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Article ; Online: The gut microbiome: a missing link in understanding the gastrointestinal manifestations of COVID-19?

Brooks, Erin F / Bhatt, Ami S

Cold Spring Harbor molecular case studies

2021 Volume 7, Issue 2

Abstract: Coronavirus disease 2019 (COVID-19), which is caused by infection with SARS-CoV-2, presents with a broad constellation of both respiratory and nonrespiratory symptoms, although it is primarily considered a respiratory disease. Gastrointestinal symptoms- ... ...

Abstract	Coronavirus disease 2019 (COVID-19), which is caused by infection with SARS-CoV-2, presents with a broad constellation of both respiratory and nonrespiratory symptoms, although it is primarily considered a respiratory disease. Gastrointestinal symptoms-including nausea, abdominal pain, vomiting, and diarrhea-rank chief among these. When coupled with the presence of viral RNA in fecal samples, the presence of gastrointestinal symptoms raises relevant questions regarding whether SARS-CoV-2 can productively infect the upper or lower gastrointestinal tract. Despite the well-documented prevalence of gastrointestinal symptoms and the high rate of SARS-CoV-2 fecal RNA shedding, the biological, clinical, and epidemiological relevance of these findings is unclear. Furthermore, the isolation of replication-competent virus from fecal samples has not been reproducibly and rigorously demonstrated. Although SARS-CoV-2 shedding likely occurs in a high proportion of patients, gastrointestinal symptoms affect only a subset of individuals. Herein, we summarize what is known about gastrointestinal symptoms and fecal viral shedding in COVID-19, explore the role of the gut microbiome in other respiratory diseases, speculate on the role of the gut microbiota in COVID-19, and discuss potential future directions. Taking these concepts together, we propose that studying gut microbiota perturbations in COVID-19 will enhance our understanding of the symptomology and pathophysiology of this novel devastating disease.
MeSH term(s)	Abdominal Pain/diagnosis ; Abdominal Pain/etiology ; Abdominal Pain/microbiology ; Abdominal Pain/pathology ; Animals ; COVID-19/complications ; COVID-19/diagnosis ; COVID-19/microbiology ; COVID-19/pathology ; Diarrhea/diagnosis ; Diarrhea/etiology ; Diarrhea/microbiology ; Diarrhea/pathology ; Feces/microbiology ; Feces/virology ; Gastrointestinal Microbiome ; Humans ; Nausea/diagnosis ; Nausea/etiology ; Nausea/microbiology ; Nausea/pathology ; SARS-CoV-2/isolation & purification ; Vomiting/diagnosis ; Vomiting/etiology ; Vomiting/microbiology ; Vomiting/pathology
Language	English
Publishing date	2021-04-08
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	2835759-0
ISSN	2373-2873 ; 2373-2873
ISSN (online)	2373-2873
ISSN	2373-2873
DOI	10.1101/mcs.a006031
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Rare transmission of commensal and pathogenic bacteria in the gut microbiome of hospitalized adults.

Siranosian, Benjamin A / Brooks, Erin F / Andermann, Tessa / Rezvani, Andrew R / Banaei, Niaz / Tang, Hua / Bhatt, Ami S

Nature communications

2022 Volume 13, Issue 1, Page(s) 586

Abstract: Bacterial bloodstream infections are a major cause of morbidity and mortality among patients undergoing hematopoietic cell transplantation (HCT). Although previous research has demonstrated that pathogens may translocate from the gut microbiome into the ... ...

