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Gut Microbiota Community and Its Assembly Associated with Age and Diet in Chinese Centenarians
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
J. Microbiol. Biotechnol. 2015; 25(8): 1195-1204
Published August 28, 2015 https://doi.org/10.4014/jmb.1410.10014
Copyright © The Korean Society for Microbiology and Biotechnology.
Abstract
Keywords
References
- Anonymous. 1996. Use of geographic information systems in epidemiology (GIS-Epi). Epidemiol. Bull. 17: 1-6.
- Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. 2005. Host-bacterial mutualism in the human intestine. Science 307: 1915-1920.
- Biagi E, Candela M, Fairweather-Tait S, Franceschi C, Brigidi P. 2012. Ageing of the human metaorganism: the microbial counterpart. Age 34: 247-267.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- Davinelli S, Willcox DC, Scapagnini G. 2012. Extending healthy ageing: nutrient sensitive pathway and centenarian population. Immun. Ageing 9: 1-7.
- 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.
- 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.
- 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.
- 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.
- 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.
- Duncan SH, Louis P, Flint HJ. 2007. Cultivable bacterial diversity from the human colon. Lett. Appl. Microbiol. 44:343-350.
- Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998.
- 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.
- 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.
- 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.
- 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.
- 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.
- Macfarlane GT, Englyst HN. 1986. Starch utilization by the human large intestinal microflora. J. Appl. Bacteriol. 60: 195-201.
- 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.
- Magoc T, Salzberg SL. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27: 2957-2963.
- 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.
- Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. 2007. Development of the human infant intestinal microbiota. PloS Biol. 5: 1556-1573.
- 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.
- 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.
- 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.
- 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.
- Salyers AA. 1984. Bacteroides of the human lower intestinal tract. Annu. Rev. Microbiol. 38: 293-313.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
Related articles in JMB

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
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
- Anonymous. 1996. Use of geographic information systems in epidemiology (GIS-Epi). Epidemiol. Bull. 17: 1-6.
- Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. 2005. Host-bacterial mutualism in the human intestine. Science 307: 1915-1920.
- Biagi E, Candela M, Fairweather-Tait S, Franceschi C, Brigidi P. 2012. Ageing of the human metaorganism: the microbial counterpart. Age 34: 247-267.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- Davinelli S, Willcox DC, Scapagnini G. 2012. Extending healthy ageing: nutrient sensitive pathway and centenarian population. Immun. Ageing 9: 1-7.
- 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.
- 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.
- 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.
- 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.
- 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.
- Duncan SH, Louis P, Flint HJ. 2007. Cultivable bacterial diversity from the human colon. Lett. Appl. Microbiol. 44:343-350.
- Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998.
- 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.
- 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.
- 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.
- 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.
- 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.
- Macfarlane GT, Englyst HN. 1986. Starch utilization by the human large intestinal microflora. J. Appl. Bacteriol. 60: 195-201.
- 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.
- Magoc T, Salzberg SL. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27: 2957-2963.
- 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.
- Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. 2007. Development of the human infant intestinal microbiota. PloS Biol. 5: 1556-1573.
- 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.
- 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.
- 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.
- 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.
- Salyers AA. 1984. Bacteroides of the human lower intestinal tract. Annu. Rev. Microbiol. 38: 293-313.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.