Abstract
BackgroundHarboring 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.ResultsWe 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.ConclusionsSome 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.
Highlights
Harboring foregut microbial communities is considered a key innovation that allows herbivorous mammals to colonize new ecological niches
Read counts for protein-coding transcripts from the foregut tissues of Neotoma stephensi and Rattus norvegicus were obtained by RNA-Seq, aligned to the protein-coding portion of the comprehensive gene annotation of Mus musculus, and analyzed for differential abundance
A multi-dimensional scaling analysis indicated that the N. stephensi and R. norvegicus grouping best separated the top 1500 genes that have the largest variation between the RNA-Seq libraries (Fig. 1a), and 77% of the variance was explained by this grouping (Fig. 1b)
Summary
Harboring foregut microbial communities is considered a key innovation that allows herbivorous mammals to colonize new ecological niches. 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. Complex and intimate associations with fermentative gut microbes have been instrumental in the success of mammalian herbivores [1, 2]. These associations take place in enlarged gut compartments that house both the symbiotic microbes and the food material being digested. Changes in gene expression profiles associated with hosting foregut microbial communities have been studied in a number of ways. Developmental studies have compared gene expression in rumen epithelial tissue from suckling animals (before the establishment of fermentation) to
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