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Composition, variability, and temporal stability of the intestinal microbiota of the elderly

Marcus J. Claesson, Siobhán Cusack, Orla O'Sullivan, Rachel Greene-Diniz, Heleen de Weerd, Edel Flannery, Julian R. Marchesi, Daniel Falush, Timothy Dinan, Gerald Fitzgerald, Catherine Stanton, Douwe van Sinderen, Michael O'Connor, Norma Harnedy, Kieran O'Connor, Colm Henry, Denis O'Mahony, Anthony P. Fitzgerald, Fergus Shanahan, Cillian Twomey, Colin Hill, R. Paul Ross and Paul W. O'Toole
PNAS March 15, 2011. 108 (Supplement 1) 4586-4591; published ahead of print June 22, 2010. https://doi.org/10.1073/pnas.1000097107
Marcus J. Claesson
aDepartment of Microbiology, University College, Cork, Ireland;bAlimentary Pharmabiotic Centre, University College, Cork, Ireland;
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Siobhán Cusack
aDepartment of Microbiology, University College, Cork, Ireland;
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Orla O'Sullivan
cTeagasc, Moorepark Food Research Centre, Moorepark, Fermoy, County Cork, Ireland;
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Rachel Greene-Diniz
aDepartment of Microbiology, University College, Cork, Ireland;
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Heleen de Weerd
dWageningen University and Research Centre for Plant Breeding, 6708 PB, Wageningen, The Netherlands;
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Edel Flannery
eDepartment of Statistics, University College, Cork, Ireland;
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Julian R. Marchesi
bAlimentary Pharmabiotic Centre, University College, Cork, Ireland;fSchool of Biosciences, Cardiff University, Cardiff CF10 3AT, United Kingdom;
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Daniel Falush
gEnvironmental Research Institute, University College, Cork, Ireland;
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Timothy Dinan
bAlimentary Pharmabiotic Centre, University College, Cork, Ireland;hDepartment of Psychiatry, University College, Cork, Ireland;
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Gerald Fitzgerald
aDepartment of Microbiology, University College, Cork, Ireland;bAlimentary Pharmabiotic Centre, University College, Cork, Ireland;
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Catherine Stanton
bAlimentary Pharmabiotic Centre, University College, Cork, Ireland;cTeagasc, Moorepark Food Research Centre, Moorepark, Fermoy, County Cork, Ireland;
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Douwe van Sinderen
aDepartment of Microbiology, University College, Cork, Ireland;bAlimentary Pharmabiotic Centre, University College, Cork, Ireland;
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Michael O'Connor
iCork University Hospital, Wilton, Cork, Ireland;jSt. Finbarr's Hospital, Cork, Ireland;
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Norma Harnedy
iCork University Hospital, Wilton, Cork, Ireland;jSt. Finbarr's Hospital, Cork, Ireland;
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Kieran O'Connor
jSt. Finbarr's Hospital, Cork, Ireland;kMercy University Hospital, Cork, Ireland;lSouth Infirmary, Victoria University Hospital, Cork, Ireland;
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Colm Henry
kMercy University Hospital, Cork, Ireland;lSouth Infirmary, Victoria University Hospital, Cork, Ireland;
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Denis O'Mahony
iCork University Hospital, Wilton, Cork, Ireland;jSt. Finbarr's Hospital, Cork, Ireland;mDepartment of Medicine, University College, Cork, Ireland; and
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Anthony P. Fitzgerald
eDepartment of Statistics, University College, Cork, Ireland;nDepartment of Epidemiology and Public Health, University College, Cork, Ireland
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Fergus Shanahan
bAlimentary Pharmabiotic Centre, University College, Cork, Ireland;mDepartment of Medicine, University College, Cork, Ireland; and
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Cillian Twomey
iCork University Hospital, Wilton, Cork, Ireland;jSt. Finbarr's Hospital, Cork, Ireland;mDepartment of Medicine, University College, Cork, Ireland; and
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Colin Hill
aDepartment of Microbiology, University College, Cork, Ireland;bAlimentary Pharmabiotic Centre, University College, Cork, Ireland;
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R. Paul Ross
bAlimentary Pharmabiotic Centre, University College, Cork, Ireland;cTeagasc, Moorepark Food Research Centre, Moorepark, Fermoy, County Cork, Ireland;
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Paul W. O'Toole
aDepartment of Microbiology, University College, Cork, Ireland;bAlimentary Pharmabiotic Centre, University College, Cork, Ireland;
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  • For correspondence: pwotoole@ucc.ie
  1. Edited by Jeffrey I. Gordon, Washington University School of Medicine, St. Louis, MO, and approved June 1, 2010 (received for review February 5, 2010)

