jarosz J, Gut flora of Galleria mellonella suppressing ingested bacteria. J Invertebr Pathol. 1979;34: 192–198. 119813
29. Johnston PR, Crickmore N, Gut bacteria are not required for the insecticidal activity of Bacillus thuringiensis toward the tobacco hornworm, Manduca sexta. Appl Environ Microbiol. 2009; 75: 5094–5099. doi: 10.1128/AEM.00966-09 19525273
30. Raymond B, Johnston PR, Nielsen-LeRoux C, Lereclus D, Crickmore N, Bacillus thuringiensis: an impotent pathogen? Trends Microbiol. 2010;18: 189–94. doi: 10.1016/j.tim.2010.02.006 20338765
31. Uwo MF, Ui-Tei K, Park P, Takeda M, Replacement of midgut epithelium in the greater wax moth, Galleria mellonela, during larval-pupal moult. Cell Tissue Res. 2002;308: 319–31. doi: 10.1007/s00441-002-0515-1 12037588
32. Tammaru T, Haukioja E, Capital breeders and income breeders among Lepidoptera: consequences to population dynamics. Oikos. 1996;77: 561–564. doi: 10.2307/3545946
33. Zdybicka-Barabas A, Stączek S, Mak P, Skrzypiec K, Mendyk E, Cytryńska M, Synergistic action of Galleria mellonella apolipophorin III and lysozyme against Gram-negative bacteria. Biochim Biophys Acta. 2013;1828: 1449–56. doi: 10.1016/j.bbamem.2013.02.004 23419829
34. Kawamoto S, Shima J, Sato R, Eguchi T, Ohmomo S, Shibato J, et al. Biochemical and Genetic Characterization of Mundticin KS, an Antilisterial Peptide Produced by Enterococcus mundtii NFRI 7393. Appl Env Microbiol. 2002; 68: 3830–3840. doi: 10.1128/AEM.68.8.3830
35. Ebert D, The Epidemiology and Evolution of Symbionts with Mixed-Mode Transmission. Annu Rev Ecol Evol Syst. 2013; 44: 623–643. doi: 10.1146/annurev-ecolsys-032513-100555
36. Koch H, Schmid-Hempel P, Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci U S A. 2011; 108: 19288–92. doi: 10.1073/pnas.1110474108 22084077
37. 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 25242028
38. Stoll S, Feldhaar H, Fraunholz MJ, Gross R, Bacteriocyte dynamics during development of a holometabolous insect, the carpenter ant Camponotus floridanus. BMC Microbiol. 2010; 10: 308. doi: 10.1186/1471-2180-10-308 21122115
39. Nicholson D, Ross A, Mayhew P, Fossil evidence for key innovations in the evolution of insect diversity. Proc R Soc B Biol Sci. 2014; 281: 1783. Available: http://rspb.royalsocietypublishing.org/content/281/1793/20141823.short
40. Arendt J, Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol. 1997; 72: 149–177.
41. Godfray H, Parasitoids: behavioral and evolutionary ecology. Princeton University Press; 1994.
42. Lazzaro BP, Rolff J, Danger, microbes, and homeostasis. Science. 2011; 332: 43–44. doi: 10.1126/science.1200486 21454776
43. Fedhila S, Buisson C, Dussurget O, Serror P, Glomski IJ, Liehl P, et al. Comparative analysis of the virulence of invertebrate and mammalian pathogenic bacteria in the oral insect infection model Galleria mellonella. J Invertebr Pathol. 2010; 103: 24–29. doi: 10.1016/j.jip.2009.09.005 19800349
44. Dunny GM, Lee LN, LeBlanc DJ, Improved electroporation and cloning vector system for gram-positive bacteria. Appl Environ Microbiol. 1991; 57: 1194–201. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=182867&tool=pmcentrez&rendertype=abstract 1905518
45. Hébert L, Courtin P, Torelli R, Sanguinetti M, Chapot-Chartier MP, Auffray Y, et al. Enterococcus faecalis constitutes an unusual bacterial model in lysozyme resistance. Infect Immun. 2007; 75: 5390–5398. doi: 10.1128/IAI.00571-07 17785473
46. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith J a, et al. Current Protocols in Molecular Biology. Molecular Biology. 2003.
47. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nature methods. 2010; 7: 335–336. doi: 10.1038/nmeth.f.303 20383131
48. Edgar RC, Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010; 26: 2460–2461. doi: 10.1093/bioinformatics/btq461 20709691
49. Hermann-Bank ML, Skovgaard K, Stockmarr A, Larsen N, Mølbak L, The gut microbiotassay: a high-throughput qPCR approach combinable with next generation sequencing to study gut microbial diversity. BMC Genomics. 2013;14: 788. doi: 10.1186/1471-2164-14-788 24225361
50. Arboleya S, Binetti A, Salazar N, Fernández N, Solís G, Hernández-Barranco A, et al. Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiol Ecol. 2012; 79: 763–772. doi: 10.1111/j.1574-6941.2011.01261.x 22126419
51. Simon D, Chopin A, Construction of a vector plasmid family and its use for molecular cloning in Streptococcus lactis. Biochimie. 1988; 0: 559–66. Available: http://www.ncbi.nlm.nih.gov/pubmed/2844302 2844302
52. Kühn A, Piepho H, Über hormonale Wirkungen bei der Verpuppung der Schmetterlinge. Nachrichten von der Gesellschaft der Wissenschaften zu Göttingen. 1936; 2: 141–154.
53. Ellis JD, Graham JR, Mortensen A, Standard methods for wax moth research. J Api Res. 2013; 52: 1–18. doi: 10.3896/IBRA.1.52.1.10
54. Vogel H, Altincicek B, Glöckner G, Vilcinskas A, A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics. 2011; 12: 308. doi: 10.1186/1471-2164-12-308 21663692
55. Wojda I, Jakubowicz T, Humoral immune response upon mild heat-shock conditions in Galleria mellonella larvae. J Insect Physiol. 2007; 53: 1134–1144. doi: 10.1016/j.jinsphys.2007.06.003 17631308
56. Therneau T, A Package for Survival Analysis in S. R package version 2.37–7 [Internet]. Survival. 2014. Available: http://cran.r-project.org/package=survival