The effect of feeding Bt MON810 maize to pigs for 110 days on intestinal microbiota

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Buzoianu, Stefan G ^a,b   Walsh, Maria C ^a   Rea, Mary C ^c,d   O'Sullivan, Orla ^c   Crispie, Fiona ^c,d   Cotter, Paul D ^c,d   Ross, R Paul ^c,d   Gardiner, Gillian E ^b   Lawlor, Peadar G ^a  

^a ANIMAL AND GRASSLAND RESEARCH AND INNOVATION CENTRE   (Ireland)

^b Ireland   (Ireland)

^c TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^d UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ENROFLOXACIN; RNA 16S;

ANAEROBE; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COUNT; CONTROLLED STUDY; DIARRHEA; DIET; ENTEROBACTERIACEAE; EXPERIMENTAL PIG; FECES ANALYSIS; FEEDING; FOOD ANALYSIS; FOOD COMPOSITION; GENE SEQUENCE; HIGH THROUGHPUT SEQUENCING; INTESTINE FLORA; LACTOBACILLUS; MAIZE; MALE; NONHUMAN; PROTEIN CONTENT; TAXONOMY; ANIMAL; ANIMAL FOOD; BACILLUS THURINGIENSIS; CECUM; GENETICALLY MODIFIED FOOD; GENETICS; INTESTINE; METAGENOME; MICROBIOLOGY; SWINE; TIME; TRANSGENIC PLANT;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; HOLDEMANIA; LACTOBACILLUS; SUIDAE; SUS; ZEA MAYS;

ANIMAL FEED; ANIMALS; BACILLUS THURINGIENSIS; CECUM; FOOD, GENETICALLY MODIFIED; INTESTINES; MALE; METAGENOME; PLANTS, GENETICALLY MODIFIED; SWINE; TIME FACTORS; ZEA MAYS;

EID: 84860520983     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033668     Document Type: Article

References (56)

