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

View ORCID ProfileDavid Minich, Christopher Madden, Mauricio A. Navarro, Leo Glowacki, Kristen French-Kim, Willow Chan, Morgan V. Evans, Kilmer Soares, Ryan Mrofchak, Rushil Madan, Gregory A. Ballash, Krista LaPerle, Subhadeep Paul, Yael Vodovotz, Francisco A. Uzal, Margaret Martinez, Jennifer Hausmann, Randall E. Junge, View ORCID ProfileVanessa L. Hale
doi: https://doi.org/10.1101/2021.09.08.459483
David Minich
1Ohio State University College of Veterinary Medicine, Columbus, OH, USA
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Christopher Madden
1Ohio State University College of Veterinary Medicine, Columbus, OH, USA
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Mauricio A. Navarro
2California Animal Health & Food Safety Lab, University of California, Davis, San Bernardino, CA, USA
3Instituto de Patología Animal, Facultad de Ciencias Veterinarias, Universidad Austral de Chile, Chile
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Leo Glowacki
4Ohio State University College of Arts and Sciences, Columbus, OH, USA
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Kristen French-Kim
1Ohio State University College of Veterinary Medicine, Columbus, OH, USA
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Willow Chan
5Ohio State University College of Food, Agricultural, and Environmental Sciences, Columbus, OH, USA
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Morgan V. Evans
1Ohio State University College of Veterinary Medicine, Columbus, OH, USA
6Ohio State University College of Public Health, Columbus, OH, USA
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Kilmer Soares
1Ohio State University College of Veterinary Medicine, Columbus, OH, USA
7Department of Animal Science, College of Agricultural Sciences (CCA), Federal University of Paraiba (UFPB), Areia, PB, Brazil
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Ryan Mrofchak
1Ohio State University College of Veterinary Medicine, Columbus, OH, USA
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Rushil Madan
1Ohio State University College of Veterinary Medicine, Columbus, OH, USA
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Gregory A. Ballash
1Ohio State University College of Veterinary Medicine, Columbus, OH, USA
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Krista LaPerle
1Ohio State University College of Veterinary Medicine, Columbus, OH, USA
8Ohio State University Comparative Pathology & Digital Imaging Shared Resource, Columbus, OH, USA
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Subhadeep Paul
4Ohio State University College of Arts and Sciences, Columbus, OH, USA
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Yael Vodovotz
5Ohio State University College of Food, Agricultural, and Environmental Sciences, Columbus, OH, USA
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Francisco A. Uzal
2California Animal Health & Food Safety Lab, University of California, Davis, San Bernardino, CA, USA
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Margaret Martinez
1Ohio State University College of Veterinary Medicine, Columbus, OH, USA
9The Marine Mammal Center, Sausalito, CA, USA
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Jennifer Hausmann
10Denver Zoo, Denver, CO, USA
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Randall E. Junge
11Columbus Zoo and Aquarium, Columbus, OH, USA
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Vanessa L. Hale
1Ohio State University College of Veterinary Medicine, Columbus, OH, USA
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  • ORCID record for Vanessa L. Hale
  • For correspondence: hale.502@osu.edu
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Abstract

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.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • minichdavid{at}gmail.com, madden.80{at}osu.edu, mnavarrob{at}ucdavis.edu, justgowacky{at}gmail.com, french-kim.1{at}osu.edu, chan.882{at}osu.edu, morgvevans{at}gmail.com, kilmerzootec2010{at}hotmail.com, mrofchak.5{at}osu.edu, madan.48{at}buckeyemail.osu.edu, ballash.4{at}osu.edu, la-perle.1{at}osu.edu, paul.963{at}osu.edu, vodovotz.1{at}osu.edu, fauzal{at}ucdavis.edu, maggiemartinez0106{at}gmail.com, JHausmann{at}denverzoo.org, randy.junge{at}columbuszoo.org, hale.502{at}osu.edu

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Gut microbiota and age shape susceptibility to clostridial enteritis in lorikeets under human care
David Minich, Christopher Madden, Mauricio A. Navarro, Leo Glowacki, Kristen French-Kim, Willow Chan, Morgan V. Evans, Kilmer Soares, Ryan Mrofchak, Rushil Madan, Gregory A. Ballash, Krista LaPerle, Subhadeep Paul, Yael Vodovotz, Francisco A. Uzal, Margaret Martinez, Jennifer Hausmann, Randall E. Junge, Vanessa L. Hale
bioRxiv 2021.09.08.459483; doi: https://doi.org/10.1101/2021.09.08.459483
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Gut microbiota and age shape susceptibility to clostridial enteritis in lorikeets under human care
David Minich, Christopher Madden, Mauricio A. Navarro, Leo Glowacki, Kristen French-Kim, Willow Chan, Morgan V. Evans, Kilmer Soares, Ryan Mrofchak, Rushil Madan, Gregory A. Ballash, Krista LaPerle, Subhadeep Paul, Yael Vodovotz, Francisco A. Uzal, Margaret Martinez, Jennifer Hausmann, Randall E. Junge, Vanessa L. Hale
bioRxiv 2021.09.08.459483; doi: https://doi.org/10.1101/2021.09.08.459483

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