Abstract	Bacterial bloodstream infections are a major cause of morbidity and mortality among patients undergoing hematopoietic cell transplantation (HCT). Although previous research has demonstrated that pathogens may translocate from the gut microbiome into the bloodstream to cause infections, the mechanisms by which HCT patients acquire pathogens in their microbiome have not yet been described. Here, we use linked-read and short-read metagenomic sequencing to analyze 401 stool samples collected from 149 adults undergoing HCT and hospitalized in the same unit over three years, many of whom were roommates. We use metagenomic assembly and strain-specific comparison methods to search for high-identity bacterial strains, which may indicate transmission between the gut microbiomes of patients. Overall, the microbiomes of patients who share time and space in the hospital do not converge in taxonomic composition. However, we do observe six pairs of patients who harbor identical or nearly identical strains of the pathogen Enterococcus faecium, or the gut commensals Akkermansia muciniphila and Hungatella hathewayi. These shared strains may result from direct transmission between patients who shared a room and bathroom, acquisition from a common hospital source, or transmission from an unsampled intermediate. We also identify multiple patients with identical strains of species commonly found in commercial probiotics, including Lactobacillus rhamnosus and Streptococcus thermophilus. In summary, our findings indicate that sharing of identical pathogens between the gut microbiomes of multiple patients is a rare phenomenon. Furthermore, the observed potential transmission of commensal, immunomodulatory microbes suggests that exposure to other humans may contribute to microbiome reassembly post-HCT.
MeSH term(s)	Adult ; Aged ; Anti-Bacterial Agents/pharmacology ; Bacteria/metabolism ; Bacterial Infections/transmission ; Cross Infection/microbiology ; Cross Infection/transmission ; Drug Resistance, Microbial/drug effects ; Drug Resistance, Microbial/genetics ; Enterococcus faecium/drug effects ; Enterococcus faecium/isolation & purification ; Escherichia coli/drug effects ; Escherichia coli/isolation & purification ; Female ; Gastrointestinal Microbiome/drug effects ; Hematopoietic Stem Cell Transplantation ; Hospitalization ; Hospitals ; Humans ; Length of Stay ; Male ; Metagenome/genetics ; Metagenomics ; Middle Aged ; Phylogeny ; Probiotics ; Sequence Analysis, DNA ; Time Factors
Chemical Substances	Anti-Bacterial Agents
Language	English
Publishing date	2022-01-31
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, U.S. Gov't, P.H.S.
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-022-28048-7
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Article: Intragenic DNA inversions expand bacterial coding capacity.

Chanin, Rachael B / West, Patrick T / Park, Ryan M / Wirbel, Jakob / Green, Gabriella Z M / Miklos, Arjun M / Gill, Matthew O / Hickey, Angela S / Brooks, Erin F / Bhatt, Ami S

bioRxiv : the preprint server for biology

2023

Abstract: Bacterial populations that originate from a single bacterium are not strictly clonal. Often, they contain subgroups with distinct phenotypes. Bacteria can generate heterogeneity through phase variation: a preprogrammed, reversible mechanism that alters ... ...

Abstract	Bacterial populations that originate from a single bacterium are not strictly clonal. Often, they contain subgroups with distinct phenotypes. Bacteria can generate heterogeneity through phase variation: a preprogrammed, reversible mechanism that alters gene expression levels across a population. One well studied type of phase variation involves enzyme-mediated inversion of specific intergenic regions of genomic DNA. Frequently, these DNA inversions flip the orientation of promoters, turning ON or OFF adjacent coding regions within otherwise isogenic populations. Through this mechanism, inversion can affect fitness, survival, or group dynamics. Here, we develop and apply bioinformatic approaches to discover thousands of previously undescribed phase-variable regions in prokaryotes using long-read datasets. We identify 'intragenic invertons', a surprising new class of invertible elements found entirely within genes, in bacteria and archaea. To date, inversions within single genes have not been described. Intragenic invertons allow a gene to encode two or more versions of a protein by flipping a DNA sequence within the coding region, thereby increasing coding capacity without increasing genome size. We experimentally characterize specific intragenic invertons in the gut commensal
Language	English
Publishing date	2023-09-16
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.03.11.532203
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Article ; Online: A pedagogical approach to science outreach.

McClure, Marni B / Hall, Kacey C / Brooks, Erin F / Allen, Catherine T / Lyle, Kenneth S

PLoS biology

2020 Volume 18, Issue 4, Page(s) e3000650

Abstract: Encouragement of students across all communities through scientific outreach programs is critical to engaging the next generation, exciting young minds to pursue careers in science and medicine. Herein, we present a uniquely structured and widely ... ...

