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Gut microbiota and age shape susceptibility to clostridial enteritis in lorikeets under human care

BACKGROUND: Enteritis is a common cause of morbidity and mortality in lorikeets that can be challenging to diagnose and treat. In this study, we examine gut microbiota in two lorikeet flocks with enteritis (Columbus Zoo and Aquarium—CZA; Denver Zoo—DZ). Since 2012, the CZA flock has experienced repe...

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Autores principales: Minich, David, Madden, Christopher, Navarro, Mauricio A., Glowacki, Leo, French-Kim, Kristen, Chan, Willow, Evans, Morgan V., Soares, Kilmer, Mrofchak, Ryan, Madan, Rushil, Ballash, Gregory A., LaPerle, Krista, Paul, Subhadeep, Vodovotz, Yael, Uzal, Francisco A., Martinez, Margaret, Hausmann, Jennifer, Junge, Randall E., Hale, Vanessa L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8744333/
https://www.ncbi.nlm.nih.gov/pubmed/35000619
http://dx.doi.org/10.1186/s42523-021-00148-7
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author Minich, David
Madden, Christopher
Navarro, Mauricio A.
Glowacki, Leo
French-Kim, Kristen
Chan, Willow
Evans, Morgan V.
Soares, Kilmer
Mrofchak, Ryan
Madan, Rushil
Ballash, Gregory A.
LaPerle, Krista
Paul, Subhadeep
Vodovotz, Yael
Uzal, Francisco A.
Martinez, Margaret
Hausmann, Jennifer
Junge, Randall E.
Hale, Vanessa L.
author_facet Minich, David
Madden, Christopher
Navarro, Mauricio A.
Glowacki, Leo
French-Kim, Kristen
Chan, Willow
Evans, Morgan V.
Soares, Kilmer
Mrofchak, Ryan
Madan, Rushil
Ballash, Gregory A.
LaPerle, Krista
Paul, Subhadeep
Vodovotz, Yael
Uzal, Francisco A.
Martinez, Margaret
Hausmann, Jennifer
Junge, Randall E.
Hale, Vanessa L.
author_sort Minich, David
collection PubMed
description BACKGROUND: Enteritis is a common cause of morbidity and mortality in lorikeets that can be challenging to diagnose and treat. In this study, we examine gut microbiota in two lorikeet flocks with enteritis (Columbus Zoo and Aquarium—CZA; Denver Zoo—DZ). Since 2012, the CZA flock has experienced repeated outbreaks of enteritis despite extensive diet, husbandry, and clinical modifications. In 2018, both CZA and DZ observed a spike in enteritis. Recent research has revealed that the gut microbiota can influence susceptibility to enteropathogens. We hypothesized that a dysbiosis, or alteration in the gut microbial community, was making some lorikeets more susceptible to enteritis, and our goal was to characterize this dysbiosis and determine the features that predicted susceptibility. RESULTS: We employed 16S rRNA sequencing to characterize the cloacal microbiota in lorikeets (CZA n = 67, DZ n = 24) over time. We compared the microbiota of healthy lorikeets, to lorikeets with enteritis, and lorikeets susceptible to enteritis, with “susceptible” being defined as healthy birds that subsequently developed enteritis. Based on sequencing data, culture, and toxin gene detection in intestinal contents, we identified Clostridium perfringens type A (CZA and DZ) and C. colinum (CZA only) at increased relative abundances in birds with enteritis. Histopathology and immunohistochemistry further identified the presence of gram-positive bacilli and C. perfringens, respectively, in the necrotizing intestinal lesions. Finally, using Random Forests and LASSO models, we identified several features (young age and the presence of Rhodococcus fascians and Pseudomonas umsongensis) associated with susceptibility to clostridial enteritis. CONCLUSIONS: We identified C. perfringens type A and C. colinum associated with lorikeet necrohemorrhagic enteritis at CZA and DZ. Susceptibility testing of isolates lead to an updated clinical treatment plan which ultimately resolved the outbreaks at both institutions. This work provides a foundation for understanding gut microbiota features that are permissive to clostridial colonization and host factors (e.g. age, prior infection) that shape responses to infection. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00148-7.
