Enriched taxa were found among the gut microbiota of centenarians in East China


Autoři: Na Wang aff001;  Rui Li aff001;  Haijiang Lin aff002;  Chaowei Fu aff001;  Xuecai Wang aff002;  Yiming Zhang aff003;  Meifang Su aff004;  Peixin Huang aff004;  Junhua Qian aff004;  Feng Jiang aff001;  Hexing Wang aff001;  Lufang Jiang aff001;  Xin Yu aff001;  Jianxiang Liu aff001;  Yue Chen aff005;  Qingwu Jiang aff001
Působiště autorů: Key Laboratory of Public Health Safety of Ministry of Education, School of Public Health, Fudan University, Shanghai, China aff001;  Taizhou Center for Disease Control and Prevention, Taizhou City, Jiangsu Province, China aff002;  Deqing Center for Disease Control and Prevention, Deqing City, Zhejiang Province, China aff003;  Yuhuan Center for Disease Control and Prevention, Wenling City, Zhejiang Province, China aff004;  School of Epidemiology and Public Health, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada aff005
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222763

Souhrn

Background

Gut microbiota is closely related to age. Studies from Europe and the U.S. identified featured microbiota in different age groups for the elderly. Asian studies mainly focused on people living in longevity areas. Featured microbiota for the elderly people of different age groups, especially in the centenarian in the general population, has not been well investigated in China.

Method

We conducted a comparative study by including 198 subjects of three age groups (65–70, 90–99, and 100+ years) in East China. Information regarding age, sex, height, weight, waist circumference, hip circumference, food preference, smoking status and alcohol consumption were collected by using a structured questionnaire. Fecal samples for each participant were collected as well. 16S rRNA gene sequencing were employed to analyze the gut microbiota composition. Logistic regression with LASSO feature selection was used to identify featured taxa in different age groups and to assess their potential interactions with other factors such as lifestyle.

Result

The gut microbiota of the 90–99 year and 100+ year age groups showed more diversity, robustness, and richness compared with the 65–70 year age group. PCoA analysis showed a clear separation between the 65–70 and 100+ year age groups. At the species level, Bacteroides fragilis, Parabacteroides merdae, Ruminococcus gnavus, Coprococcus and Clostridium perfringens increased, but Bacteroides vulgatus, Ruminococcus sp.5139BFAA and Clostridium sp.AT5 decreased in the 90–99 year age group. The age differences in gut microbiota were similar across the strata of smoking, alcohol consumption status and food preference.

Conclusion

Our study demonstrated age differences in many aspects of gut microbiota, such as overall diversity, microbiota structure, and relative abundance of key taxa. Moreover, the gut microbiota of centenarian was significantly different from those of younger age groups of the elderly.

Klíčová slova:

Age groups – Aging – Alcohol consumption – Elderly – Geriatrics – Gut bacteria – Microbiome – Ruminococcus


Zdroje

1. Claesson MJ, Jeffery IB, Conde S, Power SE, O'Connor EM, Cusack S, et al. Gut microbiota composition correlates with diet and health in the elderly. NATURE. 2012; 488(7410): 178–84. doi: 10.1038/nature11319 22797518

2. Candela M, Biagi E, Brigidi P, O Toole PW, Vos WMD. Maintenance of a healthy trajectory of the intestinal microbiome during aging: A dietary approach. Mechanisms of Ageing & Development. 2014; 136-137(1): 70–5.

3. Cevenini E, Invidia L, Lescai F, Salvioli S, Tieri P, Castellani G, et al. Human models of aging and longevity. EXPERT OPIN BIOL TH. 2008; 8(9): 1393–405. doi: 10.1517/14712598.8.9.1393 18694357

4. Fredrik BC, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. SCIENCE. 2005; 307(5717): 1915–20. doi: 10.1126/science.1104816 15790844

5. Vlieg JETV, Patrick V, Chenhong Z, Muriel D, Liping Z. Impact of microbial transformation of food on health—from fermented foods to fermentation in the gastro-intestinal tract. CURR OPIN BIOTECH. 2011; 22(2): 211–9. doi: 10.1016/j.copbio.2010.12.004 21247750

6. Elena B, Lotta N, Marco C, Rita O, Laura B, Elisa P, et al. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLOS ONE. 2010; 5(5): e10667. doi: 10.1371/journal.pone.0010667 20498852

7. Nicoletti C. Age-associated changes of the intestinal epithelial barrier: local and systemic implications. EXPERT REV GASTROENT. 2015; 9(12): 1–3.

