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Membership and Behavior of Ultra-Low-Diversity Pathogen Communities Present in the Gut of Humans during Prolonged Critical Illness
Open accessAbstract
UNLABELLED: 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. IMPORTANCE: During critical illness, the normal gut microbiota becomes disrupted in response to host physiologic stress and antibiotic treatment. Here we demonstrate that the community structure of the gut microbiota during prolonged critical illness is dramatically changed such that in many cases only two-member pathogen communities remain. Most of these ultra-low-membership communities display low virulence when grouped together (i.e., a commensal lifestyle); individually, however, they can express highly harmful behaviors (i.e., a pathogenic lifestyle). The commensal lifestyle of the whole community can be shifted to a pathogenic one in response to host factors such as opioids that are released during physiologic stress and critical illness. This shift can be prevented by using compounds such as Pi-PEG15-20 that interrupt bacterial virulence expression. Taking the data together, this report characterizes the plasticity seen with respect to the choice between a commensal lifestyle and a pathogenic lifestyle among ultra-low-diversity pathogen communities that predominate in the gut during critical illness and offers novel strategies for prevention of sepsis.
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“The lower gastrointestinal tract, which in healthy people contains hundreds of distinct bacterial species, loses diversity, and the community is overrun by a few (in some cases only one) bacterial species.”
From The microbiome and critical illness (2016) · cites this paper as [20]
In the citing paper
“Dominant species include S aureus, Enterococcus spp, and members of the Enterobacteriaceae family (including E coli and Klebsiella spp).”
From The microbiome and critical illness (2016) · cites this paper as [20]
In the citing paper
“In studies of the gut microbiome in critically ill patients, butyrate-producing bacteria are uncommon or absent,20,69–71 and butyrate production is at a minimum.”
From The microbiome and critical illness (2016) · cites this paper as [20]
In the citing paper
“P aeruginosa, which is normally low in abundance, grows in prominence.”
From The microbiome and critical illness (2016) · cites this paper as [20]
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“normally rare fungi, such as Candida spp, bloom and thrive;20 culture-based detection of candidaemia is a marker of disease severity and predictive of a poor outcome.”
From The microbiome and critical illness (2016) · cites this paper as [20]
In the citing paper
“The virulence of pathogens familiar in intensive care is promoted by conditions of nutrient scarcity, competition from neighbouring community members, disruption of stabilising commensal relationships,20 and exposure to the mediators of the host stress response”
From The microbiome and critical illness (2016) · cites this paper as [20]
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Metadata
- Authors
- Zaborin, A., Smith, D., Garfield, K., Quensen, J., Shakhsheer, B., Kade, M., Tirrell, M., Tiedje, J., Gilbert, J. A., Zaborina, O., & Alverdy, J. C.
- Affiliations
- University of Chicago (US)
- Argonne National Laboratory (US)
- Michigan State University (US)
- Corresponding author
- Zaborina, Olga
- Alverdy, John C.
- ORCID
- Venue
- mBio
- Publisher
- American Society for Microbiology
- Published
- 2014-10-31
- Volume
- 5
- Issue
- 5
- Pages
- e01361-14
- ISSN
- 2150-7511 (ISSN-L)
- 2161-2129
- PMC
- PMC4173762
- OpenAlex
- W2112208246
- Cited by
- 367
- References
- 42
- Citations by year
- 2026: 32 · 2025: 31 · 2024: 19 · 2023: 36 · 2022: 40 · 2021: 30 · 2020: 39 · 2019: 31 · 2018: 34 · 2017: 34 · 2016: 28 · 2015: 12 · 2014: 1
- FWCI
- 10.19
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- mBio (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by-nc-sa)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- Funders
- National Institutes of Health (UL1TR000430)
- National Institute of General Medical Sciences (R01 2R01GM062344-13A1, R01GM062344)
- National Center for Advancing Translational Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
- Health Sciences › Medicine › Microbiology (medical) › Antibiotic Resistance in Bacteria
- Keywords
- gut microbiota, critical illness, intensive care unit patients, multidrug resistance, Enterococcus, Staphylococcus, Enterobacteriaceae, Candida albicans, Candida glabrata, commensalism, fungal-bacterial interactions, anti-virulence agents, nutrient deprivation
- MeSH terms
- Animals, Anti-Bacterial Agents, Candida albicans, Enterobacteriaceae, Feces, Humans, Intensive Care Units, RNA, Ribosomal, 16S, Staphylococcus, Critical Illness, Enterococcus, Caenorhabditis elegans, Sepsis, Gene Expression Profiling, Drug Resistance, Bacterial, Drug Resistance, Fungal, Virulence Factors, Gastrointestinal Tract, Microbiota
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