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

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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.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s42523-021-00148-7.

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          Most cited references97

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          DADA2: High resolution sample inference from Illumina amplicon data

          We present DADA2, a software package that models and corrects Illumina-sequenced amplicon errors. DADA2 infers sample sequences exactly, without coarse-graining into OTUs, and resolves differences of as little as one nucleotide. In several mock communities DADA2 identified more real variants and output fewer spurious sequences than other methods. We applied DADA2 to vaginal samples from a cohort of pregnant women, revealing a diversity of previously undetected Lactobacillus crispatus variants.
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            Random Forests

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              Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2

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                Author and article information

                Contributors
                minichdavid@gmail.com
                madden.80@osu.edu
                mauricio.navarro@uach.cl
                justgowacky@gmail.com
                french-kim.1@osu.edu
                chan.882@osu.edu
                morgvevans@gmail.com
                kilmerzootec2010@hotmail.com
                mrofchak.5@osu.edu
                madan.48@buckeyemail.osu.edu
                ballash.4@osu.edu
                Krista.LaPerle@gmail.com
                paul.963@osu.edu
                vodovotz.1@osu.edu
                fauzal@ucdavis.edu
                maggiemartinez0106@gmail.com
                JHausmann@denverzoo.org
                randy.junge@columbuszoo.org
                hale.502@osu.edu
                Journal
                Anim Microbiome
                Anim Microbiome
                Animal Microbiome
                BioMed Central (London )
                2524-4671
                9 January 2022
                9 January 2022
                2022
                : 4
                : 7
                Affiliations
                [1 ]GRID grid.261331.4, ISNI 0000 0001 2285 7943, Department of Veterinary Preventive Medicine, , Ohio State University College of Veterinary Medicine, ; 1902 Coffey Rd., Columbus, OH 43210 USA
                [2 ]GRID grid.266097.c, ISNI 0000 0001 2222 1582, California Animal Health & Food Safety Lab, , University of California, Davis, ; San Bernardino, CA USA
                [3 ]GRID grid.7119.e, ISNI 0000 0004 0487 459X, Instituto de Patología Animal, Facultad de Ciencias Veterinarias, , Universidad Austral de Chile, ; Valdivia, Chile
                [4 ]GRID grid.261331.4, ISNI 0000 0001 2285 7943, Ohio State University College of Arts and Sciences, ; Columbus, OH USA
                [5 ]GRID grid.261331.4, ISNI 0000 0001 2285 7943, Ohio State University College of Food, Agricultural, and Environmental Sciences, ; Columbus, OH USA
                [6 ]GRID grid.261331.4, ISNI 0000 0001 2285 7943, Ohio State University College of Public Health, ; Columbus, OH USA
                [7 ]GRID grid.411216.1, ISNI 0000 0004 0397 5145, Department of Animal Science, College of Agricultural Sciences (CCA), , Federal University of Paraiba (UFPB), ; Areia, PB Brazil
                [8 ]GRID grid.261331.4, ISNI 0000 0001 2285 7943, Comparative Pathology & Digital Imaging Shared Resource, , Ohio State University, ; Columbus, OH USA
                [9 ]GRID grid.448473.8, ISNI 0000 0004 7649 3016, The Marine Mammal Center, ; Sausalito, CA USA
                [10 ]GRID grid.484088.8, ISNI 0000 0001 0078 6419, Denver Zoo, ; Denver, CO USA
                [11 ]GRID grid.431692.b, ISNI 0000 0000 9153 1261, Columbus Zoo and Aquarium, ; Columbus, OH USA
                Author information
                http://orcid.org/0000-0002-8531-7001
                Article
                148
                10.1186/s42523-021-00148-7
                8744333
                35000619
                88a7b4d7-c946-45e6-bbda-d05974ef976b
                © The Author(s) 2022

                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/.

                History
                : 6 September 2021
                : 7 December 2021
                Funding
                Funded by: Columbus Zoo and Aquarium / Ohio State Cooperative Grants Program
                Funded by: National Institutes of Health Training Grant (T35)
                Funded by: The Ohio State University Infectious Diseases Institute
                Funded by: The Ohio State University College of Veterinary Medicine
                Funded by: American Association of Zoo Veterinarians Wild Animal Health Fund
                Funded by: FundRef http://dx.doi.org/10.13039/100000054, National Cancer Institute;
                Award ID: P30 CA016058
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2022

                clostridium,enteritis,lorikeets,gut microbiota,trypsin
                clostridium, enteritis, lorikeets, gut microbiota, trypsin

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