Abstract	Encouragement of students across all communities through scientific outreach programs is critical to engaging the next generation, exciting young minds to pursue careers in science and medicine. Herein, we present a uniquely structured and widely influential science outreach program. Founded in 2005, the Duke Chemistry Outreach (DCO) employs a pedagogical approach to outreach that aims to teach its audience a new scientific concept, while instilling a pure enjoyment of science. DCO has performed 583 events reaching over 70,000 participants throughout 2,270 hours, with the majority of events in Durham, the surrounding North Carolinian communities, and across 8 other states. The flexibility and diversity of this outreach program creates a framework amendable for others to adopt in both secondary and higher education settings.
MeSH term(s)	Chemistry/education ; Community-Institutional Relations/economics ; Humans ; North Carolina ; Research Personnel ; Science/education ; Students ; Universities
Language	English
Publishing date	2020-04-16
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2126776-5
ISSN	1545-7885 ; 1544-9173
ISSN (online)	1545-7885
ISSN	1544-9173
DOI	10.1371/journal.pbio.3000650
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Article ; Online: Near-fatal Legionella pneumonia in a neonate linked to home humidifier by metagenomic next generation sequencing.

West, Patrick T / Brooks, Erin F / Costales, Cristina / Moreno, Angel / Jensen, Tanner Dean / Budvytiene, Indre / Khan, Aslam / Pham, Trung H M / Schwenk, Hayden T / Bhatt, Ami S / Banaei, Niaz

Med (New York, N.Y.)

2022 Volume 3, Issue 8, Page(s) 565–567

MeSH term(s)	High-Throughput Nucleotide Sequencing ; Humans ; Humidifiers ; Infant, Newborn ; Legionella pneumophila/genetics ; Legionnaires' Disease/diagnosis ; Pneumonia
Language	English
Publishing date	2022-07-20
Publishing country	United States
Document type	Letter
ISSN	2666-6340
ISSN (online)	2666-6340
DOI	10.1016/j.medj.2022.06.004
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Article ; Online: Publisher Correction: Standardized preservation, extraction and quantification techniques for detection of fecal SARS-CoV-2 RNA.

Natarajan, Aravind / Han, Alvin / Zlitni, Soumaya / Brooks, Erin F / Vance, Summer E / Wolfe, Marlene / Singh, Upinder / Jagannathan, Prasanna / Pinsky, Benjamin A / Boehm, Alexandria / Bhatt, Ami S

Nature communications

2021 Volume 12, Issue 1, Page(s) 7100

Language	English
Publishing date	2021-12-01
Publishing country	England
Document type	Published Erratum
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-021-27392-4
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Article: Standardized and optimized preservation, extraction and quantification techniques for detection of fecal SARS-CoV-2 RNA.

Natarajan, Aravind / Han, Alvin / Zlitni, Soumaya / Brooks, Erin F / Vance, Summer E / Wolfe, Marlene / Singh, Upinder / Jagannathan, Prasanna / Pinsky, Benjamin A / Boehm, Alexandria / Bhatt, Ami S

medRxiv : the preprint server for health sciences

2021

Abstract: COVID-19 patients shed SARS-CoV-2 viral RNA in their stool, sometimes well after they have cleared their respiratory infection. This feature of the disease may be significant for patient health, epidemiology, and diagnosis. However, to date, methods to ... ...

