전체메뉴
검색
Article Search

JMB Journal of Microbiolog and Biotechnology

QR Code QR Code

Research article

Environmental Microbiology and Biotechnology (EMB)  |  Environmental Microbiology

Microbial Community of Healthy Thai Vegetarians and Non-Vegetarians, Their Core Gut Microbiota, and Pathogen Risk

Supatjaree Ruengsomwong 1, 2, 3, Orawan La-ongkham 1, Jiahui Jiang 4, Bhusita Wannissorn 3, Jiro Nakayama 4 and Sunee Nitisinprasert 1, 2*

1Specialized Research Unit: Probiotics and Prebiotics for Health, Department of Biotechnology, Faculty of Agro-Industry, Kasetsart University, Chatuchak, Bangkok 10900, Thailand, 2Center for Advanced Studies for Agriculture and Food, Kasetsart University Institute for Advanced Studies, Kasetsart University, Chatuchak, Bangkok 10900, Thailand, 3Bioscience Department, Thailand Institute of Scientific and Technological Research, Technopolis, Pathum Thani 12120, Thailand, 4Laboratory of Microbial Technology, Division of Microbial Science and Technology, Department of Bioscience and Biotechnology, Faculty of Agriculture, Graduate School, Kyushu University, Fukuoka 812-8581, Japan

Received: March 24, 2016; Accepted: July 1, 2016

J. Microbiol. Biotechnol. 2016; 26(10): 1723-1735

Published October 28, 2016 https://doi.org/10.4014/jmb.1603.03057

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Pyrosequencing analysis of intestinal microflora from healthy Thai vegetarians and nonvegetarians exhibited 893 OTUs covering 189 species. The strong species indicators of vegetarians and non-vegetarians were Prevotella copri and Bacteroides vulgatus as well as bacteria close to Escherichia hermanii with % relative abundance of 16.9 and 4.5-4.7, respectively. Core gut microbiota of the vegetarian and non-vegetarian groups consisted of 11 and 20 different bacterial species, respectively, belonging to Actinobacteria, Firmicutes, and Proteobacteria commonly found in both groups. Two species, Faecalibacterium prausnitzii and Gemmiger formicilis, had a prevalence of 100% in both groups. Three species, Clostridium nexile, Eubacterium eligens, and P. copri, showed up in most vegetarians, whereas more diversity of Collinsella aerofaciens, Ruminococcus torques, various species of Bacteroides, Parabacteroides, Escherichia, and different species of Clostridium and Eubacterium were found in most nonvegetarians. Considering the correlation of personal characters, consumption behavior, and microbial groups, the age of non-vegetarians showed a strong positive correlation coefficient of 0.54 (p = 0.001) to Bacteroides uniformis but exhibited a moderate one to Alistipes finegoldii and B. vulgatus. Only a positive moderate correlation of body mass index and Parabacteroides distasonis appeared. Based on the significant abundance of potential pathogens, the microbiota of the non-vegetarian group showed an abundance of potential pathogen varieties of Bilophila wadsworthia, Escherichia coli, and E. hermannii, whereas that of the vegetarian group served for only Klebsiella pneumoniae. These results implied that the microbiota of vegetarians with high abundance of P. copri and low potential pathogen variety would be a way to maintain good health in Thais.

Keywords

fecal microbiota, pyrosequencing, core gut microbiota, Prevotella, pathogen risk, Enterobacteriaceae

