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References

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  2. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. 2005. Host-bacterial mutualism in the human intestine. Science 307: 1915-1920.
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    Pubmed PMC CrossRef
  9. Collado MC, Derrien M, Isolauri E. 2007. Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl. Environ. Microbiol. 73: 7767-7770.
    Pubmed PMC CrossRef
  10. Davinelli S, Willcox DC, Scapagnini G. 2012. Extending healthy ageing: nutrient sensitive pathway and centenarian population. Immun. Ageing 9: 1-7.
    Pubmed PMC CrossRef
  11. 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
  12. Dethlefsen L, Huse S, Sogin ML, Relman DA. 2008. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 6: 2383-2400.
    Pubmed PMC CrossRef
  13. Devillard E, McIntosh FM, Duncan SH, Wallace RJ. 2007. Metabolism of linoleic acid by human gut bacteria: different routes for biosynthesis of conjugated linoleic acid. J. Bacteriol. 189: 2566-2570.
    Pubmed PMC CrossRef
  14. Drago L, Toscano M, Rodighiero V, De Vecchi E, Mogna G. 2012. Cultivable and pyrosequenced fecal microflora in centenarians and young subjects. J. Clin. Gastroenterol. 46:S81-S84.
    Pubmed CrossRef
  15. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE. 2007. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl. Environ. Microbiol. 73: 1073-1078.
    Pubmed PMC CrossRef
  16. Duncan SH, Louis P, Flint HJ. 2007. Cultivable bacterial diversity from the human colon. Lett. Appl. Microbiol. 44:343-350.
    Pubmed CrossRef
  17. Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998.
    Pubmed CrossRef
  18. Fan W, Huo G, Li X, Yang L, Duan C. 2 014. Impact of diet in shaping gut microbiota revealed by a comparative study in infants during the first six months of life. J. Microbiol. Biotechnol. 24: 133-143.
    Pubmed CrossRef
  19. Ku H-J, Lee J-H. 2014. Development of a novel long-range 16S rRNA universal primer set for metagenomic analysis of gastrointestinal microbiota in newborn infants. J. Microbiol. Biotechnol. 24: 812-822.
    Pubmed CrossRef
  20. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. 2008. Evolution of mammals and their gut microbes. Science 320: 1647-1651.
    Pubmed PMC CrossRef
  21. Ling ZX, Li ZL, L iu X , Cheng YW, Luo YQ, Tong XJ, et al. 2014. Altered fecal microbiota composition associated with food allergy in infants. Appl. Environ. Microbiol. 80: 2546-2554.
    Pubmed PMC CrossRef
  22. Louis P , Duncan SH, McCrae SI, Millar J , Jackson MS, Flint HJ. 2004. Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J. Bacteriol. 186: 2099-2106.
    Pubmed PMC CrossRef
  23. Macfarlane GT, Englyst HN. 1986. Starch utilization by the human large intestinal microflora. J. Appl. Bacteriol. 60: 195-201.
    Pubmed CrossRef
  24. Macfarlane S, Furrie E, Macfarlane GT, Dillon JF. 2007. Microbial colonization of the upper gastrointestinal tract in patients with Barrett's esophagus. Clin. Infect. Dis. 45: 29-38.
    Pubmed CrossRef
  25. Magoc T, Salzberg SL. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27: 2957-2963.
    Pubmed PMC CrossRef
  26. Mueller S, Saunier K, Hanisch C, Norin E, Alm L, Midtvedt T, et al. 2006. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl. Environ. Microbiol. 72: 1027-1033.
    Pubmed PMC CrossRef
  27. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. 2007. Development of the human infant intestinal microbiota. PloS Biol. 5: 1556-1573.
    Pubmed PMC CrossRef
  28. Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ. 2002. The microbiology of butyrate formation in the human colon. FEMS Microbiol. Lett. 217: 133-139.
    Pubmed CrossRef
  29. Rajilic-Stojanovic M, Heilig HGHJ, Molenaar D, Kajander K, Surakka A, Smidt H, de Vos WM. 2009. Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ. Microbiol. 11: 1736-1751.
    Pubmed PMC CrossRef
  30. Ruengsomwong S, Korenori Y, Sakamoto N, Wannissorn B, Nakayama J, Nitisinprasert S. 2014. Senior Thai fecal microbiota comparison between vegetarians and non-vegetarians using PCR-DGGE and real-time PCR. J. Microbiol. Biotechnol. 24:1026-1033.
    Pubmed CrossRef
  31. Salonen A, Lahti L, Salojarvi J, Holtrop G, Korpela K, Duncan SH, et al. 2014. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. ISME J. 8: 2218-2230.
    Pubmed PMC CrossRef
  32. Salyers AA. 1984. Bacteroides of the human lower intestinal tract. Annu. Rev. Microbiol. 38: 293-313.
    Pubmed CrossRef
  33. Scott K P, Gratz S W, Sheridan PO, Flint HJ, Duncan SH. 2013. The influence of diet on the gut microbiota. Pharmacol. Res. 69: 52-60.
    Pubmed CrossRef
  34. Shi S , Liu S , Huang Q , Huang F, Wei Y . 2012. Guangxi Zhuang Autonomous County’s 2010 Population Census, pp. 222-240. China Statistics Press, Beijing.
  35. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley R E, et al. 2009. A core gut microbiome in obese and lean twins. Nature 457: 480-487.
    Pubmed PMC CrossRef
  36. van Hylckama Vlieg JE, Veiga P, Zhang C, Derrien M, Zhao L. 2011. Impact of microbial transformation of food on health-from fermented foods to fermentation in the gastrointestinal tract. Curr. Opin. Biotechnol. 22: 211-219.
    Pubmed CrossRef
  37. Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73: 5261-5267.
    Pubmed PMC CrossRef
  38. Wang T, Cai G, Qiu Y, Fei N, Zhang M, Pang X, et al. 2012. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteer. ISME J. 6: 320-329.
    Pubmed PMC CrossRef
  39. Wong JMW, de Souza R, Kendall CWC, Emam A, Jenkins DJA. 2006. Colonic health: fermentation and short chain fatty acids. J. Clin. Gastroenterol. 40: 235-243.
    Pubmed CrossRef
  40. Zhao L, Qiao X, Zhu J , Zhang X , Jiang J , Hao Y , Ren F . 2011. Correlations of fecal bacterial communities with age and living r egion f or t he e lderly l iving in B ama, Guangxi, China. J. Microbiol. 49: 186-192.
    Pubmed CrossRef
  41. Zhao L, Xu W, Ibrahim SA, Jin J, Feng J, Jiang J, et al. 2011. Effects of age and region on fecal microflora in elderly subjects living in Bama, Guangxi, China. Curr. Microbiol. 62: 64-70.
    Pubmed CrossRef
  42. Zwielehner J, Liszt K , Handschur M , Lassl C , Lapin A , Haslberger AG. 2009. Combined PCR-DGGE fingerprinting and quantitative-PCR indicates shifts in fecal population sizes and diversity of Bacteroides, bifidobacteria and Clostridium cluster IV in institutionalized elderly. Exp. Gerontol. 44: 440-446.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(8): 1195-1204

