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Patterns of host gene expression associated with harboring a foregut microbial community

BACKGROUND: Harboring foregut microbial communities is considered a key innovation that allows herbivorous mammals to colonize new ecological niches. However, the functions of these chambers have only been well studied at the molecular level in ruminants. Here, we investigate gene expression in the...

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Autores principales: Kohl, Kevin D., Oakeson, Kelly F., Dunn, Diane, Meyerholz, David K., Dale, Colin, Weiss, Robert B., Dearing, M. Denise
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5585965/
https://www.ncbi.nlm.nih.gov/pubmed/28874116
http://dx.doi.org/10.1186/s12864-017-4101-z
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author Kohl, Kevin D.
Oakeson, Kelly F.
Dunn, Diane
Meyerholz, David K.
Dale, Colin
Weiss, Robert B.
Dearing, M. Denise
author_facet Kohl, Kevin D.
Oakeson, Kelly F.
Dunn, Diane
Meyerholz, David K.
Dale, Colin
Weiss, Robert B.
Dearing, M. Denise
author_sort Kohl, Kevin D.
collection PubMed
description BACKGROUND: Harboring foregut microbial communities is considered a key innovation that allows herbivorous mammals to colonize new ecological niches. However, the functions of these chambers have only been well studied at the molecular level in ruminants. Here, we investigate gene expression in the foregut chamber of herbivorous rodents and ask whether these gene expression patterns are consistent with results in ruminants. We compared gene expression in foregut tissues of two rodent species: Stephen’s woodrat (Neotoma stephensi), which harbors a dense foregut microbial community, and the lab rat (Rattus norvegicus), which lacks such a community. RESULTS: We found that woodrats have higher abundances of transcripts associated with smooth muscle processes, specifically a higher expression of the smoothelin-like 1 gene, which may assist in contractile properties of this tissue to retain food material in the foregut chamber. The expression of genes associated with keratinization and cornification exhibited a complex pattern of differences between the two species, suggesting distinct molecular mechanisms. Lab rats exhibited higher abundances of transcripts associated with immune function, likely to inhibit microbial growth in the foregut of this species. CONCLUSIONS: Some of our results were consistent with previous findings in ruminants (high expression of facilitative glucose transporters, lower expression of B4galnt2), suggestive of possible convergent evolution, while other results were unclear, and perhaps represent novel host-microbe interactions in rodents. Overall, our results suggest that harboring a foregut microbiota is associated with changes to the functions and host-microbe interactions of the foregut tissues. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-017-4101-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-55859652017-09-06 Patterns of host gene expression associated with harboring a foregut microbial community Kohl, Kevin D. Oakeson, Kelly F. Dunn, Diane Meyerholz, David K. Dale, Colin Weiss, Robert B. Dearing, M. Denise BMC Genomics Research Article BACKGROUND: Harboring foregut microbial communities is considered a key innovation that allows herbivorous mammals to colonize new ecological niches. However, the functions of these chambers have only been well studied at the molecular level in ruminants. Here, we investigate gene expression in the foregut chamber of herbivorous rodents and ask whether these gene expression patterns are consistent with results in ruminants. We compared gene expression in foregut tissues of two rodent species: Stephen’s woodrat (Neotoma stephensi), which harbors a dense foregut microbial community, and the lab rat (Rattus norvegicus), which lacks such a community. RESULTS: We found that woodrats have higher abundances of transcripts associated with smooth muscle processes, specifically a higher expression of the smoothelin-like 1 gene, which may assist in contractile properties of this tissue to retain food material in the foregut chamber. The expression of genes associated with keratinization and cornification exhibited a complex pattern of differences between the two species, suggesting distinct molecular mechanisms. Lab rats exhibited higher abundances of transcripts associated with immune function, likely to inhibit microbial growth in the foregut of this species. CONCLUSIONS: Some of our results were consistent with previous findings in ruminants (high expression of facilitative glucose transporters, lower expression of B4galnt2), suggestive of possible convergent evolution, while other results were unclear, and perhaps represent novel host-microbe interactions in rodents. Overall, our results suggest that harboring a foregut microbiota is associated with changes to the functions and host-microbe interactions of the foregut tissues. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-017-4101-z) contains supplementary material, which is available to authorized users. BioMed Central 2017-09-06 /pmc/articles/PMC5585965/ /pubmed/28874116 http://dx.doi.org/10.1186/s12864-017-4101-z Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Kohl, Kevin D.
Oakeson, Kelly F.
Dunn, Diane
Meyerholz, David K.
Dale, Colin
Weiss, Robert B.
Dearing, M. Denise
Patterns of host gene expression associated with harboring a foregut microbial community
title Patterns of host gene expression associated with harboring a foregut microbial community
title_full Patterns of host gene expression associated with harboring a foregut microbial community
title_fullStr Patterns of host gene expression associated with harboring a foregut microbial community
title_full_unstemmed Patterns of host gene expression associated with harboring a foregut microbial community
title_short Patterns of host gene expression associated with harboring a foregut microbial community
title_sort patterns of host gene expression associated with harboring a foregut microbial community
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5585965/
https://www.ncbi.nlm.nih.gov/pubmed/28874116
http://dx.doi.org/10.1186/s12864-017-4101-z
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