References

  1. An QL, Yang XJ, Dong YM, Feng LJ, Kuang BJ, Li J. 2001. Using confocal laser scanning microscope to visualize the infection of rice root by GFP-labelled Klebsiella oxytoca SA2, an endophytic diazotroph. Acta Bot. Sin. 43: 558-564.
  2. Ananthan S, Raju S, Alavandi S. 1999. Enterotoxigenicity of Klebsiella pneumoniae associated with childhood gastroenteritis in Madras, India. Jpn. J. Infect. Dis. 52: 16-17.
    Pubmed
  3. Arumugam M, Raes J, Pelletier E, Paslier DL, Yamada T, Mende DR, et al. 2011. Enterotypes of the human gut microbiome. Nature 473: 174-180.
    Pubmed PMC CrossRef
  4. Bagley ST. 1985. Habitat association of Klebsiella species. Infect. Control 6: 52-56.
    Pubmed CrossRef
  5. Bentley R, Meganathan R. 1982. Biosynthesis of vitamin K (menaquinone) in bacteria. Microbiol. Rev. 46: 241-280.
    Pubmed PMC
  6. Brenner DJ, Davis BR, Steigewalt AG, Riddle CF, McWhorter AC, Allen SD, et al. 1982. Atypical biogroups of Escherichia coli found in clinical specimens and description of Escherichia hermannii sp. nov. J. Clin. Microbiol. 15: 703-713.
    Pubmed PMC
  7. Chelius MK, Triplett EW. 2000. Immunolocalization of dinitrogenase reductase produced by Klebsiella pneumoniae in association with Zea mays L. Appl. Environ. Microbiol. 66:783-787.
    CrossRef
  8. Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, et al. 2012. Gut microbiota composition correlates with diet and health in the elderly. Nature 488: 178-184.
    Pubmed
  9. Clemente JC, Ursell LK, Parfrey LW, Knight R. 2012. The impact of the gut microbiota on human health: an integrative view. Cell 148: 1258-1270.
    Pubmed PMC CrossRef
  10. Crowe FL, Roddam AW, Key TJ, Appleby PN, Overvad K, Jakobsen MU, et al. 2011. Fruit and vegetable intake and mortality from ischaemic heart disease: results from the European Prospective Investigation into Cancer and Nutrition (EPIC)-Heart Study. Eur. Heart J. 465: 1-9.
    CrossRef
  11. Cruz AY, Cazacu AC, Allen CH. 2007. Pantoea agglomerans, a plant pathogen causing human disease. J. Clin. Microbiol. 45: 1989-1992.
    Pubmed PMC CrossRef
  12. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505: 559-563.
    Pubmed PMC CrossRef
  13. De Filippis F, Pellegrini N, Vannini L, Jeffery IB, La Storia A, Laghi L, et al. 2015. High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut DOI:10.1136/gutjnl-2015-309957.5.
  14. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 107:14691-14696.
    Pubmed PMC CrossRef
  15. Dong YM, Chelius MK, Brisse S, Kozyrovska N, Kovtunovych GR, Podschun R, Triplett EW. 2003. Comparison between two Klebsiella: the plant endophyte K. pneumoniaee 342 and a clinical isolate, K. pneumoniaee MGH78578. Symbiosis 35: 247259.
  16. Do e J, Corthier G. 2010. The human intestinal microbiota. Gastroenterol. Clin. Biol. 34: S7-S15.
    CrossRef
  17. Duncan SH, Louis P, Thomson JM, Flint HJ. 2009. The role of pH in determining the species composition of the human colonic microbiota. Environ. Microbiol. 11: 2112-2122.
    Pubmed CrossRef
  18. Gentschew L, Ferguson LR. 2012. Role of nutrition and microbiota in susceptibility to inflammatory bowel diseases. Mol. Nutr. Food Res. 56: 524-535.
    Pubmed CrossRef
