Starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding
Background: The ability of animals and their microbiomes to adapt to starvation and then restore homeostasis after refeeding is fundamental to their continued survival and symbiosis. The intestine is the primary site of nutrient absorption and microbiome interaction, however our understanding of intestinal adaptations in host transcriptional programs and microbiome composition remains limited. Additionally, few studies on starvation have investigated intestinal responses to refeeding. The zebrafish presents unique opportunities to study the effects of long-term starvation and refeeding. We used RNA sequencing and 16S rRNA gene sequencing to uncover changes in the intestinal transcriptome and microbiome of zebrafish subjected to long-term starvation and refeeding compared to continuously fed controls.
Results: Starvation over 21 days led to increased diversity and altered composition in the intestinal microbiome compared to fed controls, including relative increases in Vibrio and reductions in Plesiomonas bacteria. Starvation also led to significant alterations in host gene expression in the intestine, with distinct pathways affected at early and late stages of starvation. This included increases in the expression of ribosome biogenesis genes early in starvation, followed by decreased expression of genes involved in antiviral immunity and at later stages. These effects of starvation on the host transcriptome and microbiome were within 3 days after refeeding. Comparison with published datasets identified host genes responsive to starvation as well as high-fat feeding or microbiome colonization, and predicted host transcription factors that may be involved in starvation response.
Conclusions: Long-term starvation induces progressive changes in microbiome composition and host gene expression in the zebrafish intestine, and these changes are rapidly reversed after refeeding. Our identification of bacterial taxa, host genes and host pathways involved in this response provides a framework for future investigation of the physiological and ecological mechanisms underlying intestinal adaptations to food restriction.
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Posted 16 Dec, 2020
On 28 Jan, 2021
Received 18 Jan, 2021
Received 18 Jan, 2021
Received 18 Jan, 2021
Received 18 Jan, 2021
On 13 Jan, 2021
On 13 Jan, 2021
On 13 Jan, 2021
On 13 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
Invitations sent on 29 Dec, 2020
On 15 Dec, 2020
On 15 Dec, 2020
On 15 Dec, 2020
On 02 Dec, 2020
Starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding
Posted 16 Dec, 2020
On 28 Jan, 2021
Received 18 Jan, 2021
Received 18 Jan, 2021
Received 18 Jan, 2021
Received 18 Jan, 2021
On 13 Jan, 2021
On 13 Jan, 2021
On 13 Jan, 2021
On 13 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
On 07 Jan, 2021
Invitations sent on 29 Dec, 2020
On 15 Dec, 2020
On 15 Dec, 2020
On 15 Dec, 2020
On 02 Dec, 2020
Background: The ability of animals and their microbiomes to adapt to starvation and then restore homeostasis after refeeding is fundamental to their continued survival and symbiosis. The intestine is the primary site of nutrient absorption and microbiome interaction, however our understanding of intestinal adaptations in host transcriptional programs and microbiome composition remains limited. Additionally, few studies on starvation have investigated intestinal responses to refeeding. The zebrafish presents unique opportunities to study the effects of long-term starvation and refeeding. We used RNA sequencing and 16S rRNA gene sequencing to uncover changes in the intestinal transcriptome and microbiome of zebrafish subjected to long-term starvation and refeeding compared to continuously fed controls.
Results: Starvation over 21 days led to increased diversity and altered composition in the intestinal microbiome compared to fed controls, including relative increases in Vibrio and reductions in Plesiomonas bacteria. Starvation also led to significant alterations in host gene expression in the intestine, with distinct pathways affected at early and late stages of starvation. This included increases in the expression of ribosome biogenesis genes early in starvation, followed by decreased expression of genes involved in antiviral immunity and at later stages. These effects of starvation on the host transcriptome and microbiome were within 3 days after refeeding. Comparison with published datasets identified host genes responsive to starvation as well as high-fat feeding or microbiome colonization, and predicted host transcription factors that may be involved in starvation response.
Conclusions: Long-term starvation induces progressive changes in microbiome composition and host gene expression in the zebrafish intestine, and these changes are rapidly reversed after refeeding. Our identification of bacterial taxa, host genes and host pathways involved in this response provides a framework for future investigation of the physiological and ecological mechanisms underlying intestinal adaptations to food restriction.
Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Due to technical limitations, full-text HTML conversion of this manuscript could not be completed. However, the manuscript can be downloaded and accessed as a PDF.