Acquisition and structuring of midgut bacterial communities in gypsy moth (Lepidoptera: Erebidae) larvae

Environmental Entomology

Volumn 43, Issue 3, 2014, Pages 595-604

  Mason, Charles J ^a   Raffa, Kenneth F ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Bacteria; Community; Midgut; Plant insect interaction; Pyrosequencing

Indexed keywords

BACTERIUM; BIOLOGICAL CONTROL; COLONIZATION; COMMUNITY STRUCTURE; HOST PLANT; LARVA; MICROBIAL COMMUNITY; MOTH; PLANT-INSECT INTERACTION; SPECIES DIVERSITY;

RNA 16S;

ANIMAL; BACTERIA; BACTERIAL GENE; BACTERIAL PHENOMENA AND FUNCTIONS; DIET; DNA SEQUENCE; GASTROINTESTINAL TRACT; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; LARVA; MICROBIOLOGY; MICROFLORA; MOLECULAR GENETICS; MOTH; OOCYTE; POLYMERASE CHAIN REACTION;

ANIMALS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; DIET; GASTROINTESTINAL TRACT; GENES, BACTERIAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; LARVA; MICROBIOTA; MOLECULAR SEQUENCE DATA; MOTHS; OVUM; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84901928765     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/EN14031     Document Type: Article

References (67)