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spelling pubmed-87443332022-01-11 Gut microbiota and age shape susceptibility to clostridial enteritis in lorikeets under human care Minich, David Madden, Christopher Navarro, Mauricio A. Glowacki, Leo French-Kim, Kristen Chan, Willow Evans, Morgan V. Soares, Kilmer Mrofchak, Ryan Madan, Rushil Ballash, Gregory A. LaPerle, Krista Paul, Subhadeep Vodovotz, Yael Uzal, Francisco A. Martinez, Margaret Hausmann, Jennifer Junge, Randall E. Hale, Vanessa L. Anim Microbiome Research Article BACKGROUND: Enteritis is a common cause of morbidity and mortality in lorikeets that can be challenging to diagnose and treat. In this study, we examine gut microbiota in two lorikeet flocks with enteritis (Columbus Zoo and Aquarium—CZA; Denver Zoo—DZ). Since 2012, the CZA flock has experienced repeated outbreaks of enteritis despite extensive diet, husbandry, and clinical modifications. In 2018, both CZA and DZ observed a spike in enteritis. Recent research has revealed that the gut microbiota can influence susceptibility to enteropathogens. We hypothesized that a dysbiosis, or alteration in the gut microbial community, was making some lorikeets more susceptible to enteritis, and our goal was to characterize this dysbiosis and determine the features that predicted susceptibility. RESULTS: We employed 16S rRNA sequencing to characterize the cloacal microbiota in lorikeets (CZA n = 67, DZ n = 24) over time. We compared the microbiota of healthy lorikeets, to lorikeets with enteritis, and lorikeets susceptible to enteritis, with “susceptible” being defined as healthy birds that subsequently developed enteritis. Based on sequencing data, culture, and toxin gene detection in intestinal contents, we identified Clostridium perfringens type A (CZA and DZ) and C. colinum (CZA only) at increased relative abundances in birds with enteritis. Histopathology and immunohistochemistry further identified the presence of gram-positive bacilli and C. perfringens, respectively, in the necrotizing intestinal lesions. Finally, using Random Forests and LASSO models, we identified several features (young age and the presence of Rhodococcus fascians and Pseudomonas umsongensis) associated with susceptibility to clostridial enteritis. CONCLUSIONS: We identified C. perfringens type A and C. colinum associated with lorikeet necrohemorrhagic enteritis at CZA and DZ. Susceptibility testing of isolates lead to an updated clinical treatment plan which ultimately resolved the outbreaks at both institutions. This work provides a foundation for understanding gut microbiota features that are permissive to clostridial colonization and host factors (e.g. age, prior infection) that shape responses to infection. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00148-7. BioMed Central 2022-01-09 /pmc/articles/PMC8744333/ /pubmed/35000619 http://dx.doi.org/10.1186/s42523-021-00148-7 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Minich, David
Madden, Christopher
Navarro, Mauricio A.
Glowacki, Leo
French-Kim, Kristen
Chan, Willow
Evans, Morgan V.
Soares, Kilmer
Mrofchak, Ryan
Madan, Rushil
Ballash, Gregory A.
LaPerle, Krista
Paul, Subhadeep
Vodovotz, Yael
Uzal, Francisco A.
Martinez, Margaret
Hausmann, Jennifer
Junge, Randall E.
Hale, Vanessa L.
Gut microbiota and age shape susceptibility to clostridial enteritis in lorikeets under human care
title Gut microbiota and age shape susceptibility to clostridial enteritis in lorikeets under human care
title_full Gut microbiota and age shape susceptibility to clostridial enteritis in lorikeets under human care
title_fullStr Gut microbiota and age shape susceptibility to clostridial enteritis in lorikeets under human care
title_full_unstemmed Gut microbiota and age shape susceptibility to clostridial enteritis in lorikeets under human care
title_short Gut microbiota and age shape susceptibility to clostridial enteritis in lorikeets under human care
title_sort gut microbiota and age shape susceptibility to clostridial enteritis in lorikeets under human care
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8744333/
https://www.ncbi.nlm.nih.gov/pubmed/35000619
http://dx.doi.org/10.1186/s42523-021-00148-7
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