  19. Guerrant RL, Moore RA, Kerschfeld PM, Sande MA. 1975. Role of toxigenic and invasive bacteria in acute diarrhea of childhood. N. Engl. J. Med. 293: 567-571.
    Pubmed CrossRef
  20. Hayashi H, Sakamoto M, Benno Y. 2002. Fecal microbial diversity in a strict vegetarian as determined by molecular analysis and cultivation. Microbiol. Immunol. 46: 819-831.
    Pubmed CrossRef
  21. Jain A, Bohra I, Mahajan R, Jain S, Chugh TD. 2012. Pantoea agglomerans infection behaving like a tumor after plant thorn injury: an unusual presentation. Indian J. Pathol. Microbiol. 55: 386-388.
    Pubmed CrossRef
  22. Jeffery IB, O’Toole PW. 2013. Diet-microbiota interactions and their implications for healthy living. Nutrient 5: 234-252.
    Pubmed PMC CrossRef
  23. Kabeerdoss J, Devi RS, Mary RR, Ramakrishna BS. 2012. Faecal microbiota composition in vegetarians: comparison with omnivores in a cohort of young women in southern India. Br. J. Nutr. 108: 953-957.
    Pubmed CrossRef
  24. Kadner RJ. 1978. Repression of synthesis of the vitamin B 12 receptor in Escherichia coli. J. Bacteriol. 136: 1050-1057.
    Pubmed PMC
  25. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2: 123-140.
    Pubmed CrossRef
  26. Kim MS, Hwang SS, Park EJ, Bae JW. 2013. Strict vegetarian diet improves the risk fators associated with metabolic diseases by modulating gut microbiota and reducing intestinal inflammation. Environ. Microbiol. Rep. 5: 765-775.
    Pubmed
  27. Knittel MD, Seidler RJ, Eby C, Cabe LM. 1977. Colonization of the botanical environment by Klebsiella isolates of pathogenic origin. Appl. Environ. Microbiol. 34: 557-563.
    Pubmed PMC
  28. Ladha JK, Barraquio WL, Watanabe I. 1983. Isolation and identification of nitrogen-fixing Enterobacter clocae and Klebsiella planticola associated with rice plants. Can. J. Microbiol. 29:1301-1308.
    CrossRef
  29. Lathrop SK, Bloom SM, Rao SM, Nutsch K, Lio CW, Santacruz N, et al. 2011. Peripheral education of the immune system by colonic commensal microbiota. Nature 478: 250254.
    Pubmed PMC CrossRef
  30. Mariat D, Firmesse O, Levenez F, Guimarães VD, Sokol H, Doré J, et al. 2009. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 9: 123.
    Pubmed PMC CrossRef
  31. Matijaši BB, Obermajer T, Lipoglavšek L, Grabnar I, Gorazd A, Rogelj I. 2013. Association of dietary type with fecal microbiota in vegetarians and omnivores in Slovenia. Eur. J. Nutr. 53: 1051-1064.
    Pubmed CrossRef
  32. Martinez L, Caballero-Mellaod J, Orozco J, Martinez-Romero E. 2003. Diazotrophic bacteria associated with banana (Musa spp.). Plant Soil 257: 35-47.
    CrossRef
  33. Martínez I, Muller CE, Walter J. 2013. Long-term temporal analysis of the human fecal microbiota revealed a stable core of dominant bacterial species. PLoS One 8: e69621.
    Pubmed PMC CrossRef
  34. Meer RR, Songer JG, Park DL. 1997. Human disease associated with Clostridium perfringens enterotoxin. Rev. Environ. Contam. Toxicol. 150: 75-94.
    Pubmed CrossRef
  35. Miquel S, Martin R, Rossi O, Bermúdez-Humarán LG, Chatel JM, Sokol H, et al. 2013. Faecalibacterium prausnitzii and human intestinal health. Curr. Opin. Microbiol. 16: 1-7.
    Pubmed CrossRef
  36. Nair P, Mayberry JF. 1994. Vegetarianism, dietary fibre and gastro-intestinal disease. Digest. Dis. 12: 177-185.
    Pubmed CrossRef