8. Leung K, Thuret S. Gut Microbiota: A Modulator of Brain Plasticity and Cognitive Function in Ageing. Healthcare. 2015; 3(4): 898–916. doi: 10.3390/healthcare3040898 27417803

9. Villa CR, W E W, Elena M C. Gut Microbiota-bone Axis. CRIT REV FOOD SCI. 2017; 57(8): 1664–72.

10. O'Toole PW, Claesson MJ. Gut microbiota: Changes throughout the lifespan from infancy to elderly. INT DAIRY J. 2010; 20(4): 281–91.

11. Mitsuoka T. Intestinal flora and aging. NUTRITION REVIEWS-WASHINGTON-. 1992; 50(438.

12. Zhao L, Qiao X, Zhu J, Zhang X, Jiang J, Hao Y, et al. Correlations of fecal bacterial communities with age and living region for the elderly living in Bama, Guangxi, China. J MICROBIOL. 2011; 49(2): 186–92. doi: 10.1007/s12275-011-0405-x 21538237

13. Zhao L, Xu W, Ibrahim SA, Jin J, Feng J, Jiang J, et al. Effects of age and region on fecal microflora in elderly subjects living in Bama, Guangxi, China. CURR MICROBIOL. 2011; 62(1): 64–70. doi: 10.1007/s00284-010-9676-4 20509028

14. Ling Z, Li Z, Liu X, Cheng Y, Luo Y, Tong X, et al. Altered fecal microbiota composition associated with food allergy in infants. Applied & Environmental Microbiology. 2014; 80(8): 2546–54.

15. Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLOS BIOL. 2008; 6(11): e280. doi: 10.1371/journal.pbio.0060280 19018661

16. Zwielehner J, Liszt K, Handschur M, Lassl C, Lapin A, Haslberger AG. 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. 2009; 44(6): 440–6.

17. He T, Harmsen HJM, Raangs GC, Welling GW. Composition of Faecal Microbiota of Elderly People. Microbial Ecology in Health & Disease. 2003; 15(4): 153–9.

18. Woodmansey EJ. Intestinal bacteria and ageing. J APPL MICROBIOL. 2010; 102(5): 1178–86.

19. Harri MK, Kirsti T, Soile T, Lars P, Nina R. The effect of age and non-steroidal anti-inflammatory drugs on human intestinal microbiota composition. Br J Nutr. 2010; 103(2): 227–34. doi: 10.1017/S0007114509991553 19703328

20. Zhang C, Zheng HT, Du XB, Zhang L, Zhu TX, Chen JC. Initial studies between food compositions of Bama’s health macrobian and bifidobacteria in human intestinal tract. Food Sci China. 1994; 177(47–9.

21. Komai M, Nanno M, Nakazawa Y, Hosono A. Intestinal microflora and longevity. Functions of Fermented Milk Challenges for the Health Sciences. 1992.

22. Susanne M, Katiana S, Christiana H, Elisabeth N, Livia A, Tore M, et al. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol. 2006; 72(2): 1027–33. doi: 10.1128/AEM.72.2.1027-1033.2006 16461645

23. Smith P, Willemsen D, Popkes M, Metge F, Gandiwa E, Reichard M, et al. Regulation of life span by the gut microbiota in the short-lived African turquoise killifish. eLife,6,(2017-07-13). 2017; 6(e27014. doi: 10.7554/eLife.27014 28826469

24. Bian G, Gloor GB, Gong A, Jia C, Zhang W, Hu J, et al. The Gut Microbiota of Healthy Aged Chinese Is Similar to That of the Healthy Young. MSPHERE. 2017; 2(5): e317–27.

25. Drago L, Toscano M, Rodighiero V, De VE, Mogna G. Cultivable and pyrosequenced fecal microflora in centenarians and young subjects. J CLIN GASTROENTEROL. 2012; 46(9): S81.

26. Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD. PANDAseq: paired-end assembler for illumina sequences. BMC BIOINFORMATICS. 2012; 13(1): 31.

27. Bolger AM, Marc L, Bjoern U. Trimmomatic: a flexible trimmer for Illumina sequence data. BIOINFORMATICS. 2014; 30(15): 2114–20. doi: 10.1093/bioinformatics/btu170 24695404

28. Westcott SL, Schloss PD. De novo clustering methods outperform reference-based methods for assigning 16S rRNA gene sequences to operational taxonomic units. PEERJ. 2015; 3(12): e1487.

29. Tibshirani R. Regression Shrinkage and Selection via the Lasso. Journal of the Royal Statistical Society. 1996; 58(1): 267–88.

