Individual-specific changes in the human gut microbiota after challenge with enterotoxigenic Escherichia coli and subsequent ciprofloxacin treatment

Mihai Pop; Joseph N. Paulson; Subhra Chakraborty; Irina Astrovskaya; Brianna R. Lindsay; Shan Li; Héctor Corrada Bravo; Clayton Harro; Julian Parkhill; Alan W. Walker; Richard I.  Walker; David A. Sack; O. Colin Stine

doi:10.1186/s12864-016-2777-0

Individual-specific changes in the human gut microbiota after challenge with enterotoxigenic Escherichia coli and subsequent ciprofloxacin treatment

Mihai Pop
, Joseph N. Paulson
, Subhra Chakraborty
, Irina Astrovskaya
, Brianna R. Lindsay
, Shan Li
, Héctor Corrada Bravo
, Clayton Harro
, Julian Parkhill
, Alan W. Walker
, Richard I. Walker
, David A. Sack
, O. Colin Stine

The Rowett Institute of Nutrition and Health

University of Maryland, College Park
Dana-Farber Cancer Institute
Harvard School of Public Health, Boston, Massachusetts, USA
Johns Hopkins Bloomberg School of Public Health
Merck
Wellcome Sanger Institute
PATH

Research output: Contribution to journal › Article › peer-review

57 Citations (Scopus)

17 Downloads (Pure)

Abstract

Background
Enterotoxigenic Escherichia coli (ETEC) is a major cause of diarrhea in inhabitants from low-income countries and in visitors to these countries. The impact of the human intestinal microbiota on the initiation and progression of ETEC diarrhea is not yet well understood.

Results
We used 16S rRNA (ribosomal RNA) gene sequencing to study changes in the fecal microbiota of 12 volunteers during a human challenge study with ETEC (H10407) and subsequent treatment with ciprofloxacin.

Five subjects developed severe diarrhea and seven experienced few or no symptoms. Diarrheal symptoms were associated with high concentrations of fecal E. coli as measured by quantitative culture, quantitative PCR, and normalized number of 16S rRNA gene sequences. Large changes in other members of the microbiota varied greatly from individual to individual, whether or not diarrhea occurred. Nonetheless the variation within an individual was small compared to variation between individuals. Ciprofloxacin treatment reorganized microbiota populations; however, the original structure was largely restored at one and three month follow-up visits.

Conclusion
Symptomatic ETEC infections, but not asymptomatic infections, were associated with high fecal concentrations of E. coli. Both infection and ciprofloxacin treatment caused variable changes in other bacteria that generally reverted to baseline levels after three months.

Original language	English
Article number	440
Pages (from-to)	1-11
Number of pages	11
Journal	BMC Genomics
Volume	17
DOIs	https://doi.org/10.1186/s12864-016-2777-0
Publication status	Published - 8 Jun 2016

Bibliographical note

Acknowledgements

The authors wish to thank Mark Stares, Richard Rance, and other members of the Wellcome Trust Sanger Institute’s 454 sequencing team for generating the 16S rRNA gene data. Lili Fox Vélez provided editorial support.

Funding

IA, JNP, and MP were partly supported by the NIH, grants R01-AI-100947 to MP, and R21-GM-107683 to Matthias Chung, subcontract to MP. JNP was partly supported by an NSF graduate fellowship number DGE750616. IA, JNP, BRL, OCS and MP were supported in part by the Bill and Melinda Gates Foundation, award number 42917 to OCS. JP and AWW received core funding support from The Wellcome Trust (grant number 098051). AWW, and the Rowett Institute of Nutrition and Health, University of Aberdeen, receive core funding support from the Scottish Government Rural and Environmental Science and Analysis Service (RESAS).