  37. Nakayama J. 2010. Pyrosequence-based 16S rRNA profiling of gastrointestinal microbiota. Biosci. Microflora 29: 83-96.
    CrossRef
  38. Nakayama J, Jiang J, Watanabe K, Chen K, Ninxin H, Matsuda K, et al. 2013. Up to the species-level community analysis of human gut microbiota by 16S rRNA amplicon pyrosequencing. Biosci. Microbiota Food Health 32: 69-76.
    Pubmed PMC CrossRef
  39. Nam Y, Jung M, Roh S, Kim M, Bae J. 2011. Comparative analysis of Korean human gut microbiota by barcoded pyrosequencing. PLoS One 6: e22109.
    Pubmed PMC CrossRef
  40. Ottman N, Smidt H, de Vos WM, Belzer C. 2012. The function of our microbiota: who is out there and what do they do? Front. Cell. Infect. Microbiol. 2: 1-11.
    Pubmed PMC CrossRef
  41. Palus JA, Borneman J, Ludden PW, Triplett EW. 1996. Adiazotrophic bacterial endophyte isolated from stems of Zea mays L., and Zea luxurians Itlis and Doebley. Plant Soil 186: 135-142.
    CrossRef
  42. Pien FD, Shrum S, Swenson JM, Hill BC, Thornsberry C, Farmer 3rd JJ. 1985. Colonization of human wounds by Escherichia vulneris and Escherichia hermannii. J. Clin. Microbiol. 22: 283-285.
    Pubmed PMC
  43. Poulou A, Dimitroulia E, Markou F, Tsakris A. 2008. Escherichia hermannii as the sole isolate from a patient with purulent conjunctivitis. J. Clin. Microbiol. 46: 3848-3849.
    Pubmed PMC CrossRef
  44. Reiter B, Burgmann H, Burg K, Sessitsch A. 2003. Endophytic nifH gene diversity in African sweet potato. Can. J. Microbiol. 49: 549-555.
    Pubmed CrossRef
  45. Ruengsomwong S, Korenori Y, Sakamoto N, Wannissorn B, Nakayama J, Nitisinprasert S. 2014. Senior Thai fecal microbiota comparison between vegetarians and nonvegetarians using PCR-DGGE and real-time PCR. J. Microbiol. Biotechnol. 24: 1026-1033.
    Pubmed CrossRef
  46. Sokol H, Pigneur B, Watterlot L, Lakhdari O, BermúdezHuma an LG, Gratadoux J, et al. 2008. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA 43: 16731-16736.
    Pubmed PMC CrossRef
  47. Tonstad S, Butler T, Yan R, Fraser GE. 2009. Type of vegetarian diet, body weight, and prevalence of type 2 diabetes. Diabetes Care 32: 791-796.
    Pubmed PMC CrossRef
  48. Veshnyakova A, Protze J, Rossa J, Blasig IE, Krause G, Piontek J. 2010. On the interaction of Clostridium perfringens enterotoxin with claudins. Toxins 2: 1336-1356.
    Pubmed PMC CrossRef
  49. Vincent WF. 2013. The genus Escherichia - an overview. Quest Diagnostics Infectious Disease Update 20: 36-48.
  50. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y, Keilbaugh SA, et al. 2011. Linking long-term dietary patterns with gut microbial enterotypes. Science 334: 105-108.
    Pubmed PMC CrossRef
  51. Wu GD, Bushmanc FD, Lewis JD. 2013. Diet, the human gut microbiota, and IBD. Anaerobe 24: 117-120.
    Pubmed CrossRef
  52. Woodmansey EJ. 2007. Intestinal bacteria and aging. J. Appl. Microbiol. 102: 1178-1186.
    Pubmed CrossRef
  53. Yatsuneko T, Rey FE, Manary MJ, Trehan I, DominguezBello MG, Contreras M, et al. 2012. Human gut microbiome viewed across age and geography. Nature 486: 222-227.
  54. Zhang HJ, Han P, Sun SY, Wang LY, Yan B, Zhang JH, et al. 2013. Attenuated associations between increasing BMI and unfavorable lipid profiles in Chinese Buddhist vegetarians. Asia Pac. J. Clin. Nutr. 22: 249-256.
    Pubmed