1. Cani PD, Delzenne NM, (2009) Interplay between obesity and associated metabolic disorders: new insights into the gut microbiota. Curr Opin Pharmacol 9: 737-743.
2. Sekirov I, Russell SL, Antunes LC, Finlay BB, (2010) Gut microbiota in health and disease. Physiol Rev 90: 859-904.
3. Vrieze A, Holleman F, Zoetendal E, de Vos W, Hoekstra J, et al. (2010) The environment within: how gut microbiota may influence metabolism and body composition. Diabetologia 53: 606-613.
4. Buddington RK, Sangild PT, (2011) Companion Animals Symposium: Development of the mammalian gastrointestinal tract, the resident microbiota, and the role of diet in early life. J Anim Sci 89: 1506-1519.
5. Saarela M, Lähteenmäki L, Crittenden R, Salminen S, Mattila-Sandholm T, (2002) Gut bacteria and health foods-the European perspective. Int J Food Microbiol 78: 99-117.
6. Gaskell G, (2005) Europeans and biotechnology in 2005: patterns and trends. A report to the European Commission's Directorate-General for Research.
7. Martinez-Poveda A, Molla-Bauza MB, del Campo Gomis FJ, Martinez LM-C, (2009) Consumer-perceived risk model for the introduction of genetically modified food in Spain. Food Policy 34: 519-528.
8. Rollin F, Kennedy J, Wills J, (2011) Consumers and new food technologies. Trends Food Sci Technol 22: 99-111.
9. EFSA, (2009) Scientific opinion of the panel on genetically modified organisms on applications (EFSA-GMO-RX-MON810) for the renewal of authorisation for the continued marketing of (1) existing food and food ingredients produced from genetically modified insect resistant maize MON810; (2) feed consisting of and/or containing maize MON810, including the use of seed for cultivation; and of (3) food and feed additives, and feed materials produced from maize MON810, all under Regulation (EC) No 1829/2003 from Monsanto The EFSA Journal 1149: 1-85.
10. Finamore A, Roselli M, Britti S, Monastra G, Ambra R, et al. (2008) Intestinal and peripheral immune response to MON810 maize ingestion in weaning and old mice. J Agric Food Chem 56: 11533-11539.
11. Domingo JL, Giné Bordonaba J, (2011) A literature review on the safety assessment of genetically modified plants. Environ Int 37: 734-742.
12. Yudina TG, Brioukhanov AL, Zalunin IA, Revina LP, Shestakov AI, et al. (2007) Antimicrobial activity of different proteins and their fragments from Bacillus thuringiensis parasporal crystals against clostridia and archaea. Anaerobe 13: 6-13.
13. Koskella J, Stotzky G, (2002) Larvicidal toxins from Bacillus thuringiensis subspp. kurstaki, morrisoni (strain tenebrionis), and israelensis have no microbicidal or microbiostatic activity against selected bacteria, fungi, and algae in vitro. Can J Microbiol 48: 262-267.
14. Buzoianu SG, Walsh MC, Rea MC, O'Sullivan O, Cotter PD, et al. (2012) High throughput sequence-based analysis of the intestinal microbiota of weanling pigs fed genetically modified Bt MON810 maize for 31 days. Appl Environ Microbiol, in press.
15. Einspanier R, Lutz B, Rief S, Berezina O, Zverlov V, et al. (2004) Tracing residual recombinant feed molecules during digestion and rumen bacterial diversity in cattle fed transgene maize. Eur Food Res Technol 218: 269-273.
16. Wiedemann S, Gurtler P, Albrecht C, (2007) Effect of feeding cows genetically modified maize on the bacterial community in the bovine rumen. Appl Environ Microbiol 73: 8012-8017.
17. Trabalza-Marinucci M, Brandi G, Rondini C, Avellini L, Giammarini C, et al. (2008) A three-year longitudinal study on the effects of a diet containing genetically modified Bt176 maize on the health status and performance of sheep. Livest Sci 113: 178-190.
18. Moughan PJ, Birtles MJ, Cranwell PD, Smith WC, Pedraza M, (1992) The piglet as a model animal for studying aspects of digestion and absorption in milk-fed human infants. World Rev Nutr Diet 67: 40-113.
19. Rothberg JM, Leamon JH, (2008) The development and impact of 454 sequencing. Nat Biotech 26: 1117-1124.
20. Tringe SG, Hugenholtz P, (2008) A renaissance for the pioneering 16 S rRNA gene. Curr Opin Microbiol 11: 442-446.
21. Buzoianu SG, Walsh MC, Rea MC, Cassidy JP, Ross RP, et al. (2012) Effect of feeding genetically modified Bt MON810 maize to ~40 day old pigs for 110 days on growth and health indicators. Animal doi:10.1017/S1751731112000249.
22. Walsh MC, Buzoianu SG, Gardiner GE, Cassidy JP, Rea MC, et al. (2012) Effects of short-term feeding of Bt MON810 maize on growth performance, organ morphology and function in pigs. Br J Nutr 107: 364-371.
23. OECD, (2002) Consensus document on compositional considerations for new varieties of maize (Zea Mays): key food and feed nutrients, anti-nutrients and secondary plant metabolites.
24. ILSI, (2010) International Life Sciences Institute Crop Composition Database, Version 4.2.www.cropcomposition.org.
25. Krause DO, Easter RA, White BA, Mackie RI, (1995) Effect of weaning diet on the ecology of adherent lactobacilli in the gastrointestinal tract of the pig. J Anim Sci 73: 2347-2354.
26. EFSA, (2008) Safety and nutritional assessment of GM plants and derived food and feed: The role of animal feeding trials. Food Chem Toxicol 46: S2-S70.