Published online August 28, 2015 https://doi.org/10.4014/jmb.1410.10014

Copyright © The Korean Society for Microbiology and Biotechnology.

Gut Microbiota Community and Its Assembly Associated with Age and Diet in Chinese Centenarians

Fang Wang 1, Ting Yu 1, Guohong Huang 1, 2, Da Cai 1, Xiaolin Liang 1, Haiyan Su 1, Zhenjun Zhu 1, Danlei Li 3, Yang Yang 4, Peihong Shen 4, Ruifeng Mao 1, Lian Yu 1, Mouming Zhao 1 and Quanyang Li 1*

1College of Light Industry and Food Engineering, Guangxi University, Nanning 530004, P.R. China, 2Food and Biological Technology Department, Guangxi Polytechnic, Nanning 530226, P.R. China, 3College of Life Sciences, Tianjin Normal University, Tianjin 300387, P.R. China, 4College of Life Science and Technology, Guangxi University, Nanning 530004, P.R. China

Received: October 7, 2014; Accepted: April 1, 2015

Abstract

Increasing evidence suggests that gut microbiota underpin the development of health and
longevity. However, our understanding of what influences the composition of this community
of the longevous has not been adequately described. Therefore, illumina sequencing analysis
was performed on the gut microbiota of centenarians (aged 100-108 years; RC) and younger
elderlies (aged 85-99 years; RE) living in Bama County, Guangxi, China and the elderlies (aged
80-92 years; CE) living in Nanning City, Guangxi, China. In addition, their diet was monitored
using a semiquantitative dietary questionary (FFQ 23). The results revealed the abundance of
Roseburia and Escherichia was significantly greater, whereas that of Lactobacillus,
Faecalibacterium, Parabacteroides, Butyricimonas, Coprococcus, Megamonas, Mitsuokella, Sutterella,
and Akkermansia was significantly less in centenarians at the genus level. Both clustering
analysis and UniFraq distance analysis showed structural segregation with age and diet
among the three populations. Using partial least square discriminate analysis and redundancy
analysis, we identified 33 and 34 operational taxonomic units (OTUs) as key OTUs that were
significantly associated with age and diet, respectively. Age-related OTUs were characterized
as Ruminococcaceae, Clostridiaceae, and Lachnospiraceae, and the former two were increased in
the centenarians; diet-related OTUs were classified as Bacteroidales, Lachnospiraceae, and
Ruminococcaceae. The former two were deceased, whereas the later one was increased, in the
high-fiber diet. The age and high-fiber diet were concomitant with changes in the gut
microbiota of centenarians, suggesting that age and high-fiber diet can establish a new
structurally balanced architecture of gut microbiota that may benefit the health of
centenarians.

