Associations of fruit, whole grain, and total energy intakes with gut microbiome diversity and composition

Yixiao Wang; Keming Zhang; Linna Dai; Fengya Sun; Dan Wang; Sijia Meng; Jing Zhao; Yanfang Liu; Wanting Liu; Chunyan Li; Yuan Wang; Wenli Lu; Yun Zhu

doi:10.29219/fnr.v67.9725

Yixiao Wang Department of Epidemiology and Biostatistics, School of Public Health, Tianjin Medical University, Tianjin, China
Keming Zhang First Teaching Hospital of Tianjin University of Traditional Chinese Medicine, Tianjin, China
Linna Dai Department of Epidemiology and Biostatistics, School of Public Health, Tianjin Medical University, Tianjin, China
Fengya Sun Department of Epidemiology and Biostatistics, School of Public Health, Tianjin Medical University, Tianjin, China
Dan Wang Department of Epidemiology and Biostatistics, School of Public Health, Tianjin Medical University, Tianjin, China
Sijia Meng Department of Epidemiology and Biostatistics, School of Public Health, Tianjin Medical University, Tianjin, China
Jing Zhao Department of Epidemiology and Biostatistics, School of Public Health, Tianjin Medical University, Tianjin, China
Yanfang Liu Department of Epidemiology and Biostatistics, School of Public Health, Tianjin Medical University, Tianjin, China
Wanting Liu Department of Epidemiology and Biostatistics, School of Public Health, Tianjin Medical University, Tianjin, China
Chunyan Li Tianjin Nankai Hospital, Tianjin, China
Yuan Wang Department of Epidemiology and Biostatistics, School of Public Health, Tianjin Medical University, Tianjin, China
Wenli Lu Department of Epidemiology and Biostatistics, School of Public Health, Tianjin Medical University, Tianjin, China
Yun Zhu Department of Epidemiology and Biostatistics, School of Public Health, Tianjin Medical University, Tianjin, China

DOI: https://doi.org/10.29219/fnr.v67.9725

Keywords: gut microbiota, fruits, whole grains, total energy

Abstract

Background: The relationship between fruit, whole grain, and total energy consumption and the gut microbiome in the Chinese population remains unclear.

Objective: We investigated the relationship between intakes of fruits, whole grains, and energy, and the diversity and composition of gut microbiota.

Design: This cross-sectional study included 167 subjects aged 40-75 years who underwent colonoscopy at Nankai Hospital in Tianjin, China. Each of the participants completed a personal history questionnaire, a 7-day dietary record, and donated a fecal sample. The V3-V4 hypervariable region of the bacterial 16S rRNAgene was amplified and sequenced using Illumina Novaseq. The relationship between diet and gut microbiota was evaluated in terms of both the overall composition and the abundance of specific taxon.

Results: Fruits intake was positively related to the abundance of Bacilli, Porphyromonadaceae, Streptococcaceae, Parabacteroides, Streptococcus, and Bilophila in fecal samples. Higher whole grains intake was associated with higher microbial diversity, as measured by Shannon, Simpson, and Chao1 indices. Specifically, there was a significant increase inthe relative abundance of Lachnospiraceae and a decrease in Actinobacteria with increased whole grains intake. Moreover, higher intake of total energy was associated with a lower abundance of Anaerostipes and a higher abundance of Lactobacillales and Acidaminococcus.

Conclusion: Whole grains intake was positively associated with gut microbial diversity. Fruits and total energy intake were related to the abundance of specifictaxon (e.g., Bacilli and Acidaminococcus). These findings highlight the potential importance of dietary interventions for modulating gut microbiota composition and promoting overall health.

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References

1.
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality Worldwide for 36 cancers in 185 Countries. CA Cancer J Clin 2021; 71(3): 209–49. doi: 10.3322/caac.21660

2.
Simpson HL, Campbell BJ. Review article: dietary fibre- microbiota interactions. Aliment Pharmacol Ther 2015; 42(2): 158–79. doi:10.1111/apt.13248

3.
Bultman SJ. Interplay between diet, gut microbiota, epigenetic events, and colorectal cancer. Mol Nutr Food Res 2017; 61(1): 1–21. doi: 10.1002/mnfr.201500902

4.
Matsuoka K, Kanai T. The gut microbiota and inflammatory bowel disease. Semin Immunopathol 2015; 37(1): 47–55. doi: 10.1007/s00281-014-0454-4

