Stool consistency is strongly associated with gut microbiota richness and composition, enterotypes and bacterial growth rates

Doris Vandeputte, Gwen Falony, Sara Vieira-Silva, Raul Y Tito, Marie Joossens, Jeroen Raes, Doris Vandeputte, Gwen Falony, Sara Vieira-Silva, Raul Y Tito, Marie Joossens, Jeroen Raes

Abstract

Objective: The assessment of potentially confounding factors affecting colon microbiota composition is essential to the identification of robust microbiome based disease markers. Here, we investigate the link between gut microbiota variation and stool consistency using Bristol Stool Scale classification, which reflects faecal water content and activity, and is considered a proxy for intestinal colon transit time.

Design: Through 16S rDNA Illumina profiling of faecal samples of 53 healthy women, we evaluated associations between microbiome richness, Bacteroidetes:Firmicutes ratio, enterotypes, and genus abundance with self-reported, Bristol Stool Scale-based stool consistency. Each sample's microbiota growth potential was calculated to test whether transit time acts as a selective force on gut bacterial growth rates.

Results: Stool consistency strongly correlates with all known major microbiome markers. It is negatively correlated with species richness, positively associated to the Bacteroidetes:Firmicutes ratio, and linked to Akkermansia and Methanobrevibacter abundance. Enterotypes are distinctly distributed over the BSS-scores. Based on the correlations between microbiota growth potential and stool consistency scores within both enterotypes, we hypothesise that accelerated transit contributes to colon ecosystem differentiation. While shorter transit times can be linked to increased abundance of fast growing species in Ruminococcaceae-Bacteroides samples, hinting to a washout avoidance strategy of faster replication, this trend is absent in Prevotella-enterotyped individuals. Within this enterotype adherence to host tissue therefore appears to be a more likely bacterial strategy to cope with washout.

Conclusions: The strength of the associations between stool consistency and species richness, enterotypes and community composition emphasises the crucial importance of stool consistency assessment in gut metagenome-wide association studies.

Keywords: INTESTINAL BACTERIA; INTESTINAL MICROBIOLOGY.

Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://www.bmj.com/company/products-services/rights-and-licensing/

Figures

Figure 1
Figure 1
Stool consistency variation drives species richness and human enterotypes. Correlation between (A) observed species richness and stool consistency, defined by Bristol Stool Scale (BSS) (Spearman's correlation, r=−0.45, p=0.0007) and (B) enterotype distribution and stool consistency (BSS); Blue: Ruminococcaceae-Bacteroides (RB) enterotype (r=−0.88, p=0.019), green: P enterotype (r=0.88, p=0.019).
Figure 2
Figure 2
Microbiota growth potential correlates to faster intestinal transit in the Ruminococcaceae-Bacteroides (RB) enterotype. Microbiota growth potential over stool consistency (Bristol Stool Scale (BSS)), which is proposed as a proxy for transit time, in the RB-enterotype (r=0.34, p=0.028).

