Abstract
The influence of gender and obesity on the abundance of human colonic Feacalibacterium prausnitzii is currently unclear. We collected fecal samples from 54 obese and 54 sex- and age-matched normal-weight Chinese adults and quantified the fecal F. prausnitzii as percentage of 16S rRNA gene copies of F. prausnitzii accounting to that of total gut bacteria with quantitative PCR. The fecal F. prausnitzii amount was not significantly different between obese and lean subjects. Men possessed significantly lower level of fecal F. prausnitzii than women, and the significant and positive correlation of fecal F. prausnitzii quantity with fasting glucose level was observed in men, not in women. Our results suggest that the gender effect, in addition to other factors including the geographic location, ethnicity, diet and gut transit times of study subjects, has to be considered when studying the relationship between gut F. prausnitzii and diseases.
References
Aguirre de Carcer D, Cuiv PO, Wang T, Kang S, Worthley D, Whitehall V, Gordon I, McSweeney C, Leggett B, Morrison M (2011) Numerical ecology validates a biogeographical distribution and gender-based effect on mucosa-associated bacteria along the human colon. ISME J 5(5):801–809
Ahmed S, Macfarlane GT, Fite A, McBain AJ, Gilbert P, Macfarlane S (2007) Mucosa-associated bacterial diversity in relation to human terminal ileum and colonic biopsy samples. Appl Environ Microbiol 73(22):7435–7442
Balamurugan R, George G, Kabeerdoss J, Hepsiba J, Chandragunasekaran AM, Ramakrishna BS (2010) Quantitative differences in intestinal Faecalibacterium prausnitzii in obese Indian children. Br J Nutr 103(3):335–338
Basu R, Dalla Man C, Campioni M, Basu A, Klee G, Toffolo G, Cobelli C, Rizza RA (2006) Effects of age and sex on postprandial glucose metabolism: differences in glucose turnover, insulin secretion, insulin action, and hepatic insulin extraction. Diabetes 55(7):2001–2014
Benus RF, van der Werf TS, Welling GW, Judd PA, Taylor MA, Harmsen HJ, Whelan K (2010) Association between Faecalibacterium prausnitzii and dietary fibre in colonic fermentation in healthy human subjects. Br J Nutr 104(5):693–700
Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmee E, Cousin B, Sulpice T, Chamontin B, Ferrieres J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56(7):1761–1772
De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P (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(33):14691–14696
Degen LP, Phillips SF (1996) Variability of gastrointestinal transit in healthy women and men. Gut 39(2):299–305
Ding S, Lund PK (2011) Role of intestinal inflammation as an early event in obesity and insulin resistance. Curr Opin Clin Nutr Metab Care 14(4):328–333
Duncan SH, Hold GL, Harmsen HJ, Stewart CS, Flint HJ (2002) Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as F. prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol 52(Pt 6):2141–2146
Fleischman A, Shoelson SE, Bernier R, Goldfine AB (2008) Salsalate improves glycemia and inflammatory parameters in obese young adults. Diabetes Care 31(2):289–294
Furet JP, Kong LC, Tap J, Poitou C, Basdevant A, Bouillot JL, Mariat D, Corthier G, Dore J, Henegar C, Rizkalla S, Clement K (2010) Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 59(12):3049–3057
Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, Cefalu WT, Ye J (2009) Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 58(7):1509–1517
Hold GL, Schwiertz A, Aminov RI, Blaut M, Flint HJ (2003) Oligonucleotide probes that detect quantitatively significant groups of butyrate-producing bacteria in human feces. Appl Environ Microbiol 69(7):4320–4324
Jumpertz R, Le DS, Turnbaugh PJ, Trinidad C, Bogardus C, Gordon JI, Krakoff J (2011) Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am J Clin Nutr 94(1):58–65
Kashyap PC, Marcobal A, Ursell LK, Larauche M, Duboc H, Earle KA, Sonnenburg ED, Ferreyra JA, Higginbottom SK, Million M, Tache Y, Pasricha PJ, Knight R, Farrugia G, Sonnenburg JL (2013) Complex interactions among diet, gastrointestinal transit, and gut microbiota in humanized mice. Gastroenterology 144(5):967–977
Khan MT, Duncan SH, Stams AJ, van Dijl JM, Flint HJ, Harmsen HJ (2012) The gut anaerobe Faecalibacterium prausnitzii uses an extracellular electron shuttle to grow at oxic-anoxic interphases. ISME J 6(8):1578–1585