Related articles in JMB

More Related Articles

Article

Research article

J. Microbiol. Biotechnol. 2016; 26(10): 1723-1735

Published online October 28, 2016 https://doi.org/10.4014/jmb.1603.03057

Copyright © The Korean Society for Microbiology and Biotechnology.

Microbial Community of Healthy Thai Vegetarians and Non-Vegetarians, Their Core Gut Microbiota, and Pathogen Risk

Supatjaree Ruengsomwong 1, 2, 3, Orawan La-ongkham 1, Jiahui Jiang 4, Bhusita Wannissorn 3, Jiro Nakayama 4 and Sunee Nitisinprasert 1, 2*

1Specialized Research Unit: Probiotics and Prebiotics for Health, Department of Biotechnology, Faculty of Agro-Industry, Kasetsart University, Chatuchak, Bangkok 10900, Thailand, 2Center for Advanced Studies for Agriculture and Food, Kasetsart University Institute for Advanced Studies, Kasetsart University, Chatuchak, Bangkok 10900, Thailand, 3Bioscience Department, Thailand Institute of Scientific and Technological Research, Technopolis, Pathum Thani 12120, Thailand, 4Laboratory of Microbial Technology, Division of Microbial Science and Technology, Department of Bioscience and Biotechnology, Faculty of Agriculture, Graduate School, Kyushu University, Fukuoka 812-8581, Japan

Received: March 24, 2016; Accepted: July 1, 2016

Abstract

Pyrosequencing analysis of intestinal microflora from healthy Thai vegetarians and nonvegetarians
exhibited 893 OTUs covering 189 species. The strong species indicators of
vegetarians and non-vegetarians were Prevotella copri and Bacteroides vulgatus as well as
bacteria close to Escherichia hermanii with % relative abundance of 16.9 and 4.5-4.7,
respectively. Core gut microbiota of the vegetarian and non-vegetarian groups consisted of 11
and 20 different bacterial species, respectively, belonging to Actinobacteria, Firmicutes, and
Proteobacteria commonly found in both groups. Two species, Faecalibacterium prausnitzii and
Gemmiger formicilis, had a prevalence of 100% in both groups. Three species, Clostridium nexile,
Eubacterium eligens, and P. copri, showed up in most vegetarians, whereas more diversity of
Collinsella aerofaciens, Ruminococcus torques, various species of Bacteroides, Parabacteroides,
Escherichia, and different species of Clostridium and Eubacterium were found in most nonvegetarians.
Considering the correlation of personal characters, consumption behavior, and
microbial groups, the age of non-vegetarians showed a strong positive correlation coefficient
of 0.54 (p = 0.001) to Bacteroides uniformis but exhibited a moderate one to Alistipes finegoldii
and B. vulgatus. Only a positive moderate correlation of body mass index and Parabacteroides
distasonis appeared. Based on the significant abundance of potential pathogens, the microbiota
of the non-vegetarian group showed an abundance of potential pathogen varieties of Bilophila
wadsworthia, Escherichia coli, and E. hermannii, whereas that of the vegetarian group served for
only Klebsiella pneumoniae. These results implied that the microbiota of vegetarians with high
abundance of P. copri and low potential pathogen variety would be a way to maintain good
health in Thais.

Keywords: fecal microbiota, pyrosequencing, core gut microbiota, Prevotella, pathogen risk, Enterobacteriaceae