1. Aksoy, S., X. Chen, and V. Hypsa. 1997. Phylogeny and potential transmission routes of midgut-Associated endosymbionts of tsetse (Diptera:Glossinidae). Insect Mol. Biol. 6: 183-190
2. Anderson, K. E., J. A. Russell, C. S. Moreau, S. Kautz, K. E. Sullam, Y. Hu, U. Basinger, B. M. Mott, N. Buck, and D. E. Wheeler. 2012. Highly similar microbial communities are shared among related and trophically similar ant species. Mol. Ecol. 21: 2282-2296
3. Appel, H. M., and L. W. Maines. 1995. The inßuence of host plant on gut conditions of gypsy moth (Lymantria dispar) caterpillars. J. Insect Physiol. 41: 241-246
4. Bando, H., K. Okado, W. M. Guelbeogo, A. Badolo, H. Aonuma, B. Nelson, S. Fukumoto, X. Xuan, N. Sagnon, and H. Kanuka. 2013. Intra-specific diversity of Serratia marcescens in Anopheles mosquito midgut defines Plasmodium transmission capacity. Sci. Rep. 3: 1-8
5. Bansal, R., S. Hulbert, B. Schemerhorn, J. C. Reese, R. J. Whitworth, J. J. Stuart, and M.-S. Chen. 2011. Hessian ßy-Associated bacteria: Transmission, essentiality, and composition. PLoS ONE 6: E23170
6. Baumann, P. 2005. Biology bacteriocyte-Associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59: 155-189
7. Belda, E., L. Pedrola, J. Peretó, J. F. Marti'nez-Blanch, A. Montagud, E. Navarro, J. Urchuegui'a, D. Ramó n, A. Moya, and M. Porcar. 2011. Microbial diversity in the midguts of field and lab-reared populations of the European corn borer Ostrinia nubilalis. PLoS ONE 6: E21751
8. Blum, J. E., C. N. Fischer, J. Miles, and J. Handelsman. 2013. Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster. MBio 4: E00860-13
9. Boissière, A., M. T. Tchioffo, D. Bachar, L. Abate, A. Marie, S. E. Nsango, H. R. Shahbazkia, P. H. Awono-Ambene, E. A Levashina, R. Christen, et al. 2012. Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathog. 8: E1002742
10. Broderick, N. A., and B. Lemaitre. 2012. Gut-Associated microbes of Drosophila melanogaster. Gut Microbes 3: 307-321
11. Broderick, N. A, K. F. Raffa, and J. Handelsman. 2006. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc. Natl. Acad. Sci. U.S.A. 103: 15196-15199
12. Broderick, N. A., K. F. Raffa, R. M. Goodman, and J. Handelsman. 2004. Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl. Environ. Microbiol. 70: 293-300
13. Brucker, R. M., and S. R. Bordenstein. 2012. The roles of host evolutionary relationships (genus: Nasonia) and development in structuring microbial communities. Evolution 66: 349-362
14. Buchon, N., N. A. Broderick, and B. Lemaitre. 2013. Gut homeostasis in a microbial world: Insights from Drosophila melanogaster. Nat. Rev. Microbiol. 11: 615-626
15. Chao, A. 1984. Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 11: 265-270
16. Clark, T. M. 1999. Evolution and adaptive significance of larval midgut alkalization in the insect superorder Mecopterida. J. Chem. Ecol. 25: 1945-1960
17. Colman, D. R., E. C. Toolson, and C. D. Takacs-Vesbach. 2012. Do diet and taxonomy inßuence insect gut bacterial communities?. Mol. Ecol. 21: 5124-5137
18. Dematheis, F., U Zimmerling, C. Flocco, B. Kurtz, S. Vidal, S. Kropf, and K. Smalla. 2012. Multitrophic interaction in the rhizosphere of maize: Root feeding of western corn rootworm larvae alters the microbial community composition., PLoS ONE 7: E37288
19. Dillon, R. J., and V. M. Dillon. 2004. The gut bacteria of insects: Nonpathogenic interactions. Annu. Rev. Entomol. 49: 71-92
20. Dillon, R. J., C. T. Vennard, A. Buckling, and A. K. Charnley. 2005. Diversity of locust gut bacteria protects against pathogen invasion. Ecol. Lett. 8: 1291-1298
21. Edgar, R. C., B. J. Haas, J. C. Clemente, C. Quince, and R. Knight. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200
22. Engel, P., and N. A. Moran. 2013. The gut microbiota of insects -diversity in structure and function. FEMS Microbiol. Rev. 37: 699-735
23. Fukatsu, T., and T. Hosokawa. 2002. Capsule-Transmitted gut symbiotic bacterium of the Japanese comon plataspid stinkbug, Megacopta punctatissim. Appl. Environ. Microbiol. 62: 389-396
24. Fukatsu, T., N. Nikoh, and R. Kawai. 2000. The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta: Homoptera).Appl. Enviorn. Microbiol. 66: 2748-2758