Li M, Wang B, Zhang M, Rantalainen M, Wang S, Zhou H, Zhang Y, Shen J, Pang X, Wei H, Chen Y, Lu H, Zuo J, Su M, Qiu Y, Jia W, Xiao C, Smith LM, Yang S, Holmes E, Tang H, Zhao G, Nicholson JK, Li L, Zhao L (2008) Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci USA 105(6):2117–2122
Liebman M, Propst K, Moore SA, Pelican S, Holmes B, Wardlaw MK, Melcher LM, Harker JC, Dennee PM, Dunnagan T (2003) Gender differences in selected dietary intakes and eating behaviors in rural communities in Wyoming, Montana, and Idaho. Nutr Res 23(8):991–1002
Lopez-Siles M, Khan TM, Duncan SH, Harmsen HJ, Garcia-Gil LJ, Flint HJ (2012) Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and host-derived substrates for growth. Appl Environ Microbiol 78(2):420–428
Mueller S, Saunier K, Hanisch C, Norin E, Alm L, Midtvedt T, Cresci A, Silvi S, Orpianesi C, Verdenelli MC, Clavel T, Koebnick C, Zunft HJ, Dore J, Blaut M (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(2):1027–1033
Must A, Dallal GE, Dietz WH (1991) Reference data for obesity: 85th and 95th percentiles of body mass index (wt/ht2) and triceps skinfold thickness. Am J Clin Nutr 53(4):839–846
Payne AN, Chassard C, Zimmermann M, Müller P, Stinca S, Lacroix C (2011) The metabolic activity of gut microbiota in obese children is increased compared with normal-weight children and exhibits more exhaustive substrate utilization. Nutr Diabetes 1(7):e12
Ramirez-Farias C, Slezak K, Fuller Z, Duncan A, Holtrop G, Louis P (2009) Effect of inulin on the human gut microbiota: stimulation of bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br J Nutr 101(4):541–550
Regitz-Zagrosek V, Lehmkuhl E, Mahmoodzadeh S (2007) Gender aspects of the role of the metabolic syndrome as a risk factor for cardiovascular disease. Gend Med 4 Suppl B:S162–177
Ruan H, Pownall HJ, Lodish HF (2003) Troglitazone antagonizes tumor necrosis factor-alpha-induced reprogramming of adipocyte gene expression by inhibiting the transcriptional regulatory functions of NF-kappaB. J Biol Chem 278(30):28181–28192
Sarwer DB, Dilks RJ, West-Smith L (2011) Dietary intake and eating behavior after bariatric surgery: threats to weight loss maintenance and strategies for success. Surg Obes Relat Dis 7(5):644–651
Shen J, Zhang B, Wei G, Pang X, Wei H, Li M, Zhang Y, Jia W, Zhao L (2006) Molecular profiling of the clostridium leptum subgroup in human fecal microflora by PCR-denaturing gradient gel electrophoresis and clone library analysis. Appl Environ Microbiol 72(8):5232–5238
Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, Grangette C, Vasquez N, Pochart P, Trugnan G, Thomas G, Blottiere HM, Dore J, Marteau P, Seksik P, Langella P (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of crohn disease patients. Proc Natl Acad Sci USA 105(43):16731–16736
Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, Brown D, Stares MD, Scott P, Bergerat A, Louis P, McIntosh F, Johnstone AM, Lobley GE, Parkhill J, Flint HJ (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J 5(2):220–230
Wang RF, Cao WW, Cerniglia CE (1996) Phylogenetic analysis of Fusobacterium prausnitzii based upon the 16S rRNA gene sequence and PCR confirmation. Int J Syst Bacteriol 46(1):341–343
Woo J, Ho SC, Sham A, Sea MM, Lam KS, Lam TH, Janus ED (2003) Diet and glucose tolerance in a Chinese population. Eur J Clin Nutr 57(4):523–530
Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334(6052):105–108
Zoetendal EG, von Wright A, Vilpponen-Salmela T, Ben-Amor K, Akkermans AD, de Vos WM (2002) Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl Environ Microbiol 68(7):3401–3407
Acknowledgments
This work was supported by a Grant from the National Natural Science Foundation of China (81100632).
Conflict of interest
The authors declare no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Jie Feng and Huang Tang have contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Feng, J., Tang, H., Li, M. et al. The abundance of fecal Faecalibacterium prausnitzii in relation to obesity and gender in Chinese adults. Arch Microbiol 196, 73–77 (2014). https://doi.org/10.1007/s00203-013-0942-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-013-0942-2