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Abstract

Alterations in the human intestinal microbiota are linked to conditions including inflammatory bowel disease, irritable bowel syndrome, and obesity. The microbiota also undergoes substantial changes at the extremes of life, in infants and older people, the ramifications of which are still being explored. We applied pyrosequencing of over 40,000 16S rRNA gene V4 region amplicons per subject to characterize the fecal microbiota in 161 subjects aged 65 y and older and 9 younger control subjects. The microbiota of each individual subject constituted a unique profile that was separable from all others. In 68% of the individuals, the microbiota was dominated by phylum Bacteroides, with an average proportion of 57% across all 161 baseline samples. Phylum Firmicutes had an average proportion of 40%. The proportions of some phyla and genera associated with disease or health also varied dramatically, including Proteobacteria, Actinobacteria, and Faecalibacteria. The core microbiota of elderly subjects was distinct from that previously established for younger adults, with a greater proportion of Bacteroides spp. and distinct abundance patterns of Clostridium groups. Analyses of 26 fecal microbiota datasets from 3-month follow-up samples indicated that in 85% of the subjects, the microbiota composition was more like the corresponding time-0 sample than any other dataset. We conclude that the fecal microbiota of the elderly shows temporal stability over limited time in the majority of subjects but is characterized by unusual phylum proportions and extreme variability.

  • etagenomics
  • gerontology
  • inflammation
  • Faecalibacterium
  • Firmicutes

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: pwotoole{at}ucc.ie.
  • Author contributions: J.R.M., T.D., G.F., C.S., D.v.S., D.O., A.P.F., F.S., C. Hill, R.P.R., and P.W.O. designed research; M.J.C., S.C., O.O., R.G.-D., E.F., M.O., N.H., K.O., C. Henry, D.O., A.P.F., and C.T. performed research; H.d.W., M.O., N.H., K.O., C. Henry, D.O., and C.T. contributed new reagents/analytic tools; M.J.C., S.C., O.O., R.G.-D., H.d.W., J.R.M., D.F., T.D., A.P.F., F.S., C.T., C. Hill, R.P.R., and P.W.O. analyzed data; and M.J.C., S.C., J.R.M., G.F., C.S., D.v.S., F.S., C. Hill, R.P.R., and P.W.O. wrote the paper.

  • The authors declare no conflict of interest.

  • This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “Microbes and Health” held November 2–3, 2009, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, CA. The complete program and audio files of most presentations are available on the NAS Web site at http://www.nasonline.org/SACKLER_Microbes_and_Health.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequence data reported in this paper have been deposited in the National Center for Biotechnology Information Short Read Archive (accession no. SRA021022).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1000097107/-/DCSupplemental.

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Composition, variability, and temporal stability of the intestinal microbiota of the elderly
Marcus J. Claesson, Siobhán Cusack, Orla O'Sullivan, Rachel Greene-Diniz, Heleen de Weerd, Edel Flannery, Julian R. Marchesi, Daniel Falush, Timothy Dinan, Gerald Fitzgerald, Catherine Stanton, Douwe van Sinderen, Michael O'Connor, Norma Harnedy, Kieran O'Connor, Colm Henry, Denis O'Mahony, Anthony P. Fitzgerald, Fergus Shanahan, Cillian Twomey, Colin Hill, R. Paul Ross, Paul W. O'Toole
Proceedings of the National Academy of Sciences Mar 2011, 108 (Supplement 1) 4586-4591; DOI: 10.1073/pnas.1000097107

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Composition, variability, and temporal stability of the intestinal microbiota of the elderly
Marcus J. Claesson, Siobhán Cusack, Orla O'Sullivan, Rachel Greene-Diniz, Heleen de Weerd, Edel Flannery, Julian R. Marchesi, Daniel Falush, Timothy Dinan, Gerald Fitzgerald, Catherine Stanton, Douwe van Sinderen, Michael O'Connor, Norma Harnedy, Kieran O'Connor, Colm Henry, Denis O'Mahony, Anthony P. Fitzgerald, Fergus Shanahan, Cillian Twomey, Colin Hill, R. Paul Ross, Paul W. O'Toole
Proceedings of the National Academy of Sciences Mar 2011, 108 (Supplement 1) 4586-4591; DOI: 10.1073/pnas.1000097107
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