25. Priya, N. G., A. Ojha, M. K. Kajla, A. Raj, and R. Rajagopal. 2012. Host plant induced variation in gut bacteria of Helicoverpa armigera. PLoS ONE 7: E30768
26. Geib, S. M., M.D.M. Jimenez-Gasco, J. E. Carlson, and K. Hoover. 2009a. Effect of host plant tree species on cellulase activity and bacterial community composition in the gut of larval Asian longhorned beetle. Environ. Entomol. 38: 686-699
27. Geib, S. M., M.D.M. Jimenez-Gasco, J. E. Carlson, M. Tien, R. Jabbour, and K. Hoover. 2009b. Microbial community profiling to investigate transmission of bacteria between life stages of the wood-boring beetle, Anoplophora glabripennis. Microb. Ecol. 58: 199-211
28. Good, I. J. 1953. The population frequencies of species and estimation of population parameters. Biometrika 40: 237-264
29. Hammer, T. J., W. O. McMillan, and N. Fierer. 2014. Metamorphosis of a butterßy-Associated bacterial community. PLoS ONE 9: E86995
30. Hanshew, A. S., C. J. Mason, K. F. Raffa, and C. R. Currie. 2013. Minimization of chloroplast contamination in 16S rRNA gene pyrosequencing of insect herbivore bacterial communities. J. Microbiol. Methods 95: 149-155
31. Hosokawa, T., M. Hironaka, H. Mukai, K. Inadomi, N. Suzuki, and T. Fukatsu. 2012. Mothers never miss the moment: A fine-Tuned mechanism for vertical symbiont transmission in a subsocial insect. Anim. Behav. 83: 293-300
32. Ikeda, S., T. Kaneko, T. Okubo, L.E.E. Rallos, S. Eda, H. Mitsui, S. Sato, Y. Nakamura, S. Tabata, and K. Minamisawa. 2009. Development of a bacterial cell enrichment method and its application to the community analysis in soybean stems. Microb. Ecol. 58: 703-714
33. Johnson, K., and V. Barbehenn. 2000. Oxygen levels in the gut lumens of herbivorous insects. J. Insect Physiol. 46: 897-903
34. Jones, R. T., L. G. Sanchez, and N. Fierer. 2013. A crosstaxon analysis of insect-Associated bacterial diversity. PLoS ONE 8: E61218
35. Kaltenpoth, M., S. A Winter, and A. Kleinhammer. 2009. Localization and transmission route of Coriobacterium glomerans, the endosymbiont of pyrrhocorid bugs. FEMS Microbiol. Ecol. 69: 373-383
36. Kautz, S., B.E.R. Rubin, J. A. Russell, and C. S. Moreau. 2013. Surveying the microbiome of ants: Comparing 454 pyrosequencing with traditional methods to uncover bacterial diversity. Appl. Environ. Microbiol. 79: 525-534
37. Kikuchi, Y., T. Hosokawa, and T. Fukatsu. 2007. Insect-microbe mutualism without vertical transmission: A stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl. Environ. Microbiol. 73: 4308-4316
38. Kikuchi, Y., T. Hosokawa, and T. Fukatsu. 2011a. Anancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J. 5: 446-460
39. Kikuchi, Y., T. Hosokawa, and T. Fukatsu. 2011b. Specific developmental window for establishment of an insectmicrobe gut symbiosis. Appl. Environ. Microbiol. 77: 4075-4081
40. Koch, H., and P. Schmid-Hempel. 2011. Bacterial communities in central European bumblebees: Low diversity and high specificity. Microb. Ecol. 62: 121-133
41. Kohl, K. D., and M. D. Dearing. 2012. Experience matters: Prior exposure to plant toxins enhances diversity of gut microbes in herbivores. Ecol. Lett. 15: 1008-1015
42. Kö hler, T., C. Dietrich, R. H. Scheffrahn, and A. Brune. 2012. High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher termites (Nasutitermes spp.). Appl. Environ. Microbiol. 78: 4691-4701
43. Lauber, C. L., M. Hamady, R. Knight, and N. Fierer. 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 75: 5111-5120
44. Lauzon, C. R., S.D.M.C. Combs, and S. E. Potter. 2009. Establishment and vertical passage of Enterobacter (Pantoea) agglomerans and Klebsiella pneumoniae through all life stages of the Mediterranean fruit ßy (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 102: 85-95
45. Leonard, D. E. 1970. Intrinsic factors causing qualitative changes in populations of Porthetria dispar (Lepidoptera: Lymantriidae). Can. Entomol. 102: 239-249
46. Liebhold, A. M., K. W. Gottschalk, R. M. Muzika, M. E. Montgomery, R. Young, K. O'Day, and B. Kelley. 1995. Suitability of North American tree species to the gypsy moth: A summary of field and laboratory tests. U.S. Department of Agriculture Forest Service NE Forest Experimental Station General Technical Bulletin NE-211. U.S. Department of Agriculture, Washington, DC.