Abstract	COVID-19 patients shed SARS-CoV-2 viral RNA in their stool, sometimes well after they have cleared their respiratory infection. This feature of the disease may be significant for patient health, epidemiology, and diagnosis. However, to date, methods to preserve stool samples from COVID patients, and to extract and quantify viral RNA concentration have yet to be optimized. We sought to meet this urgent need by developing and benchmarking a standardized protocol for the fecal detection of SARS-CoV-2 RNA. We test three preservative conditions for their ability to yield detectable SARS-CoV-2 RNA: OMNIgene-GUT, Zymo DNA/RNA shield kit, and the most common condition, storage without any preservative. We test these in combination with three extraction kits: the QIAamp Viral RNA Mini Kit, Zymo Quick-RNA Viral Kit, and MagMAX Viral/Pathogen Kit. Finally, we also test the utility of two detection methods, ddPCR and RT-qPCR, for the robust quantification of SARS-CoV-2 viral RNA from stool. We identify that the Zymo DNA/RNA shield collection kit and the QiaAMP viral RNA mini kit yield more detectable RNA than the others, using both ddPCR and RT-qPCR assays. We also demonstrate key features of experimental design including the incorporation of appropriate controls and data analysis, and apply these techniques to effectively extract viral RNA from fecal samples acquired from COVID-19 outpatients enrolled in a clinical trial.
Language	English
Publishing date	2021-04-17
Publishing country	United States
Document type	Preprint
DOI	10.1101/2021.04.10.21255250
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Article: Tomato brown rugose fruit virus Mo gene is a novel microbial source tracking marker.

Natarajan, Aravind / Fremin, Brayon J / Schmidtke, Danica T / Wolfe, Marlene K / Zlitni, Soumaya / Graham, Katherine E / Brooks, Erin F / Severyn, Christopher J / Sakamoto, Kathleen M / Lacayo, Norman J / Kuersten, Scott / Koble, Jeff / Caves, Glorianna / Kaplan, Inna / Singh, Upinder / Jagannathan, Prasanna / Rezvani, Andrew R / Bhatt, Ami S / Boehm, Alexandria B

bioRxiv : the preprint server for biology

2023

Abstract: Microbial source tracking (MST) identifies sources of fecal contamination in the environment using fecal host-associated markers. While there are numerous bacterial MST markers, there are few viral markers. Here we design and test novel viral MST markers ...

Abstract	Microbial source tracking (MST) identifies sources of fecal contamination in the environment using fecal host-associated markers. While there are numerous bacterial MST markers, there are few viral markers. Here we design and test novel viral MST markers based on tomato brown rugose fruit virus (ToBRFV) genomes. We assembled eight nearly complete genomes of ToBRFV from wastewater and stool samples from the San Francisco Bay Area in the United States of America. Next, we developed two novel probe-based RT-PCR assays based on conserved regions of the ToBRFV genome, and tested the markersâ€™ sensitivities and specificities using human and non-human animal stool as well as wastewater. TheToBRFV markers are sensitive and specific; in human stool and wastewater, they are more prevalent and abundant than a currently used marker, the pepper mild mottle virus (PMMoV) coat protein (CP) gene. We applied the assays to detect fecal contamination in urban stormwater samples and found that the ToBRFV markers matched cross-assembly phage (crAssphage), an established viral MST marker, in prevalence across samples. Taken together, ToBRFV is a promising viral human-associated MST marker. Importance: Human exposure to fecal contamination in the environment can cause transmission of infectious diseases. Microbial source tracking (MST) can identify sources of fecal contamination so that contamination can be remediated and human exposures can be reduced. MST requires the use of fecal host-associated MST markers. Here we design and test novel MST markers from genomes of tomato brown rugose fruit virus (ToBRFV). The markers are sensitive and specific to human stool, and highly abundant in human stool and wastewater samples.
Language	English
Publishing date	2023-01-10
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.01.09.523366
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Article ; Online: Standardized preservation, extraction and quantification techniques for detection of fecal SARS-CoV-2 RNA.

Natarajan, Aravind / Han, Alvin / Zlitni, Soumaya / Brooks, Erin F / Vance, Summer E / Wolfe, Marlene / Singh, Upinder / Jagannathan, Prasanna / Pinsky, Benjamin A / Boehm, Alexandria / Bhatt, Ami S

Nature communications

2021 Volume 12, Issue 1, Page(s) 5753

Abstract: Patients with COVID-19 shed SARS-CoV-2 RNA in stool, sometimes well after their respiratory infection has cleared. This may be significant for patient health, epidemiology, and diagnosis. However, methods to preserve stool, and to extract and quantify ... ...

