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Succession in the caecal microbiota of developing broilers colonised by extended-spectrum β-lactamase-producing Escherichia coli

BACKGROUND: Broilers are among the most common and dense poultry production systems, where antimicrobials have been used extensively to promote animal health and performance. The continuous usage of antimicrobials has contributed to the appearance of resistant bacteria, such as extended-spectrum β-l...

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Autores principales: Cárdenas-Rey, Ingrid, Bello Gonzalez, Teresita d. J., van der Goot, Jeanet, Ceccarelli, Daniela, Bouwhuis, Gerwin, Schillemans, Danielle, Jurburg, Stephanie D., Veldman, Kees T., de Visser, J. Arjan G. M., Brouwer, Michael S. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9389726/
https://www.ncbi.nlm.nih.gov/pubmed/35986389
http://dx.doi.org/10.1186/s42523-022-00199-4
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author Cárdenas-Rey, Ingrid
Bello Gonzalez, Teresita d. J.
van der Goot, Jeanet
Ceccarelli, Daniela
Bouwhuis, Gerwin
Schillemans, Danielle
Jurburg, Stephanie D.
Veldman, Kees T.
de Visser, J. Arjan G. M.
Brouwer, Michael S. M.
author_facet Cárdenas-Rey, Ingrid
Bello Gonzalez, Teresita d. J.
van der Goot, Jeanet
Ceccarelli, Daniela
Bouwhuis, Gerwin
Schillemans, Danielle
Jurburg, Stephanie D.
Veldman, Kees T.
de Visser, J. Arjan G. M.
Brouwer, Michael S. M.
author_sort Cárdenas-Rey, Ingrid
collection PubMed
description BACKGROUND: Broilers are among the most common and dense poultry production systems, where antimicrobials have been used extensively to promote animal health and performance. The continuous usage of antimicrobials has contributed to the appearance of resistant bacteria, such as extended-spectrum β-lactamase-producing Escherichia coli (ESBL-Ec). Here, we studied the ESBL-Ec prevalence and successional dynamics of the caecal microbiota of developing broilers in a commercial flock during their production life cycle (0–35 days). Broilers were categorised as ESBL-Ec colonised (ESBL-Ec(+)) or ESBL-Ec non-colonised (ESBL-Ec(−)) by selective culturing. Using 16S rRNA gene sequencing, we i. compared the richness, evenness and composition of the caecal microbiota of both broilers’ groups and ii. assessed the combined role of age and ESBL-Ec status on the broilers’ caecal microbiota. RESULTS: From day two, we observed an increasing linear trend in the proportions of ESBL-Ec throughout the broilers' production life cycle, X(2) (1, N = 12) = 28.4, p < 0.001. Over time, the caecal microbiota richness was consistently higher in ESBL-Ec(−) broilers, but significant differences between both broilers’ groups were found exclusively on day three (Wilcoxon rank-sum test, p = 0.016). Bray–Curtis distance-based RDA (BC-dbRDA) showed no explanatory power of ESBL-Ec status, while age explained 14% of the compositional variation of the caecal microbiota, F (2, 66) = 6.47, p = 0.001. CONCLUSIONS: This study assessed the role of ESBL-Ec in the successional dynamics of the caecal microbiota in developing broilers and showed that the presence of ESBL-Ec is associated with mild but consistent reductions in alpha diversity and with transient bacterial compositional differences. We also reported the clonal spread of ESBL-Ec and pointed to the farm environment as a likely source for ESBLs. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00199-4.
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spelling pubmed-93897262022-08-20 Succession in the caecal microbiota of developing broilers colonised by extended-spectrum β-lactamase-producing Escherichia coli Cárdenas-Rey, Ingrid Bello Gonzalez, Teresita d. J. van der Goot, Jeanet Ceccarelli, Daniela Bouwhuis, Gerwin Schillemans, Danielle Jurburg, Stephanie D. Veldman, Kees T. de Visser, J. Arjan G. M. Brouwer, Michael S. M. Anim Microbiome Research Article BACKGROUND: Broilers are among the most common and dense poultry production systems, where antimicrobials have been used extensively to promote animal health and performance. The continuous usage of antimicrobials has contributed to the appearance of resistant bacteria, such as extended-spectrum β-lactamase-producing Escherichia coli (ESBL-Ec). Here, we studied the ESBL-Ec prevalence and successional dynamics of the caecal microbiota of developing broilers in a commercial flock during their production life cycle (0–35 days). Broilers were categorised as ESBL-Ec colonised (ESBL-Ec(+)) or ESBL-Ec non-colonised (ESBL-Ec(−)) by selective culturing. Using 16S rRNA gene sequencing, we i. compared the richness, evenness and composition of the caecal microbiota of both broilers’ groups and ii. assessed the combined role of age and ESBL-Ec status on the broilers’ caecal microbiota. RESULTS: From day two, we observed an increasing linear trend in the proportions of ESBL-Ec throughout the broilers' production life cycle, X(2) (1, N = 12) = 28.4, p < 0.001. Over time, the caecal microbiota richness was consistently higher in ESBL-Ec(−) broilers, but significant differences between both broilers’ groups were found exclusively on day three (Wilcoxon rank-sum test, p = 0.016). Bray–Curtis distance-based RDA (BC-dbRDA) showed no explanatory power of ESBL-Ec status, while age explained 14% of the compositional variation of the caecal microbiota, F (2, 66) = 6.47, p = 0.001. CONCLUSIONS: This study assessed the role of ESBL-Ec in the successional dynamics of the caecal microbiota in developing broilers and showed that the presence of ESBL-Ec is associated with mild but consistent reductions in alpha diversity and with transient bacterial compositional differences. We also reported the clonal spread of ESBL-Ec and pointed to the farm environment as a likely source for ESBLs. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00199-4. BioMed Central 2022-08-19 /pmc/articles/PMC9389726/ /pubmed/35986389 http://dx.doi.org/10.1186/s42523-022-00199-4 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
Cárdenas-Rey, Ingrid
Bello Gonzalez, Teresita d. J.
van der Goot, Jeanet
Ceccarelli, Daniela
Bouwhuis, Gerwin
Schillemans, Danielle
Jurburg, Stephanie D.
Veldman, Kees T.
de Visser, J. Arjan G. M.
Brouwer, Michael S. M.
Succession in the caecal microbiota of developing broilers colonised by extended-spectrum β-lactamase-producing Escherichia coli
title Succession in the caecal microbiota of developing broilers colonised by extended-spectrum β-lactamase-producing Escherichia coli
title_full Succession in the caecal microbiota of developing broilers colonised by extended-spectrum β-lactamase-producing Escherichia coli
title_fullStr Succession in the caecal microbiota of developing broilers colonised by extended-spectrum β-lactamase-producing Escherichia coli
title_full_unstemmed Succession in the caecal microbiota of developing broilers colonised by extended-spectrum β-lactamase-producing Escherichia coli
title_short Succession in the caecal microbiota of developing broilers colonised by extended-spectrum β-lactamase-producing Escherichia coli
title_sort succession in the caecal microbiota of developing broilers colonised by extended-spectrum β-lactamase-producing escherichia coli
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9389726/
https://www.ncbi.nlm.nih.gov/pubmed/35986389
http://dx.doi.org/10.1186/s42523-022-00199-4
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