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Keywords

diarrhea
enterotoxigenic Escherichia coli
16S rRNA gene survey
microbiota
antibiotic treatment

Access to Document

10.1186/s12864-016-2777-0Licence: CC BY

Individual-specific changes in the human gut microbiota after challenge with enterotoxigenic Escherichia coli and subsequent ciprofloxacin treatment
This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Final published version, 3.62 MBLicence: CC BY

Cite this

Pop, M., Paulson, J. N., Chakraborty, S., Astrovskaya, I., Lindsay, B. R., Li, S., Corrada Bravo, H., Harro, C., Parkhill, J., Walker, A. W., Walker, R. I., Sack, D. A., & Stine, O. C. (2016). Individual-specific changes in the human gut microbiota after challenge with enterotoxigenic Escherichia coli and subsequent ciprofloxacin treatment. BMC Genomics, 17, 1-11. Article 440. https://doi.org/10.1186/s12864-016-2777-0

Pop, M, Paulson, JN, Chakraborty, S, Astrovskaya, I, Lindsay, BR, Li, S, Corrada Bravo, H, Harro, C, Parkhill, J, Walker, AW, Walker, RI, Sack, DA & Stine, OC 2016, 'Individual-specific changes in the human gut microbiota after challenge with enterotoxigenic Escherichia coli and subsequent ciprofloxacin treatment', BMC Genomics, vol. 17, 440, pp. 1-11. https://doi.org/10.1186/s12864-016-2777-0

@article{7af7575903ec456a830c0463241699d9,

title = "Individual-specific changes in the human gut microbiota after challenge with enterotoxigenic Escherichia coli and subsequent ciprofloxacin treatment",

abstract = "Background Enterotoxigenic Escherichia coli (ETEC) is a major cause of diarrhea in inhabitants from low-income countries and in visitors to these countries. The impact of the human intestinal microbiota on the initiation and progression of ETEC diarrhea is not yet well understood. Results We used 16S rRNA (ribosomal RNA) gene sequencing to study changes in the fecal microbiota of 12 volunteers during a human challenge study with ETEC (H10407) and subsequent treatment with ciprofloxacin. Five subjects developed severe diarrhea and seven experienced few or no symptoms. Diarrheal symptoms were associated with high concentrations of fecal E. coli as measured by quantitative culture, quantitative PCR, and normalized number of 16S rRNA gene sequences. Large changes in other members of the microbiota varied greatly from individual to individual, whether or not diarrhea occurred. Nonetheless the variation within an individual was small compared to variation between individuals. Ciprofloxacin treatment reorganized microbiota populations; however, the original structure was largely restored at one and three month follow-up visits. Conclusion Symptomatic ETEC infections, but not asymptomatic infections, were associated with high fecal concentrations of E. coli. Both infection and ciprofloxacin treatment caused variable changes in other bacteria that generally reverted to baseline levels after three months.",

keywords = "diarrhea, enterotoxigenic Escherichia coli, 16S rRNA gene survey, microbiota, antibiotic treatment",

author = "Mihai Pop and Paulson, \{Joseph N.\} and Subhra Chakraborty and Irina Astrovskaya and Lindsay, \{Brianna R.\} and Shan Li and \{Corrada Bravo\}, H{\'e}ctor and Clayton Harro and Julian Parkhill and Walker, \{Alan W.\} and Walker, \{Richard I.\} and Sack, \{David A.\} and Stine, \{O. Colin\}",

note = "Acknowledgements The authors wish to thank Mark Stares, Richard Rance, and other members of the Wellcome Trust Sanger Institute{\textquoteright}s 454 sequencing team for generating the 16S rRNA gene data. Lili Fox V{\'e}lez provided editorial support. Funding IA, JNP, and MP were partly supported by the NIH, grants R01-AI-100947 to MP, and R21-GM-107683 to Matthias Chung, subcontract to MP. JNP was partly supported by an NSF graduate fellowship number DGE750616. IA, JNP, BRL, OCS and MP were supported in part by the Bill and Melinda Gates Foundation, award number 42917 to OCS. JP and AWW received core funding support from The Wellcome Trust (grant number 098051). AWW, and the Rowett Institute of Nutrition and Health, University of Aberdeen, receive core funding support from the Scottish Government Rural and Environmental Science and Analysis Service (RESAS).",

year = "2016",

month = jun,

day = "8",

doi = "10.1186/s12864-016-2777-0",

language = "English",

volume = "17",

pages = "1--11",

journal = "BMC Genomics",

issn = "1471-2164",

publisher = "BioMed Central",

}

TY - JOUR

T1 - Individual-specific changes in the human gut microbiota after challenge with enterotoxigenic Escherichia coli and subsequent ciprofloxacin treatment

AU - Pop, Mihai

AU - Paulson, Joseph N.

AU - Chakraborty, Subhra

AU - Astrovskaya, Irina

AU - Lindsay, Brianna R.

