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Title: Membership and Behavior of Ultra-Low-Diversity Pathogen Communities Present in the Gut of Humans during Prolonged Critical Illness

Abstract

We analyzed the 16S rRNA amplicon composition in fecal samples of selected patients during their prolonged stay in an intensive care unit (ICU) and observed the emergence of ultra-low-diversity communities (1 to 4 bacterial taxa) in 30% of the patients. Bacteria associated with the genera Enterococcus and Staphylococcus and the family Enterobacteriaceae comprised the majority of these communities. The composition of cultured species from stool samples correlated to the 16S rRNA analysis and additionally revealed the emergence of Candida albicans and Candida glabrata in ~75% of cases. Four of 14 ICU patients harbored 2-member pathogen communities consisting of one Candida taxon and one bacterial taxon. Bacterial members displayed a high degree of resistance to multiple antibiotics. The virulence potential of the 2-member communities was examined in C. elegans during nutrient deprivation and exposure to opioids in order to mimic local conditions in the gut during critical illness. Under conditions of nutrient deprivation, the bacterial members attenuated the virulence of fungal members, leading to a “commensal lifestyle.” However, exposure to opioids led to a breakdown in this commensalism in 2 of the ultra-low-diversity communities. Application of a novel antivirulence agent (phosphate-polyethylene glycol [Pi-PEG]) that creates local phosphate abundance prevented opioid-induced virulencemore » among these pathogen communities, thus rescuing the commensal lifestyle. To conclude, the gut microflora in critically ill patients can consist of ultra-low-diversity communities of multidrug-resistant pathogenic microbes. Local environmental conditions in gut may direct pathogen communities to adapt to either a commensal style or a pathogenic style.« less

Authors:
 [1];  [2];  [3];  [3];  [1];  [1];  [1];  [3];  [4];  [1];  [1]
+ Show Author Affiliations
  1. Univ. of Chicago, Chicago, Illinois, (United States)
  2. Argonne National Lab. (ANL), Argonne, IL (United States); Baylor College of Medicine, Houston, TX (United States)
  3. Michigan State Univ., East Lansing, Michigan, (United States)
  4. Univ. of Chicago, Chicago, Illinois, (United States); Argonne National Lab. (ANL), Argonne, IL (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); Argonne National Laboratory; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22), Materials Sciences and Engineering Division
OSTI Identifier:
1214650
Alternate Identifier(s):
OSTI ID: 1392642
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 5; Journal Issue: 5; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Zaborin, Alexander, Smith, Daniel, Garfield, Kevin, Quensen, John, Shakhsheer, Baddr, Kade, Matthew, Tirrell, Matthew, Tiedje, James, Gilbert, Jack A., Zaborina, Olga, and Alverdy, John C. Membership and Behavior of Ultra-Low-Diversity Pathogen Communities Present in the Gut of Humans during Prolonged Critical Illness. United States: N. p., 2014. Web. doi:10.1128/mBio.01361-14.
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Zaborin, Alexander, Smith, Daniel, Garfield, Kevin, Quensen, John, Shakhsheer, Baddr, Kade, Matthew, Tirrell, Matthew, Tiedje, James, Gilbert, Jack A., Zaborina, Olga, & Alverdy, John C. Membership and Behavior of Ultra-Low-Diversity Pathogen Communities Present in the Gut of Humans during Prolonged Critical Illness. United States. https://doi.org/10.1128/mBio.01361-14
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Zaborin, Alexander, Smith, Daniel, Garfield, Kevin, Quensen, John, Shakhsheer, Baddr, Kade, Matthew, Tirrell, Matthew, Tiedje, James, Gilbert, Jack A., Zaborina, Olga, and Alverdy, John C. Tue . "Membership and Behavior of Ultra-Low-Diversity Pathogen Communities Present in the Gut of Humans during Prolonged Critical Illness". United States. https://doi.org/10.1128/mBio.01361-14. https://www.osti.gov/servlets/purl/1214650.
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@article{osti_1214650,
title = {Membership and Behavior of Ultra-Low-Diversity Pathogen Communities Present in the Gut of Humans during Prolonged Critical Illness},
author = {Zaborin, Alexander and Smith, Daniel and Garfield, Kevin and Quensen, John and Shakhsheer, Baddr and Kade, Matthew and Tirrell, Matthew and Tiedje, James and Gilbert, Jack A. and Zaborina, Olga and Alverdy, John C.},
abstractNote = {We analyzed the 16S rRNA amplicon composition in fecal samples of selected patients during their prolonged stay in an intensive care unit (ICU) and observed the emergence of ultra-low-diversity communities (1 to 4 bacterial taxa) in 30% of the patients. Bacteria associated with the genera Enterococcus and Staphylococcus and the family Enterobacteriaceae comprised the majority of these communities. The composition of cultured species from stool samples correlated to the 16S rRNA analysis and additionally revealed the emergence of Candida albicans and Candida glabrata in ~75% of cases. Four of 14 ICU patients harbored 2-member pathogen communities consisting of one Candida taxon and one bacterial taxon. Bacterial members displayed a high degree of resistance to multiple antibiotics. The virulence potential of the 2-member communities was examined in C. elegans during nutrient deprivation and exposure to opioids in order to mimic local conditions in the gut during critical illness. Under conditions of nutrient deprivation, the bacterial members attenuated the virulence of fungal members, leading to a “commensal lifestyle.” However, exposure to opioids led to a breakdown in this commensalism in 2 of the ultra-low-diversity communities. Application of a novel antivirulence agent (phosphate-polyethylene glycol [Pi-PEG]) that creates local phosphate abundance prevented opioid-induced virulence among these pathogen communities, thus rescuing the commensal lifestyle. To conclude, the gut microflora in critically ill patients can consist of ultra-low-diversity communities of multidrug-resistant pathogenic microbes. Local environmental conditions in gut may direct pathogen communities to adapt to either a commensal style or a pathogenic style.},
doi = {10.1128/mBio.01361-14},
journal = {mBio (Online)},
number = 5,
volume = 5,
place = {United States},
year = {Tue Sep 23 00:00:00 EDT 2014},
month = {Tue Sep 23 00:00:00 EDT 2014}
}
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