30. Tiihonen K, Ouwehand AC, Rautonen N. Human intestinal microbiota and healthy ageing. AGEING RES REV. 2010; 9(2): 107–16. doi: 10.1016/j.arr.2009.10.004 19874918

31. Nam YD, Jung MJ, Roh SW, Kim MS, Bae JW. Comparative analysis of Korean human gut microbiota by barcoded pyrosequencing. PLOS ONE. 2011; 6(7): e22109. doi: 10.1371/journal.pone.0022109 21829445

32. Kim KA, Jung IH, Park SH, Ahn YT, Huh CS, Kim DH. Comparative Analysis of the Gut Microbiota in People with Different Levels of Ginsenoside Rb1 Degradation to Compound K. PLOS ONE. 2013; 8(4): e62409. doi: 10.1371/journal.pone.0062409 23638073

33. Greenhalgh K, Meyer KM, Aagaard KM, Wilmes P. The human gut microbiome in health: establishment and resilience of microbiota over a lifetime. ENVIRON MICROBIOL. 2016; 18(7): 2103–16. doi: 10.1111/1462-2920.13318 27059297

34. Kong F, Hua Y, Zeng B, Ning R, Li Y, Zhao J. Gut microbiota signatures of longevity. CURR BIOL. 2016; 26(18): R832–3. doi: 10.1016/j.cub.2016.08.015 27676296

35. Wang F, Yu T, Huang G, Cai D, Liang X, Su H, et al. Gut microbiota community and its assembly associated with age and diet in Chinese centenarians. J Microbiol Biotechnol. 2015; 25(8): 1195. doi: 10.4014/jmb.1410.10014 25839332

36. Suau A, Bonnet R, Sutren M, Godon JJ, Gibson GR, Collins MD, et al. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Applied & Environmental Microbiology. 1999; 65(11): 4799–807.

37. Hopkins MJ, Macfarlane GT. Changes in predominant bacterial populations in human faeces with age and with Clostridium difficile infection. J MED MICROBIOL. 2002; 51(5): 448–54. doi: 10.1099/0022-1317-51-5-448 11990498

38. Woodmansey EJ, Mcmurdo MET, Macfarlane GT, Sandra M. Comparison of compositions and metabolic activities of fecal microbiotas in young adults and in antibiotic-treated and non-antibiotic-treated elderly subjects. Appl Environ Microbiol. 2004; 70(10): 6113–22. doi: 10.1128/AEM.70.10.6113-6122.2004 15466557

39. Dzierżewicz Z, Szczerba J, Glarz LJMA, Tkowska LZJM, Jasinska D, Wilczok T. Intraspecies variability of Desulfovibrio desulfuricans strains determined by the genetic profiles. FEMS MICROBIOL LETT. 2010; 219(1): 69–74.

40. Biagi E, Franceschi C, Rampelli S, Severgnini M, Ostan R, Turroni S, et al. Gut Microbiota and Extreme Longevity. CURR BIOL. 2016; 26(11): 1480–5. doi: 10.1016/j.cub.2016.04.016 27185560

41. Louis P, Duncan SH, McCrae SI, Millar J, Jackson MS, Flint HJ. Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J BACTERIOL. 2004; 186(7): 2099–106. doi: 10.1128/JB.186.7.2099-2106.2004 15028695

42. Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandezgarayzabal J, Garcia P, et al. The Phylogeny of the Genus Clostridium: Proposal of Five New Genera and Eleven New Species Combinations. Int J Syst Bacteriol. 1994; 44(4): 812–26. doi: 10.1099/00207713-44-4-812 7981107

43. Lupton JR. Microbial degradation products influence colon cancer risk: the butyrate controversy. The Journal of nutrition. 2004; 134(2): 479–82. doi: 10.1093/jn/134.2.479 14747692

44. Salonen A, Lahti L, Salojärvi J, Holtrop G, Korpela K, Duncan SH, et al. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. ISME J. 2014; 8(11): 2218–30. doi: 10.1038/ismej.2014.63 24763370

45. Park SH, Kim KA, Ahn YT, Jeong JJ, Huh CS, Kim DH. Comparative analysis of gut microbiota in elderly people of urbanized towns and longevity villages. BMC MICROBIOL. 2015; 15(1): 49.

46. Wong JM, De SR, Kendall CW, Emam A, Jenkins DJ. Colonic health: fermentation and short chain fatty acids. J CLIN GASTROENTEROL. 2006; 40(3): 235–43. doi: 10.1097/00004836-200603000-00015 16633129

47. Duncan S, Louis PH. Cultivable bacterial diversity from the human colon. LETT APPL MICROBIOL. 2010; 44(4): 343–50.

48. Ottaviani E, Ventura N, Mandrioli M, Candela M, Franchini A, Franceschi C. Gut microbiota as a candidate for lifespan extension: an ecological/evolutionary perspective targeted on living organisms as metaorganisms. BIOGERONTOLOGY. 2011; 12(6): 599–609. doi: 10.1007/s10522-011-9352-5 21814818


Článek vyšel v časopise

PLOS One


2019 Číslo 10