27. Castillo M, Martín-Orúe SM, Anguita M, Pérez JF, Gasa J, (2007) Adaptation of gut microbiota to corn physical structure and different types of dietary fibre. Livest Sci 109: 149-152.
28. Dona A, Arvanitoyannis IS, (2009) Health risks of genetically modified foods. Crit Rev Food Sci Nutr 49: 164-175.
29. Cummings JH, Macfarlane GT, (1991) The control and consequences of bacterial fermentation in the human colon. J Appl Microbiol 70: 443-459.
30. Schrøder M, Poulsen M, Wilcks A, Kroghsbo S, Miller A, et al. (2007) A 90-day safety study of genetically modified rice expressing Cry1Ab protein (Bacillus thuringiensis toxin) in Wistar rats. Food Chem Toxicol 45: 339-349.
31. Naito S, Hayashidani H, Kaneko K, Ogawa M, Benno Y, (1995) Development of intestinal lactobacilli in normal piglets. J Appl Bacteriol 79: 230-236.
32. Walter J, (2008) Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl Environ Microbiol 74: 4985-4996.
33. Gardiner GE, Casey PG, Casey G, Lynch PB, Lawlor PG, et al. (2004) Relative ability of orally administered Lactobacillus murinus to predominate and persist in the porcine gastrointestinal tract. Appl Environ Microbiol 70: 1895-1906.
34. Poletto R, Rostagno MH, Richert BT, Marchant-Forde JN, (2009) Effects of a "step-up" ractopamine feeding program, sex, and social rank on growth performance, hoof lesions, and Enterobacteriaceae shedding in finishing pigs. J Anim Sci 87: 304-313.
35. Jensen BB, Jorgensen H, (1994) Effect of dietary fiber on microbial activity and microbial gas production in various regions of the gastrointestinal tract of pigs. Appl Environ Microbiol 60: 1897-1904.
36. Franklin MA, Mathew AG, Vickers JR, Clift RA, (2002) Characterization of microbial populations and volatile fatty acid concentrations in the jejunum, ileum, and cecum of pigs weaned at 17 vs 24 days of age. J Anim Sci 80: 2904-2910.
37. Canibe N, Højberg O, Højsgaard S, Jensen BB, (2005) Feed physical form and formic acid addition to the feed affect the gastrointestinal ecology and growth performance of growing pigs. J Anim Sci 83: 1287-1302.
38. Poroyko V, White JR, Wang M, Donovan S, Alverdy J, et al. (2010) Gut microbial gene expression in mother-fed and formula-fed piglets. PLoS ONE 5: e12459.
39. Vahjen W, Pieper R, Zentek J, (2010) Bar-coded pyrosequencing of 16 S rRNA gene amplicons reveals changes in ileal porcine bacterial communities due to high dietary zinc intake. Appl Environ Microbiol 76: 6689-6691.
40. Kim HB, Borewicz K, White BA, Singer RS, Sreevatsan S, et al. (2011) Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs. Vet Microbiol 153: 124-133.
41. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, et al. (2005) Diversity of the human intestinal microbial flora. Science 308: 1635-1638.
42. Flint HJ, Duncan SH, Scott KP, Louis P, (2007) Interactions and competition within the microbial community of the human colon: links between diet and health. Environ Microbiol 9: 1101-1111.
43. Armougom F, Henry M, Vialettes B, Raccah D, Raoult D, (2009) Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and methanogens in anorexic patients. PLoS ONE 4: e7125.
44. Larsen N, Vogensen FK, van den Berg FWJ, Nielsen DS, Andreasen AS, et al. (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE 5: e9085.
45. Leser TD, Amenuvor JZ, Jensen TK, Lindecrona RH, Boye M, et al. (2002) Culture independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 68: 673-690.
46. Chassard C, Scott KP, Marquet P, Martin JC, Del'homme C, et al. (2008) Assessment of metabolic diversity within the intestinal microbiota from healthy humans using combined molecular and cultural approaches. FEMS Microbiol Ecol 66: 496-504.
47. Gosalbes MJ, Durbán A, Pignatelli M, Abellan JJ, Jiménez-Hernández N, et al. (2011) Metatranscriptomic approach to analyze the functional human gut microbiota. PLoS ONE 6: e17447.
48. Agans R, Rigsbee L, Kenche H, Michail S, Khamis HJ, et al. (2011) Distal gut microbiota of adolescent children is different from that of adults. FEMS Microbiol Ecol 77: 404-412.
49. Hartnell GF, Cromwell GL, Dana GR, Lewis AJ, Baker DH, et al. (2007) Best practices for the conduct of animal studies to evaluate crops genetically modified for output traits; ILSI, editor. Washington, DC, USA.
50. NRC, (1998) Nutrient requirements of swine. Washington, DC, USA National Academy of Sciences.
51. Rea MC, Clayton E, O'Connor PM, Shanahan F, Kiely B, et al. (2007) Antimicrobial activity of lacticin 3147 against clinical Clostridium difficile strains. J Med Microbiol 56: 940-946.
52. Rantakokko-Jalava K, Jalava J, (2002) Optimal DNA isolation method for detection of bacteria in clinical specimens by broad-range PCR. J Clin Microbiol 40: 4211-4217.
53. Murphy EF, Cotter PD, Healy S, Marques TM, O'Sullivan O, et al. (2010) Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut 59: 1635-1642.
54. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
55. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, 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. 22 SAS/STAT®9, (2010) User's Guide. Cary, NC, USA SAS Institute Inc.