Keywords: centenarians, gut microbiota, illumina sequencing, age, diet

References

  1. Anonymous. 1996. Use of geographic information systems in epidemiology (GIS-Epi). Epidemiol. Bull. 17: 1-6.
  2. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. 2005. Host-bacterial mutualism in the human intestine. Science 307: 1915-1920.
    Pubmed CrossRef
  3. Biagi E, Candela M, Fairweather-Tait S, Franceschi C, Brigidi P. 2012. Ageing of the human metaorganism: the microbial counterpart. Age 34: 247-267.
    Pubmed KoreaMed CrossRef
  4. Biagi E, Nylund L, Candela M, Ostan R, Bucci L, Pini E, et al. 2010. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One 5: 1-14.
    KoreaMed CrossRef
  5. Caporaso J G, Kuczynski J , Stombaugh J , Bittinger K , Bushman FD, Costello EK, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7: 335-336.
    Pubmed KoreaMed CrossRef
  6. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA 108: 4516-4522.
    Pubmed KoreaMed CrossRef
  7. Chen Y, Yang F, Lu H, Wang B, Chen Y, Lei D, et al. 2011. Characterization of fecal microbial communities in patients with liver cirrhosis. Hepatology 54: 562-572.
    Pubmed CrossRef
  8. Claesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, et al. 2011. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc. Natl. Acad. Sci. USA 108: 4586-4591.
    Pubmed KoreaMed CrossRef
  9. Collado MC, Derrien M, Isolauri E. 2007. Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl. Environ. Microbiol. 73: 7767-7770.
    Pubmed KoreaMed CrossRef
  10. Davinelli S, Willcox DC, Scapagnini G. 2012. Extending healthy ageing: nutrient sensitive pathway and centenarian population. Immun. Ageing 9: 1-7.
    Pubmed KoreaMed CrossRef
  11. 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
  12. Dethlefsen L, Huse S, Sogin ML, Relman DA. 2008. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 6: 2383-2400.
    Pubmed KoreaMed CrossRef
  13. Devillard E, McIntosh FM, Duncan SH, Wallace RJ. 2007. Metabolism of linoleic acid by human gut bacteria: different routes for biosynthesis of conjugated linoleic acid. J. Bacteriol. 189: 2566-2570.
    Pubmed KoreaMed CrossRef
  14. Drago L, Toscano M, Rodighiero V, De Vecchi E, Mogna G. 2012. Cultivable and pyrosequenced fecal microflora in centenarians and young subjects. J. Clin. Gastroenterol. 46:S81-S84.
    Pubmed CrossRef
  15. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE. 2007. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl. Environ. Microbiol. 73: 1073-1078.
    Pubmed KoreaMed CrossRef
  16. Duncan SH, Louis P, Flint HJ. 2007. Cultivable bacterial diversity from the human colon. Lett. Appl. Microbiol. 44:343-350.
    Pubmed CrossRef
  17. Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998.
    Pubmed CrossRef
  18. Fan W, Huo G, Li X, Yang L, Duan C. 2 014. Impact of diet in shaping gut microbiota revealed by a comparative study in infants during the first six months of life. J. Microbiol. Biotechnol. 24: 133-143.
    Pubmed CrossRef
  19. Ku H-J, Lee J-H. 2014. Development of a novel long-range 16S rRNA universal primer set for metagenomic analysis of gastrointestinal microbiota in newborn infants. J. Microbiol. Biotechnol. 24: 812-822.
    Pubmed CrossRef
  20. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. 2008. Evolution of mammals and their gut microbes. Science 320: 1647-1651.
    Pubmed KoreaMed CrossRef
  21. Ling ZX, Li ZL, L iu X , Cheng YW, Luo YQ, Tong XJ, et al. 2014. Altered fecal microbiota composition associated with food allergy in infants. Appl. Environ. Microbiol. 80: 2546-2554.
    Pubmed KoreaMed CrossRef
  22. Louis P , Duncan SH, McCrae SI, Millar J , Jackson MS, Flint HJ. 2004. Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J. Bacteriol. 186: 2099-2106.
    Pubmed KoreaMed CrossRef