47. Lundgren, J. G., and R. M. Lehman. 2010. Bacterial gut symbionts contribute to seed digestion in an omnivorous beetle. PLoS ONE 5: E10831
48. Minkley, N., A. Fujita, A. Brune, and W. H. Kirchner. 2006. Nest specificity of the bacterial community in termite guts (Hodotermes mossambicus). Insectes Soc. 53: 339-344
49. Moran, N. A, A. K. Hansen, J. E. Powell, and Z. L. Sabree. 2012. Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS ONE 7: E36393
50. Pinto-Tomás, A.A.A., A. Sittenfeld, L. Uribe-lorío, M. Mora, D. H. Janzen, R. M. Goodman, M. Holly, and H. M. Simon. 2011. Comparison of midgut bacterial diversity in tropical caterpillars (Lepidoptera: Saturniidae) fed on Different diets. Environ. Entomol. 40: 1111-1122
51. Rani, A., A Sharma, R. Rajagopal, T. Adak, and R. K. Bhatnagar. 2009. Bacterial diversity analysis of larvae and adult midgut microßora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi-An Asian malarial vector.BMC Microbiol. 9: 96
52. Rawls, J. F., M. A Mahowald, R. E. Ley, and J. I. Gordon. 2006. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127: 423-433
53. Robinson, C. J., B.J.M. Bohannan, and V. B. Young. 2010. From structure to function: The ecology of host-Associated microbial communities. Microbiol. Mol. Biol. Rev. 74: 453-476
54. Russell, J. A., S. Weldon, A. H. Smith, K. L. Kim, Y. Hu, P. Lukasik, S. Doll, I. Anastopoulos, M. Novin, and K. M. Oliver. 2013. Uncovering symbiont-driven genetic diversity across North American pea aphids. Mol. Ecol. 22: 2045-2059
55. Schloss, P. D., S. L. Westcott, T. Ryabin, J. R. Hall, M. Hartmann, E. B. Hollister, R.ALesniewski, B. B. Oakley, D. H. Parks, C. J. Robinson, et al. 2009. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75: 7537-7541
56. Schloss, P. D., D. Gevers, and S. L. Westcott. 2011. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS ONE 6: E27310
57. Schultz, J. C., and M. J. Lechowicz. 1986. Hostplant, larval age, and feeding behavior inßuence midgut pH in gypsy moth (Lymantria dispar). Oecologia 71: 133-137
58. Shrestha, P. M., M. Kube, R. Reinhardt, and W. Liesack. 2009. Transcriptional activity of paddy soil bacterial communities. Environ. Microbiol. 11: 960-970
59. Su, Z., M. Zhang, X. Liu, L. Tong, Y. Huang, G. Li, and Y. Pang. 2010. Comparison of bacterial diversity in wheat bran and in the gut of larvae and newly emerged adult of Musca domestica (Diptera: Muscidae) by use of ethidium monoazide reveals bacterial colonization. J. Econ. Entomol. 103: 1832-1841
60. Sudakaran, S., H. Salem, C. Kost, and M. Kaltenpoth. 2012. Geographical and ecological stability of the symbiotic mid-gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae). Mol. Ecol. 21: 6134-6151
61. Tang, X., D. Freitak, H. Vogel, L. Ping, Y. Shao, E. A. Cordero, G. Andersen, M. Westermann, D. G. Heckel, and W. Boland. 2012. Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. PLoS ONE 7: E36978
62. von Dohlen, C. D., U. Spaulding, K. Shields, N. P. Havill, C. Rosa, and K. Hoover. 2013. Diversity of proteobacterial endosymbionts in hemlock woolly adelgid (Adelges tsugae) (Hemiptera: Adelgidae) from its native and introduced range. Environ. Microbiol. 15: 2043-2062
63. Wong, A.C.-N., P. Ng, and A. E. Douglas. 2011. Low-diversity bacerial community in the gut of the fruitßy Drosophila melanogaster. Environ. Microbiol. 13: 1889-1900
64. Wong, A.C.-N., J. M. Chaston, and A. E. Douglas. 2013. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J. 7: 1922-1932
65. Woodbury, N., M. Moore, and G. Gries. 2013. Horizontal transmission of the microbial symbionts Enterobacter cloacae and Mycotypha microspora to their firebrat host. Entomol. Exp. Appl. 147: 160-166
66. Xiang, H., G. Wei, S. Jia, J. Huang, X. Miao, Z. Zhou, L. Zhao, and Y. Huang. 2006. Microbial communities in the larval midgut of laboratory and field populations of cotton bollworm (Helicoverpa armigera). 1092: 1085-1092
67. Yue, J. C., and M. K. Clayton. 2005. A similarity measure based on species proportions. Commun. Stat. Theory Methods 34: 2123-2131.