References

    1. Qin J, Li R, Raes J, et al. . A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010;464:59–65. 10.1038/nature08821
    1. Gevers D, Knight R, Petrosino JF, et al. . The Human Microbiome Project: a community resource for the healthy human microbiome. PLoS Biol 2012;10:e1001377 10.1371/journal.pbio.1001377
    1. Costello EK, Lauber CL, Hamady M, et al. . Bacterial community variation in human body habitats across space and time. Science 2009;326:1694–7. 10.1126/science.1177486
    1. Brown J, de Vos WM, DiStefano PS, et al. . Translating the human microbiome. Nat Biotechnol 2013;31:304–8. 10.1038/nbt.2543
    1. Wu GD, Chen J, Hoffmann C, et al. . Linking long-term dietary patterns with gut microbial enterotypes. Science 2011;334:105–8. 10.1126/science.1208344
    1. David LA, Maurice CF, Carmody RN, et al. . Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014;505:559–63. 10.1038/nature12820
    1. Cho I, Yamanishi S, Cox L, et al. . Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 2012;488:621–6. 10.1038/nature11400
    1. Le Chatelier E, Nielsen T, Qin J, et al. . Richness of human gut microbiome correlates with metabolic markers. Nature 2013;500:541–6. 10.1038/nature12506
    1. Hildebrand F, Nguyen TLA, Brinkman B, et al. . Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome Biol 2013;14:R4 10.1186/gb-2013-14-1-r4
    1. Lewis SJ, Heaton KW. Stool form scale as a useful guide to intestinal transit time. Scand J Gastroenterol 1997;32:920–4. 10.3109/00365529709011203
    1. Heaton KW, Radvan J, Cripps H, et al. . Defecation frequency and timing, and stool form in the general population: a prospective study. Gut 1992;33:818–24. 10.1136/gut.33.6.818
    1. Degen LP, Phillips SF. How well does stool form reflect colonic transit? Gut 1996;39:109–13. 10.1136/gut.39.1.109
    1. Longstreth GF, Thompson WG, Chey WD, et al. . Functional Bowel Disorders. Gastroenterology 2006;130:1480–91. 10.1053/j.gastro.2005.11.061
    1. Videlock EJ, Cheng V, Cremonini F. Effects of linaclotide in patients with irritable bowel syndrome with constipation or chronic constipation: a meta-analysis. Clin Gastroenterol Hepatol 2013;11:1084–92. 10.1016/j.cgh.2013.04.032
    1. Collado Yurrita L, San Mauro Martín I, Ciudad-Cabañas MJ, et al. . Effectiveness of inulin intake on indicators of chronic constipation; a meta-analysis of controlled randomized clinical trials. Nutr Hosp 2014;30:244–52. 10.3305/nh.2014.30.2.7565
    1. Saad RJ, Rao SSC, Koch KL, et al. . Do stool form and frequency correlate with whole-gut and colonic transit? Results from a multicenter study in constipated individuals and healthy controls. Am J Gastroenterol 2010;105:403–11.10.1038/ajg.2009.612
    1. Schiraldi A, Fessas D, Signorelli M. Water activity in biological systems—a review. Polish J Food Nutr Sci 2012;62:5–13. 10.2478/v10222-011-0033-5
    1. Degen LP, Phillips SF. Variability of gastrointestinal transit in healthy women and men. Gut 1996;39:299–305. 10.1136/gut.39.2.299
    1. Godon JJ, Zumstein E, Dabert P, et al. . Molecular microbial diversity of an anaerobic digestor as determined by small-subunit rDNA sequence analysis. Appl Environ Microbiol 1997;63:2802–13.
    1. Aronesty E. Comparison of Sequencing Utility Programs. Open Bioinforma J 2013;7:1–8. 10.2174/1875036201307010001
    1. Maechler AM, Analysis DC, Struyf A. cluster: Cluster Analysis Basics and Extensions. R package version 1.14.4 2013.
    1. Holmes I, Harris K, Quince C. Dirichlet multinomial mixtures: generative models for microbial metagenomics. PLoS ONE 2012;7:e30126 10.1371/journal.pone.0030126
    1. Arumugam M, Raes J, Pelletier E, et al. . Enterotypes of the human gut microbiome. Nature 2011;473:174–80. 10.1038/nature09944
    1. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 2013;8:e61217 10.1371/journal.pone.0061217
    1. Vieira-Silva S, Rocha EPC. The systemic imprint of growth and its uses in ecological (meta)genomics. PLoS Genet 2010;6:e1000808 10.1371/journal.pgen.1000808
    1. Lozupone CA, Stombaugh JI, Gordon JI, et al. . Diversity, stability and resilience of the human gut microbiota. Nature 2012;489:220–30. 10.1038/nature11550