References

  1. An QL, Yang XJ, Dong YM, Feng LJ, Kuang BJ, Li J. 2001. Using confocal laser scanning microscope to visualize the infection of rice root by GFP-labelled Klebsiella oxytoca SA2, an endophytic diazotroph. Acta Bot. Sin. 43: 558-564.
  2. Ananthan S, Raju S, Alavandi S. 1999. Enterotoxigenicity of Klebsiella pneumoniae associated with childhood gastroenteritis in Madras, India. Jpn. J. Infect. Dis. 52: 16-17.
    Pubmed
  3. Arumugam M, Raes J, Pelletier E, Paslier DL, Yamada T, Mende DR, et al. 2011. Enterotypes of the human gut microbiome. Nature 473: 174-180.
    Pubmed KoreaMed CrossRef
  4. Bagley ST. 1985. Habitat association of Klebsiella species. Infect. Control 6: 52-56.
    Pubmed CrossRef
  5. Bentley R, Meganathan R. 1982. Biosynthesis of vitamin K (menaquinone) in bacteria. Microbiol. Rev. 46: 241-280.
    Pubmed KoreaMed
  6. Brenner DJ, Davis BR, Steigewalt AG, Riddle CF, McWhorter AC, Allen SD, et al. 1982. Atypical biogroups of Escherichia coli found in clinical specimens and description of Escherichia hermannii sp. nov. J. Clin. Microbiol. 15: 703-713.
    Pubmed KoreaMed
  7. Chelius MK, Triplett EW. 2000. Immunolocalization of dinitrogenase reductase produced by Klebsiella pneumoniae in association with Zea mays L. Appl. Environ. Microbiol. 66:783-787.
    CrossRef
  8. Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, et al. 2012. Gut microbiota composition correlates with diet and health in the elderly. Nature 488: 178-184.
    Pubmed
  9. Clemente JC, Ursell LK, Parfrey LW, Knight R. 2012. The impact of the gut microbiota on human health: an integrative view. Cell 148: 1258-1270.
    Pubmed KoreaMed CrossRef
  10. Crowe FL, Roddam AW, Key TJ, Appleby PN, Overvad K, Jakobsen MU, et al. 2011. Fruit and vegetable intake and mortality from ischaemic heart disease: results from the European Prospective Investigation into Cancer and Nutrition (EPIC)-Heart Study. Eur. Heart J. 465: 1-9.
    CrossRef
  11. Cruz AY, Cazacu AC, Allen CH. 2007. Pantoea agglomerans, a plant pathogen causing human disease. J. Clin. Microbiol. 45: 1989-1992.
    Pubmed KoreaMed CrossRef
  12. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505: 559-563.
    Pubmed KoreaMed CrossRef
  13. De Filippis F, Pellegrini N, Vannini L, Jeffery IB, La Storia A, Laghi L, et al. 2015. High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut DOI:10.1136/gutjnl-2015-309957.5.
  14. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 107:14691-14696.
    Pubmed KoreaMed CrossRef
  15. Dong YM, Chelius MK, Brisse S, Kozyrovska N, Kovtunovych GR, Podschun R, Triplett EW. 2003. Comparison between two Klebsiella: the plant endophyte K. pneumoniaee 342 and a clinical isolate, K. pneumoniaee MGH78578. Symbiosis 35: 247259.
  16. Do e J, Corthier G. 2010. The human intestinal microbiota. Gastroenterol. Clin. Biol. 34: S7-S15.
    CrossRef
  17. Duncan SH, Louis P, Thomson JM, Flint HJ. 2009. The role of pH in determining the species composition of the human colonic microbiota. Environ. Microbiol. 11: 2112-2122.
    Pubmed CrossRef
  18. Gentschew L, Ferguson LR. 2012. Role of nutrition and microbiota in susceptibility to inflammatory bowel diseases. Mol. Nutr. Food Res. 56: 524-535.
    Pubmed CrossRef
