Bacterial community structures in honeybee intestines and their response to two insecticidal proteins

FEMS Microbiology Ecology

Volumn 59, Issue 3, 2007, Pages 600-610

  Babendreier, Dirk ^a   Joller, David ^a   Romeis, Jörg ^a   Bigler, Franz ^a   Widmer, Franco ^a  

^a AGROSCOPE RECKENHOLZ TÄNIKON RESEARCH STATION ART   (Switzerland)

Author keywords

Apis mellifera; Bacteria; Bt maize; Risk assessment; T RFLP; Transgenic plants

Indexed keywords

BACTERIAL RNA; BEE VENOM; CRY1AB TOXIN; DNA FRAGMENT; INSECTICIDE; PROTEIN; RNA 16S; SOYBEAN TRYPSIN INHIBITOR; UNCLASSIFIED DRUG;

BACTERIUM; BIOINDICATOR; BIOPESTICIDE; COMMENSAL; COMMUNITY STRUCTURE; DIGESTIVE SYSTEM; HONEYBEE; INHIBITOR; MAIZE; MICROBIAL COMMUNITY; PHYSIOLOGICAL RESPONSE; PROTEIN; RISK ASSESSMENT; RNA; SUBLETHAL EFFECT; TOXIN; TRANSGENIC PLANT;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL FLORA; BACTERIAL GENE; BETAPROTEOBACTERIA; CONCENTRATION (PARAMETERS); FIRMICUTES; FLYING; GAMMAPROTEOBACTERIA; GENE AMPLIFICATION; GENETIC ANALYSIS; HONEYBEE; INTESTINE; INTESTINE FLORA; INTESTINE FUNCTION; LABORATORY; MAIZE; MIDGUT; MORTALITY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLLEN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; STATISTICAL SIGNIFICANCE; SWITZERLAND;

ANIMALS; BACTERIA; BACTERIAL TOXINS; BEES; INTESTINES; PLANTS, GENETICALLY MODIFIED; POLLEN; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RISK ASSESSMENT; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SOYBEAN PROTEINS; SWITZERLAND; TRYPSIN INHIBITORS; ZEA MAYS;

CENTRAL EUROPE; EURASIA; EUROPE; SWITZERLAND;

APIS MELLIFERA; APOIDEA; BACTERIA (MICROORGANISMS); FIRMICUTES; GAMMAPROTEOBACTERIA; GLYCINE MAX; ZEA MAYS;

EID: 33847748265     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2006.00249.x     Document Type: Article

References (41)