    1. Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet 2012;13:260–70. 10.1038/nrg3182
    1. Gorkiewicz G, Thallinger G, Trajanoski S. Alterations in the colonic microbiota in response to osmotic diarrhea. PLoS ONE 2013;8:e55817 10.1371/journal.pone.0055817
    1. Yatsunenko T, Rey FE, Manary MJ, et al. . Human gut microbiome viewed across age and geography. Nature 2012;486:222–7. 10.1038/nature11053
    1. Salonen A, de Vos WM. Impact of diet on human intestinal microbiota and health. Annu Rev Food Sci Technol 2014;5:239–62. 10.1146/annurev-food-030212-182554
    1. De Filippo C, Cavalieri D, Di Paola M, et al. . Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 2010;107:14691–6. 10.1073/pnas.1005963107
    1. Mudgil D, Barak S. Composition, properties and health benefits of indigestible carbohydrate polymers as dietary fiber: a review. Int J Biol Macromol 2013;61:1–6. 10.1016/j.ijbiomac.2013.06.044
    1. Sahakian AB, Jee S-R, Pimentel M. Methane and the gastrointestinal tract. Dig Dis Sci 2010;55:2135–43. 10.1007/s10620-009-1012-0
    1. Pimentel M, Lin HC, Enayati P, et al. . Methane, a gas produced by enteric bacteria, slows intestinal transit and augments small intestinal contractile activity. Am J Physiol Gastrointest Liver Physiol 2006;290:1089–95. 10.1152/ajpgi.00574.2004
    1. Flint H, Duncan S, Scott KP, et al. . Interactions and competition within the microbial community of the human colon: links between diet and health. Environ Microbiol 2007;9:1101–11. 10.1111/j.1462-2920.2007.01281.x
    1. Koch a L. Oligotrophs versus copiotrophs. Bioessays 2001;23:657–61. 10.1002/bies.1091
    1. James TW. Continous culture of microorganisms. Annu Rev Microbiol 1960:27–46.
    1. Hobson PN. Continuous culture of some anerobic and facultatively anaerobic rumen bacteria. J Gen Microbiol 1965;38:167–80. 10.1099/00221287-38-2-167
    1. Isaacson HR, Hinds FC, Bryant MP, et al. . Efficiency of energy utilization by mixed rumen bacteria in continuous culture. J Dairy Sci 1975;58:1645–59. 10.3168/jds.S0022-0302(75)84763-1
    1. Stephen a M, Wiggins HS, Cummings JH. Effect of changing transit time on colonic microbial metabolism in man. Gut 1987;28:601–9. 10.1136/gut.28.5.601
    1. Stephen M, Cummings JH. The microbial contribution to human fecal mass. J Med Microbiol 1980;13:45–56. 10.1099/00222615-13-1-45
    1. Grenier D. Collagen-binding activity of Prevotella intermedia measured by a microtitre plate adherence assay. Microbiology 1996;142:1537–41. 10.1099/13500872-142-6-1537
    1. Wright D, Rosendale D, Robertson A. Prevotella enzymes involved in mucin oligosaccharide degradation and evidence for a small operon of genes expressed during growth on mucin. FEMS Microbiol Lett 2000;190:73–9. 10.1111/j.1574-6968.2000.tb09265.x
    1. Santiago A, Panda S, Mengels G, et al. . Processing faecal samples: a step forward for standards in microbial community analysis. BMC Microbiol 2014;14:112 10.1186/1471-2180-14-112
    1. Scheperjans F, Aho V, Pereira P a. B, et al. . Gut microbiota are related to Parkinson's disease and clinical phenotype. Mov Disord 2014;30:350–8. 10.1002/mds.26069
    1. Kaye J, Gage H, Kimber A, et al. . Excess burden of constipation in Parkinson's disease: a pilot study. Mov Disord 2006;21:1270–3. 10.1002/mds.20942
    1. Agachan F, Chen T, Pfeifer J, et al. . A constipation scoring system to simplify evaluation and management of constipated patients. Dis Colon Rectum 1996;39:681–5. 10.1007/BF02056950
    1. Lewis SJ, Heaton KW. Increasing butyrate concentration in the distal colon by accelerating intestinal transit. Gut 1997;41:245–51. 10.1136/gut.41.2.245
    1. Lewis SJ, Heaton KW. The metabolic consequences of slow colonic transit. Am J Gastroenterol 1999;94:2010–16. 10.1111/j.1572-0241.1999.01271.x
    1. Burkitt D, Walker A, Painter N. Effect of dietary fibre on stools and transit times and its role in the causation of disease. Lancet 1972;300:1408–11. 10.1016/S0140-6736(72)92974-1

Source: PubMed

Patrocinadores y Colaboradores

Condiciones médicas

Intervenciones de drogas

3
Suscribir