  19. Guerrant RL, Moore RA, Kerschfeld PM, Sande MA. 1975. Role of toxigenic and invasive bacteria in acute diarrhea of childhood. N. Engl. J. Med. 293: 567-571.
    Pubmed CrossRef
  20. Hayashi H, Sakamoto M, Benno Y. 2002. Fecal microbial diversity in a strict vegetarian as determined by molecular analysis and cultivation. Microbiol. Immunol. 46: 819-831.
    Pubmed CrossRef
  21. Jain A, Bohra I, Mahajan R, Jain S, Chugh TD. 2012. Pantoea agglomerans infection behaving like a tumor after plant thorn injury: an unusual presentation. Indian J. Pathol. Microbiol. 55: 386-388.
    Pubmed CrossRef
  22. Jeffery IB, O’Toole PW. 2013. Diet-microbiota interactions and their implications for healthy living. Nutrient 5: 234-252.
    Pubmed KoreaMed CrossRef
  23. Kabeerdoss J, Devi RS, Mary RR, Ramakrishna BS. 2012. Faecal microbiota composition in vegetarians: comparison with omnivores in a cohort of young women in southern India. Br. J. Nutr. 108: 953-957.
    Pubmed CrossRef
  24. Kadner RJ. 1978. Repression of synthesis of the vitamin B 12 receptor in Escherichia coli. J. Bacteriol. 136: 1050-1057.
    Pubmed KoreaMed
  25. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2: 123-140.
    Pubmed CrossRef
  26. Kim MS, Hwang SS, Park EJ, Bae JW. 2013. Strict vegetarian diet improves the risk fators associated with metabolic diseases by modulating gut microbiota and reducing intestinal inflammation. Environ. Microbiol. Rep. 5: 765-775.
    Pubmed
  27. Knittel MD, Seidler RJ, Eby C, Cabe LM. 1977. Colonization of the botanical environment by Klebsiella isolates of pathogenic origin. Appl. Environ. Microbiol. 34: 557-563.
    Pubmed KoreaMed
  28. Ladha JK, Barraquio WL, Watanabe I. 1983. Isolation and identification of nitrogen-fixing Enterobacter clocae and Klebsiella planticola associated with rice plants. Can. J. Microbiol. 29:1301-1308.
    CrossRef
  29. Lathrop SK, Bloom SM, Rao SM, Nutsch K, Lio CW, Santacruz N, et al. 2011. Peripheral education of the immune system by colonic commensal microbiota. Nature 478: 250254.
    Pubmed KoreaMed CrossRef
  30. Mariat D, Firmesse O, Levenez F, Guimarães VD, Sokol H, Doré J, et al. 2009. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 9: 123.
    Pubmed KoreaMed CrossRef
  31. Matijaši BB, Obermajer T, Lipoglavšek L, Grabnar I, Gorazd A, Rogelj I. 2013. Association of dietary type with fecal microbiota in vegetarians and omnivores in Slovenia. Eur. J. Nutr. 53: 1051-1064.
    Pubmed CrossRef
  32. Martinez L, Caballero-Mellaod J, Orozco J, Martinez-Romero E. 2003. Diazotrophic bacteria associated with banana (Musa spp.). Plant Soil 257: 35-47.
    CrossRef
  33. Martínez I, Muller CE, Walter J. 2013. Long-term temporal analysis of the human fecal microbiota revealed a stable core of dominant bacterial species. PLoS One 8: e69621.
    Pubmed KoreaMed CrossRef
  34. Meer RR, Songer JG, Park DL. 1997. Human disease associated with Clostridium perfringens enterotoxin. Rev. Environ. Contam. Toxicol. 150: 75-94.
    Pubmed CrossRef
  35. Miquel S, Martin R, Rossi O, Bermúdez-Humarán LG, Chatel JM, Sokol H, et al. 2013. Faecalibacterium prausnitzii and human intestinal health. Curr. Opin. Microbiol. 16: 1-7.
    Pubmed CrossRef
  36. Nair P, Mayberry JF. 1994. Vegetarianism, dietary fibre and gastro-intestinal disease. Digest. Dis. 12: 177-185.
    Pubmed CrossRef