5.
Liu BN, Liu XT, Liang ZH, Wang JH. Gut microbiota in obesity. World J Gastroenterol 2021; 27(25): 3837–50. doi: 10.3748/wjg.v27.i25.3837

6.
Han H, Li Y, Fang J, Liu G, Yin J, Li T, et al. Gut microbiota and type 1 Diabetes. Int J Mol Sci 2018; 19(4): 995. doi: 10.3390/ijms19040995

7.
Zhou Z, Sun B, Yu D, Zhu C. Gut microbiota: An important player in type 2 Diabetes Mellitus. Front Cell Infect Microbiol 2022; 12: 834485. doi: 10.3389/fcimb.2022.834485

8.
Mousa WK, Chehadeh F, Husband S. Microbial dysbiosis in the gut drives systemic autoimmune diseases. Front Immunol 2022; 13: 906258. doi: 10.3389/fimmu.2022.906258

9.
Bibbo S, Ianiro G, Giorgio V, Scaldaferri F, Masucci L, Gasbarrini A, et al. The role of diet on gut microbiota composition. Eur Rev Med Pharmacol Sci 2016; 20(22): 4742–49.

10.
Kataoka K. The intestinal microbiota and its role in human health and disease. J Med Invest 2016; 63(1–2): 27–37. doi: 10.2152/jmi.63.27

11.
Donati Zeppa S, Agostini D, Gervasi M, Annibalini G, Amatori S, Ferrini F, et al. Mutual interactions among exercise, sport supplements and microbiota. Nutrients 2019; 12(1): 17. doi: 10.3390/nu12010017

12.
Dreher ML. Whole fruits and fruit fiber emerging health effects. Nutrients 2018; 10(12): 1833. doi: 10.3390/nu10121833

13.
Foerster J, Maskarinec G, Reichardt N, Tett A, Narbad A, Blaut M, et al. The influence of whole grain products and red meat on intestinal microbiota composition in normal weight adults: a randomized crossover intervention trial. PLoS One 2014; 9(10): e109606. doi: 10.1371/journal.pone.0109606

14.
Markowiak P, Slizewska K. Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients 2017; 9(9): 1021. doi: 10.3390/nu9091021

15.
Wang Y, Qi W, Guo X, Song G, Pang S, Fang W, et al. Effects of oats, tartary buckwheat, and foxtail millet supplementation on lipid metabolism, oxido-inflammatory responses, gut microbiota, and colonic SCFA composition in High-Fat Diet Fed rats. Nutrients 2022; 14(14): 2760. doi: 10.3390/nu14132760

16.
P NPV. Joye IJ. Dietary fibre from whole grains and their benefits on metabolic health. Nutrients 2020; 12(10): 3045. doi: 10.3390/nu12103045

17.
Lattimer JM, Haub MD. Effects of dietary fiber and its components on metabolic health. Nutrients 2010; 2(12): 1266–89. doi: 10.3390/nu2121266

18.
Singh RK, Chang HW, Yan D, Lee KM, Ucmak D, Wong K, et al. Influence of diet on the gut microbiome and implications for human health. J Transl Med 2017; 15: 73. doi: 10.1186/s12967-017-1175-y

19.
Belcheva A, Irrazabal T, Robertson SJ, Streutker C, Maughan H, Rubino S, et al. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell 2014; 158(2): 288–99. doi: 10.1016/j.cell.2014.04.051

20.
Mingyang S, Chat AT, Sun J. Influence of the gut microbiome, diet, and environment on risk of colorectal cancer Gastroenterology 2020; 158(2): 322–40. doi: 10.1053/j.gastro.2019.06.048

21.
Lozupone CA, Hamady M, Kelley ST, Knight R. Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol. 2007; 73(5): 1576–85.

22.
Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005; 71(12): 8228–35.