  23. Macfarlane GT, Englyst HN. 1986. Starch utilization by the human large intestinal microflora. J. Appl. Bacteriol. 60: 195-201.
    Pubmed CrossRef
  24. Macfarlane S, Furrie E, Macfarlane GT, Dillon JF. 2007. Microbial colonization of the upper gastrointestinal tract in patients with Barrett's esophagus. Clin. Infect. Dis. 45: 29-38.
    Pubmed CrossRef
  25. Magoc T, Salzberg SL. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27: 2957-2963.
    Pubmed KoreaMed CrossRef
  26. Mueller S, Saunier K, Hanisch C, Norin E, Alm L, Midtvedt T, et al. 2006. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl. Environ. Microbiol. 72: 1027-1033.
    Pubmed KoreaMed CrossRef
  27. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. 2007. Development of the human infant intestinal microbiota. PloS Biol. 5: 1556-1573.
    Pubmed KoreaMed CrossRef
  28. Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ. 2002. The microbiology of butyrate formation in the human colon. FEMS Microbiol. Lett. 217: 133-139.
    Pubmed CrossRef
  29. Rajilic-Stojanovic M, Heilig HGHJ, Molenaar D, Kajander K, Surakka A, Smidt H, de Vos WM. 2009. Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ. Microbiol. 11: 1736-1751.
    Pubmed KoreaMed CrossRef
  30. Ruengsomwong S, Korenori Y, Sakamoto N, Wannissorn B, Nakayama J, Nitisinprasert S. 2014. Senior Thai fecal microbiota comparison between vegetarians and non-vegetarians using PCR-DGGE and real-time PCR. J. Microbiol. Biotechnol. 24:1026-1033.
    Pubmed CrossRef
  31. Salonen A, Lahti L, Salojarvi J, Holtrop G, Korpela K, Duncan SH, et al. 2014. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. ISME J. 8: 2218-2230.
    Pubmed KoreaMed CrossRef
  32. Salyers AA. 1984. Bacteroides of the human lower intestinal tract. Annu. Rev. Microbiol. 38: 293-313.
    Pubmed CrossRef
  33. Scott K P, Gratz S W, Sheridan PO, Flint HJ, Duncan SH. 2013. The influence of diet on the gut microbiota. Pharmacol. Res. 69: 52-60.
    Pubmed CrossRef
  34. Shi S , Liu S , Huang Q , Huang F, Wei Y . 2012. Guangxi Zhuang Autonomous County’s 2010 Population Census, pp. 222-240. China Statistics Press, Beijing.
  35. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley R E, et al. 2009. A core gut microbiome in obese and lean twins. Nature 457: 480-487.
    Pubmed KoreaMed CrossRef
  36. van Hylckama Vlieg JE, Veiga P, Zhang C, Derrien M, Zhao L. 2011. Impact of microbial transformation of food on health-from fermented foods to fermentation in the gastrointestinal tract. Curr. Opin. Biotechnol. 22: 211-219.
    Pubmed CrossRef
  37. Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73: 5261-5267.
    Pubmed KoreaMed CrossRef
  38. Wang T, Cai G, Qiu Y, Fei N, Zhang M, Pang X, et al. 2012. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteer. ISME J. 6: 320-329.
    Pubmed KoreaMed CrossRef
  39. Wong JMW, de Souza R, Kendall CWC, Emam A, Jenkins DJA. 2006. Colonic health: fermentation and short chain fatty acids. J. Clin. Gastroenterol. 40: 235-243.
    Pubmed CrossRef
  40. Zhao L, Qiao X, Zhu J , Zhang X , Jiang J , Hao Y , Ren F . 2011. Correlations of fecal bacterial communities with age and living r egion f or t he e lderly l iving in B ama, Guangxi, China. J. Microbiol. 49: 186-192.
    Pubmed CrossRef
  41. Zhao L, Xu W, Ibrahim SA, Jin J, Feng J, Jiang J, et al. 2011. Effects of age and region on fecal microflora in elderly subjects living in Bama, Guangxi, China. Curr. Microbiol. 62: 64-70.
    Pubmed CrossRef
  42. Zwielehner J, Liszt K , Handschur M , Lassl C , Lapin A , Haslberger AG. 2009. Combined PCR-DGGE fingerprinting and quantitative-PCR indicates shifts in fecal population sizes and diversity of Bacteroides, bifidobacteria and Clostridium cluster IV in institutionalized elderly. Exp. Gerontol. 44: 440-446.
    Pubmed CrossRef