  37. Nakayama J. 2010. Pyrosequence-based 16S rRNA profiling of gastrointestinal microbiota. Biosci. Microflora 29: 83-96.
    CrossRef
  38. Nakayama J, Jiang J, Watanabe K, Chen K, Ninxin H, Matsuda K, et al. 2013. Up to the species-level community analysis of human gut microbiota by 16S rRNA amplicon pyrosequencing. Biosci. Microbiota Food Health 32: 69-76.
    Pubmed KoreaMed CrossRef
  39. Nam Y, Jung M, Roh S, Kim M, Bae J. 2011. Comparative analysis of Korean human gut microbiota by barcoded pyrosequencing. PLoS One 6: e22109.
    Pubmed KoreaMed CrossRef
  40. Ottman N, Smidt H, de Vos WM, Belzer C. 2012. The function of our microbiota: who is out there and what do they do? Front. Cell. Infect. Microbiol. 2: 1-11.
    Pubmed KoreaMed CrossRef
  41. Palus JA, Borneman J, Ludden PW, Triplett EW. 1996. Adiazotrophic bacterial endophyte isolated from stems of Zea mays L., and Zea luxurians Itlis and Doebley. Plant Soil 186: 135-142.
    CrossRef
  42. Pien FD, Shrum S, Swenson JM, Hill BC, Thornsberry C, Farmer 3rd JJ. 1985. Colonization of human wounds by Escherichia vulneris and Escherichia hermannii. J. Clin. Microbiol. 22: 283-285.
    Pubmed KoreaMed
  43. Poulou A, Dimitroulia E, Markou F, Tsakris A. 2008. Escherichia hermannii as the sole isolate from a patient with purulent conjunctivitis. J. Clin. Microbiol. 46: 3848-3849.
    Pubmed KoreaMed CrossRef
  44. Reiter B, Burgmann H, Burg K, Sessitsch A. 2003. Endophytic nifH gene diversity in African sweet potato. Can. J. Microbiol. 49: 549-555.
    Pubmed CrossRef
  45. Ruengsomwong S, Korenori Y, Sakamoto N, Wannissorn B, Nakayama J, Nitisinprasert S. 2014. Senior Thai fecal microbiota comparison between vegetarians and nonvegetarians using PCR-DGGE and real-time PCR. J. Microbiol. Biotechnol. 24: 1026-1033.
    Pubmed CrossRef
  46. Sokol H, Pigneur B, Watterlot L, Lakhdari O, BermúdezHuma an LG, Gratadoux J, et al. 2008. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA 43: 16731-16736.
    Pubmed KoreaMed CrossRef
  47. Tonstad S, Butler T, Yan R, Fraser GE. 2009. Type of vegetarian diet, body weight, and prevalence of type 2 diabetes. Diabetes Care 32: 791-796.
    Pubmed KoreaMed CrossRef
  48. Veshnyakova A, Protze J, Rossa J, Blasig IE, Krause G, Piontek J. 2010. On the interaction of Clostridium perfringens enterotoxin with claudins. Toxins 2: 1336-1356.
    Pubmed KoreaMed CrossRef
  49. Vincent WF. 2013. The genus Escherichia - an overview. Quest Diagnostics Infectious Disease Update 20: 36-48.
  50. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y, Keilbaugh SA, et al. 2011. Linking long-term dietary patterns with gut microbial enterotypes. Science 334: 105-108.
    Pubmed KoreaMed CrossRef
  51. Wu GD, Bushmanc FD, Lewis JD. 2013. Diet, the human gut microbiota, and IBD. Anaerobe 24: 117-120.
    Pubmed CrossRef
  52. Woodmansey EJ. 2007. Intestinal bacteria and aging. J. Appl. Microbiol. 102: 1178-1186.
    Pubmed CrossRef
  53. Yatsuneko T, Rey FE, Manary MJ, Trehan I, DominguezBello MG, Contreras M, et al. 2012. Human gut microbiome viewed across age and geography. Nature 486: 222-227.
  54. Zhang HJ, Han P, Sun SY, Wang LY, Yan B, Zhang JH, et al. 2013. Attenuated associations between increasing BMI and unfavorable lipid profiles in Chinese Buddhist vegetarians. Asia Pac. J. Clin. Nutr. 22: 249-256.
    Pubmed