23.
McArdle BH, Anderson MJ. Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology. 2001; 82(1): 290–7.

24.
Zhernakova A, Kurilshikov A, Bonder MJ, Tigchelaar EF, Schirmer M, Vatanen T, et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science 2016; 352: 565–9. doi: 10.1126/science.aad3369

25.
Fan J, Zhou Y, Meng R, Tang J, Zhu J, Aldrich MC, et al. Cross-talks between gut microbiota and tobacco smoking: a two-sample Mendelian randomization study. BMC Med 2023; 21(1): 163. doi: 10.1186/s12916-023-02863-1

26.
Bai X, Wei H, Liu W, Coker OO, Gou H, Liu C, et al. Cigarette smoke promotes colorectal cancer through modulation of gut microbiota and related metabolites. Gut 2022; 71(12): 2439–50. doi: 10.1136/gutjnl-2021-325021

27.
Kang JW, Tang X, Walton CJ, Brown MJ, Brewer RA, Maddela RL, et al. Multi-Omic analyses reveal bifidogenic effect and metabolomic shifts in healthy human cohort supplemented with a prebiotic dietary fiber blend. Front Nutr 2022; 9: 908534. doi: 10.3389/fnut.2022.908534

28.
Zhang Y, Chen H, Lu M, Cai J, Lu B, Luo C, et al. Habitual diet pattern associations with gut microbiome diversity and composition: results from a Chinese Adult Cohort. Nutrients 2022; 14(13): 2639. doi: 10.3390/nu14132639

29.
Um CY, Peters BA, Choi HS, Oberstein P, Beggs DB, Usyk M, et al. Grain, gluten, and dietary fiber intake influence gut microbial diversity: data from the food and microbiome longitudinal investigation. Cancer Res Commun 2023; 3(1): 43–53. doi: 10.1158/2767-9764.CRC-22-0154

30.
Zeyneb H, Pei H, Cao X, Wang Y, Win Y, Gong L. In vitro study of the effect of quinoa and quinoa polysaccharides on human gut microbiota. Food Sci Nutr 2021; 9(10): 5735–45. doi: 10.1002/fsn3.2540

31.
Li L, Houghton D, Lietz G, Watson A, Stewart CJ, Bal W, et al. Impact of daily consumption of whole-grain Quinoa-Enriched bread on gut microbiome in males. Nutrients 2022; 14(22): 4888. doi: 10.3390/nu14224888

32.
Vanegas SM, Meydani M, Barnett JB, Goldin B, Kane A, Rasmussen H, et al. Substituting whole grains for refined grains in a 6-wk randomized trial has a modest effect on gut microbiota and immune and inflammatory markers of healthy adults. Am J Clin Nutr 2017; 105(3): 635–50. doi: 10.3945/ajcn.116.146928

33.
Lewin GR, Carlos C, Chevrette MG, Horn HA, McDonald BR, Stankey RJ, et al. Evolution and ecology of actinobacteria and their bioenergy applications. Annu Rev Microbiol 2016; 70: 235–54. doi: 10.1146/annurev-micro-102215-095748

34.
Chao Z, Kejia M, Kai N, Minzi D, Weiwei L, Xing W, et al. Assessment of the safety and probiotic properties of Roseburia intestinalis: a potential ‘Next Generation Probiotic’. Frontiers in Microbiology 2022; 13: 973046. doi: 10.3389/fmicb.2022.973046

35.
Costabile A, Klinder A, Fava F, Napolitano A, Fogliano V, Leonard C, et al. Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study. Br J Nutr 2008; 99(1): 110–20. doi: 10.1017/S0007114507793923

36.
Christensen EG, Licht TR, Kristensen M, Bahl MI. Bifidogenic effect of whole-grain wheat during a 12-week energy-restricted dietary intervention in postmenopausal women. Eur J Clin Nutr 2013; 67(12): 1316–21. doi: 10.1038/ejcn.2013.207

37.
Carvalho-Wells AL, Helmolz K, Nodet C, Molzer C, Leonard C, McKevith B, et al. Determination of the in vivo prebiotic potential of a maize-based whole grain breakfast cereal: a human feeding study. Br J Nutr 2010; 104(9): 1353–56. doi: 10.1017/S0007114510002084

38.
Martinez I, Lattimer JM, Hubach KL, Case JA, Yang J, Weber CG, et al. Gut microbiome composition is linked to whole grain-induced immunological improvements. ISME J 2013; 7(2): 269–80. doi: 10.1038/ismej.2012.104

39.
Vitaglione P, Mennella I, Ferracane R, Rivellese AA, Giacco R, Ercolini D, et al. Whole-grain wheat consumption reduces inflammation in a randomized controlled trial on overweight and obese subjects with unhealthy dietary and lifestyle behaviors: role of polyphenols bound to cereal dietary fiber. Am J Clin Nutr 2015; 101(2): 251–61. doi: 10.3945/ajcn.114.088120