AU - Li, Shan

AU - Corrada Bravo, Héctor

AU - Harro, Clayton

AU - Parkhill, Julian

AU - Walker, Alan W.

AU - Walker, Richard I.

AU - Sack, David A.

AU - Stine, O. Colin

N1 - Acknowledgements The authors wish to thank Mark Stares, Richard Rance, and other members of the Wellcome Trust Sanger Institute’s 454 sequencing team for generating the 16S rRNA gene data. Lili Fox Vélez provided editorial support. Funding IA, JNP, and MP were partly supported by the NIH, grants R01-AI-100947 to MP, and R21-GM-107683 to Matthias Chung, subcontract to MP. JNP was partly supported by an NSF graduate fellowship number DGE750616. IA, JNP, BRL, OCS and MP were supported in part by the Bill and Melinda Gates Foundation, award number 42917 to OCS. JP and AWW received core funding support from The Wellcome Trust (grant number 098051). AWW, and the Rowett Institute of Nutrition and Health, University of Aberdeen, receive core funding support from the Scottish Government Rural and Environmental Science and Analysis Service (RESAS).

PY - 2016/6/8

Y1 - 2016/6/8

N2 - Background Enterotoxigenic Escherichia coli (ETEC) is a major cause of diarrhea in inhabitants from low-income countries and in visitors to these countries. The impact of the human intestinal microbiota on the initiation and progression of ETEC diarrhea is not yet well understood. Results We used 16S rRNA (ribosomal RNA) gene sequencing to study changes in the fecal microbiota of 12 volunteers during a human challenge study with ETEC (H10407) and subsequent treatment with ciprofloxacin. Five subjects developed severe diarrhea and seven experienced few or no symptoms. Diarrheal symptoms were associated with high concentrations of fecal E. coli as measured by quantitative culture, quantitative PCR, and normalized number of 16S rRNA gene sequences. Large changes in other members of the microbiota varied greatly from individual to individual, whether or not diarrhea occurred. Nonetheless the variation within an individual was small compared to variation between individuals. Ciprofloxacin treatment reorganized microbiota populations; however, the original structure was largely restored at one and three month follow-up visits. Conclusion Symptomatic ETEC infections, but not asymptomatic infections, were associated with high fecal concentrations of E. coli. Both infection and ciprofloxacin treatment caused variable changes in other bacteria that generally reverted to baseline levels after three months.

AB - Background Enterotoxigenic Escherichia coli (ETEC) is a major cause of diarrhea in inhabitants from low-income countries and in visitors to these countries. The impact of the human intestinal microbiota on the initiation and progression of ETEC diarrhea is not yet well understood. Results We used 16S rRNA (ribosomal RNA) gene sequencing to study changes in the fecal microbiota of 12 volunteers during a human challenge study with ETEC (H10407) and subsequent treatment with ciprofloxacin. Five subjects developed severe diarrhea and seven experienced few or no symptoms. Diarrheal symptoms were associated with high concentrations of fecal E. coli as measured by quantitative culture, quantitative PCR, and normalized number of 16S rRNA gene sequences. Large changes in other members of the microbiota varied greatly from individual to individual, whether or not diarrhea occurred. Nonetheless the variation within an individual was small compared to variation between individuals. Ciprofloxacin treatment reorganized microbiota populations; however, the original structure was largely restored at one and three month follow-up visits. Conclusion Symptomatic ETEC infections, but not asymptomatic infections, were associated with high fecal concentrations of E. coli. Both infection and ciprofloxacin treatment caused variable changes in other bacteria that generally reverted to baseline levels after three months.

KW - diarrhea

KW - enterotoxigenic Escherichia coli

KW - 16S rRNA gene survey

KW - microbiota

KW - antibiotic treatment

U2 - 10.1186/s12864-016-2777-0

DO - 10.1186/s12864-016-2777-0

M3 - Article

SN - 1471-2164

VL - 17

SP - 1

EP - 11

JO - BMC Genomics

JF - BMC Genomics

M1 - 440

ER -

Individual-specific changes in the human gut microbiota after challenge with enterotoxigenic Escherichia coli and subsequent ciprofloxacin treatment

Abstract

Bibliographical note

UN SDGs

Keywords

Access to Document

Fingerprint

Cite this