Abstract	Patients with COVID-19 shed SARS-CoV-2 RNA in stool, sometimes well after their respiratory infection has cleared. This may be significant for patient health, epidemiology, and diagnosis. However, methods to preserve stool, and to extract and quantify viral RNA are not standardized. We test the performance of three preservative approaches at yielding detectable SARS-CoV-2 RNA: the OMNIgene-GUT kit, Zymo DNA/RNA shield kit, and the most commonly applied, storage without preservative. We test these in combination with three extraction kits: QIAamp Viral RNA Mini Kit, Zymo Quick-RNA Viral Kit, and MagMAX Viral/Pathogen Kit. We also test the utility of ddPCR and RT-qPCR for the reliable quantification of SARS-CoV-2 RNA from stool. We identify that the Zymo DNA/RNA preservative and the QiaAMP extraction kit yield more detectable RNA than the others, using both ddPCR and RT-qPCR. Taken together, we recommend a comprehensive methodology for preservation, extraction and detection of RNA from SARS-CoV-2 and other coronaviruses in stool.
MeSH term(s)	COVID-19/diagnosis ; COVID-19 Nucleic Acid Testing/standards ; Coronavirus Nucleocapsid Proteins/genetics ; Feces/virology ; Humans ; Phosphoproteins/genetics ; Preservation, Biological/standards ; RNA, Viral/analysis ; RNA, Viral/genetics ; Reagent Kits, Diagnostic ; Reference Standards ; SARS-CoV-2/genetics ; SARS-CoV-2/isolation & purification ; Specimen Handling/standards ; Viral Load/standards
Chemical Substances	Coronavirus Nucleocapsid Proteins ; Phosphoproteins ; RNA, Viral ; Reagent Kits, Diagnostic ; nucleocapsid phosphoprotein, SARS-CoV-2
Language	English
Publishing date	2021-10-01
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-021-25576-6
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Article ; Online: The Tomato Brown Rugose Fruit Virus Movement Protein Gene Is a Novel Microbial Source Tracking Marker.

Applied and environmental microbiology

2023 Volume 89, Issue 7, Page(s) e0058323

Abstract: Microbial source tracking (MST) identifies sources of fecal contamination in the environment using host-associated fecal markers. While there are numerous bacterial MST markers that can be used herein, there are few such viral markers. Here, we designed ... ...

Abstract	Microbial source tracking (MST) identifies sources of fecal contamination in the environment using host-associated fecal markers. While there are numerous bacterial MST markers that can be used herein, there are few such viral markers. Here, we designed and tested novel viral MST markers based on tomato brown rugose fruit virus (ToBRFV) genomes. We assembled eight nearly complete genomes of ToBRFV from wastewater and stool samples from the San Francisco Bay Area in the United States. Next, we developed two novel probe-based reverse transcription-PCR (RT-PCR) assays based on conserved regions of the ToBRFV genome and tested the markers' sensitivities and specificities using human and non-human animal stool as well as wastewater. The ToBRFV markers are sensitive and specific; in human stool and wastewater, they are more prevalent and abundant than a commonly used viral marker, the pepper mild mottle virus (PMMoV) coat protein (CP) gene. We used the assays to detect fecal contamination in urban stormwater samples and found that the ToBRFV markers matched cross-assembly phage (crAssphage), an established viral MST marker, in prevalence across samples. Taken together, these results indicate that ToBRFV is a promising viral human-associated MST marker.
MeSH term(s)	Animals ; Wastewater ; Solanum lycopersicum ; Fruit ; Biomarkers ; Feces/microbiology ; Environmental Monitoring/methods
Chemical Substances	Wastewater ; Biomarkers
Language	English
Publishing date	2023-07-05
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, P.H.S. ; Research Support, Non-U.S. Gov't
ZDB-ID	223011-2
ISSN	1098-5336 ; 0099-2240
ISSN (online)	1098-5336
ISSN	0099-2240
DOI	10.1128/aem.00583-23
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