40.
Ampatzoglou A, Atwal KK, Maidens CM, Williams CL, Ross AB, Thielecke F, et al. Increased whole grain consumption does not affect blood biochemistry, body composition, or gut microbiology in healthy, low-habitual whole grain consumers. J Nutr 2015; 145(2): 215–21. doi: 10.3945/jn.114.202176

41.
Duenas M, Munoz-Gonzalez I, Cueva C, Jimenez-Giron A, Sanchez-Patan F, Santos-Buelga C, et al. A survey of modulation of gut microbiota by dietary polyphenols. Biomed Res Int 2015; 2015: 850902. doi: 10.1155/2015/850902

42.
Smith AH, Mackie RI. Effect of condensed tannins on bacterial diversity and metabolic activity in the rat gastrointestinal tract. Appl Environ Microbiol 2004; 70(2): 1104–15. doi: 10.1128/AEM.70.2.1104-1115.2004

43.
Smith-Brown P, Morrison M, Krause L, Davies PS. Dairy and plant based food intakes are associated with altered faecal microbiota in 2 to 3 year old Australian children. Sci Rep 2016; 6: 32385. doi: 10.1038/srep32385

44.
Cani PD. The colon matters in blood sugar management: how prebiotic fibers can work in gut microbiota, glucose metabolism and metabolic disorders. Ann Nutr Metabol 2017; 71: 132–3.

45.
Borgonovi TF, Virgolin LB, Janzantti NS, Casarotti SN, Penna ALB. Fruit bioactive compounds: effect on lactic acid bacteria and on intestinal microbiota. Food Res Int 2022; 161: 111809. doi: 10.1016/j.foodres.2022.111809

46.
Unno T, Tanaka H, Kohara A. Consumption of young barley leaf extract increases fecal short-chain fatty acid levels: a before-after clinical trial. Food Res 2020; 4(4): 1151–5.

47.
Chun-Han L, Raaj SM, Long HN, Yiqing W, Wenjie M, Kai W, et al. 802 empirical dietary pattern associated with short-chain fatty acid-producing bacteria in relation to colorectal cancer risk. Gastroenterology 2021; 160(6): S165–66. doi: 10.1016/S0016-5085(21)01147-1

48.
Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008; 3: 213–23. doi: 10.1016/j.chom.2008.02.015

49.
Niu Z, Wu L, Kang J, Bai J, Chen Y, Xia H. Regulation of sleep disorders in patients with traumatic brain injury by intestinal flora based on the background of brain-gut axis&#13. Frontiers in Neuroscience 2022; 16: 934822. doi: 10.3389/fnins.2022.934822

50.
Hamada K, Isobe J, Hattori K, Hosonuma M, Baba Y, Murayama M, et al. Turicibacter and acidaminococcus predict immune-related adverse events and efficacy of immune checkpoint inhibitor. Front Immunol 2023; 14: 1164724. doi: 10.3389/fimmu.2023.1164724

51.
Qin Z, Mu HW, Ling DY, Jing WJ, Jun WY, Ping J. Dysbiosis of gut microbiota and decreased propionic acid associated with metabolic abnormality in Cushing’s syndrome&#13. Front Endocrinol 2023; 13: 1095438. doi: 10.3389/fendo.2022.1095438

52.
Muralidharan J, Moreno-Indias I, Bullo M, Lopez JV, Corella D, Castaner O, et al. Effect on gut microbiota of a 1-y lifestyle intervention with Mediterranean diet compared with energy-reduced Mediterranean diet and physical activity promotion: PREDIMED-Plus Study. Am J Clin Nutr 2021; 114(3): 1148–58. doi: 10.1093/ajcn/nqab150

53.
Zhu S, Han M, Liu S, Fan L, Shi H, Li P. Composition and diverse differences of intestinal microbiota in ulcerative colitis patients. Front Cell Infect Microbiol 2022; 12: 953962. doi: 10.3389/fcimb.2022.953962

54.
Tang B, Hu Y, Chen J, Su C, Zhang Q, Huang C. Oral and fecal microbiota in patients with diarrheal irritable bowel syndrome. Heliyon 2023; 9(1): e13114. doi: 10.1016/j.heliyon.2023.e13114

55.
Lin P, Li D, Shi Y, Li Q, Guo X, Dong K, et al. Dysbiosis of the Gut Microbiota and Kynurenine (Kyn) pathway activity as potential biomarkers in patients with major depressive disorder. Nutrients 2023; 15(7): 1752. doi: 10.3390/nu15071752