1. Alippi AM, Lopez AC & Aguilar OM (2002) Differentiation of Paenibacillus larvae subsp. larvae, the cause of American foulbrood of honeybees, by using PCR and Restriction Fragment Analysis of genes encoding 16 s rRNA. Appl Environ Microbiol 68: 3655-3660.
2. Amann RI, Ludwig W & Schleifer KH (1995) Phylogenetic identification and in-situ detection of individual microbialcells without cultivation. Microb Rev 59: 143-169.
3. Babendreier D, Kalberer N, Romeis J, Fluri P, Mulligan E & Bigler F (2005) Influence of transgenic Bt-Pollen, Bt-Toxin and Proteinase Inhibitor (SBTI) ingestion on development of the hypopharyngeal gland in honeybees. Apidologie 36: 585-594.
4. Bürgmann H, Pesaro M, Widmer F & Zeyer J (2001) A strategy for optimizing quality and quantity of DNA extracted from soil. J Microbiol Methods 45: 7-20.
5. Burgess EPJ, Malone LA & Christeller JT (1996) Effects of two proteinase inhibitors on the digestive enzymes and survival of honey bees (Apis mellifera). J Insect Physiol 42: 823-828.
6. Cole JR, Chai B, Marsh TL et al. (2003) The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31: 442-443.
7. Conner AJ, Glare TR & Nap JP (2003) The release of genetically modified crops into the environment - part II. Overview of ecological risk assessment. Plant J 33: 19-46.
8. Deml R, Meise M & Dettner K (1999) Effects of Bacillus thuringiensis delta-endotoxins on food utilization, growth, and survival of selected phytophagous insects. J Appl Entomol 123: 55-64.
9. Dillon RJV & Dillon M (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49: 71-92.
10. EPPO (2001) Revised draft of EPPO Guidelines PP 1/170: guidelines for the efficacy evaluation of plant protection products: side effects on honey bees. Appendix I. Hazards of Pesticides to Bees (Belzunces LP, Pélissier C & Lewis GB, eds), pp. 279-286. Les Colloques de l'INRA 98, INRA, Paris.
11. Free JB (1993) Insect Pollination of Crops. Academic Press, London.
12. Gilliam M (1979) Microbiology of pollen and beebread: the genus Bacillus. Apidologie 10: 269-274.
13. Gilliam M (1997) Identification and roles of non-pathogenic microflora associated with honey bees. Fems Microbiol Lett 155: 1-10.
14. Gilliam M & Morton HL (1978) Bacteria belonging to genus Bacillus isolated from honey bees, Apis mellifera, fed 2,4-d and antibiotics (1). Apidologie 9: 213-221.
15. Gilliam M & Valentine DK (1976) Bacteria isolated from the intestinal contents of foraging worker honey bees, Apis mellifera: the genus Bacillus. J Invertebr Pathol 28: 275-276.
16. Gilliam M, Lorenz BJ & Richardson GV (1988a) Digestive enzymes and microorganisms in honey bees, Apis mellifera - Influence of Streptomycin, age, season and pollen. Microbios 55: 95-114.
17. Gilliam M, Taber S, Lorenz BJ & Prest DB (1988b) Factors affecting development of chalkbrood disease in colonies of honey bees, Apis mellifera, fed pollen contaminated with Ascosphaera apis. J Invertebr Pathol 52: 314-325.
18. Gilliam M, Buchmann SL, Lorenz BJ & Schmalzel RJ (1990) Bacteria belonging to the genus Bacillus associated with 3 species of solitary bees. Apidologie 21: 99-105.
19. Hails RS (2000) Genetically modified plants - the debate continues. Trends Ecol Evol 15: 14-18.
20. Hall TA (1999) Bio Edit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symp Ser 41: 95-98.
21. Hartmann M, Frey B, Kölliker R & Widmer F (2005) Semi-automated genetic analyses of soil microbial communities: comparison of T-RFLP and RISA based on descriptive and discriminative statistical approaches. J Microbiol Methods 61: 349-360.
22. Heuer H, Krsek M, Baker P, Smalla K & Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gelelectrophoretic separation in denaturing gradients. Appl Environ Microbiol 63: 3233-3241.
23. Hongoh Y, Ohkuma M & Kudo T (2003) Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). Fems Microbiol Ecol 44: 231-242.
24. Jeyaprakash A, Hoy MA & Allsopp MH (2003) Bacterial diversity in worker adults of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) assessed using 16S rRNA sequences. J Invertebr Pathol 84: 96-103.
25. Jouanin L, Bonade-Bottino M, Girard C, Morrot G & Giband M (1998) Transgenic plants for insect resistance. Plant Sci 131: 1-11.
26. Koziel MG et al. (1993) Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. Biotechn 11: 194-200.
27. Laskowski M & Kato L (1980) Protein inhibitors of proteinases. Annu Rev Biochem 49: 593-626.
28. Lawrence PK & Koundal KR (2002) Plant protease inhibitors in control of phytophagous insects. Electr J Biotechnol 5: U122-U138.
29. Malone LA & Pham-Delegue MH (2001) Effects of transgene products on honey bees (Apis mellifera) and bumblebees (Bombus sp.). Apidologie 32: 287-304.
30. Malone LA, Giacon HA, Burgess EPJ, Maxwell JZ, Christeller JT & Laing WA (1995) Toxicity of Trypsin endopeptidase inhibitors to honeybees (Hymenoptera, Apidae). J Econ Entomol 88: 46-50.
31. Malone LA, Todd JH, Burgess EPJ & Christeller JT (2004) Development of hypopharyngeal glands in adult honey bees fed with a Bt toxin, a biotin binding protein and a protease inhibitor. Apidologie 35: 655-664.
32. McManus MT, White DWR & McGregor PG (1994) Accumulation of a chymotrypsin inhibitor in transgenic tobacco can affect the growth of insect pests. Transgenic Research 3: 50-58.
33. Mohr KI & Tebbe CC (2006) Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environ Microbiol 8: 258-272.
34. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR & Dean DH (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Molec Biol Rev 62: 775-806.
35. Shelton AM, Zhao JZ & Roush RT (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annu Rev Entomol 47: 845-881.
36. Sokal RR & Rohlf FJ (1995) Biometry. W.H. Freeman and Company, New York, NY.
37. Tajima K, Arai S, Ogata K, Nagamine T, Matsui H, Namakura M, Aminov RI & Benno Y (2000) Rumen bacterial community transition during adaptation to high-grain diet. Anaerobe 6: 273-284.
38. Ter Braak (1996) Unimodal models to relate species to environment. PhD thesis, Agricultural Mathematics Group-DLO: Wageningen, the Netherlands.
39. Tokura M, Ohkuma M & Kudo T (2000) Molecular phylogeny of methanogens associated with flagellated protists in the gut and with the gut epithelium of termites. Fems Microbiol Ecol 33: 233-240.
40. US EPA (1996) Ecological effects test guidelines OPPTS 850.3020 Honeybee acute contact toxicity test, EPA 712-C-96-147, Washington, DC.
41. Van de Peer Y & Dewachter R (1994) Treecon for Windows - a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Computer Appl Biosci 10: 569-570.