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  • ReceivedAug 17, 2020
  • AcceptedSep 29, 2020
  • PublishedNov 5, 2020

Abstract


Funded by

the National Natural Science Foundation of China(31822052,31572381)

the National Thousand Youth Talents Plan to Y.J.

National Natural Science Foundation of China(31660644)

National Natural Science Foundation of China(41422604)

the Independent Research Fund Denmark(8049-00098B)

Zhengzhi Wei

Zixin Yang

and Haiyu Gao from Institute of Deep-sea Science and Engineering

Chinese Academy of Sciences

for helping to collect samples from the porpoise and whale. We thank High-Performance Computing(HPC)


Acknowledgment

This project was supported by the National Natural Science Foundation of China (31822052, 31572381), the National Thousand Youth Talents Plan to Y.J., National Natural Science Foundation of China (31660644) to S.H., National Natural Science Foundation of China (41422604) to S.L. The Villum Foundation (VKR 023447) and the Independent Research Fund Denmark (8049-00098B) are thanked for supporting R.H. We thank the members of the FANNG project for sharing their transcriptome data. We thank Yongchuan Li, Zhengzhi Wei, Zixin Yang, and Haiyu Gao from Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, for helping to collect samples from the porpoise and whale. We thank High-Performance Computing (HPC) of Northwest A&F University (NWAFU) for providing computing resources.


Interest statement

Two provisional Chinese patent applications on potential application in the antimicrobial and antibiotic substitute by way of the DEFB1 gene and LYZ1 gene have been filed by Northwest A&F University (application number 202010100677.8 and 202010097562.8), where Y.J., X.P., X.C, and W.W. are listed as inventors. The author(s) declare that they have no conflict of interest.


Supplement

SUPPORTING INFORMATION

The supporting information is available online at https://doi.org/10.1007/s11427-020-1828-8. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.


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  • Figure 1

    Phylogenomic placement of species with multi-chamber stomach in the Artiodactyla and Ruminantia. Maximum-likelihood (ML) tree generated using 3,316,385 four-fold degenerate sites with 11,567 single-copy orthologous genes. Dates for major events are taken from the TimeTree Database (Kumar et al., 2017) and Chen et al. (Chen et al., 2019). The green rectangular block indicates the Ruminantia. Dotted lines link to the detailed divergence times of the two taxa. The esophagus is colored red, the additional stomach chambers in the multi-stomach lineages purple, the rumen green, and the true stomach/abomasum orange.

  • Figure 2

    Comparisons of gene expression profile among rumen and other tissues. A, Hierarchical clustering results showing the relationships among 50 tissues of sheep and a heatmap showing the pairwise Spearman correlations between sheep tissues (the top triangle), between 14 tissues of camels (lower left triangle) and between eight tissues of two cetaceans (lower right triangle). B, Heatmap of differentially expressed rumen specifically expressed genes among the rumen and other FC stomachs. The color bars on the left present 136 DEGs of the rumen relative to the FC stomach of cetaceans (yellow), 21 DEGs relative to the FC stomach of camels (green), and 427 DEGs relative to the FC stomach of both species (purple). The expression levels were normalized by Z-scores. C, KEGG pathway analysis of 427 rumen up-regulated DEGs relative to both the FC stomach of camels and cetaceans. D, Heatmap showing the gene expression profiles of all 655 rumen relatively highly expressed genes across 43 tissues of sheep. Different colored lines represent the primary tissues from which the rumen relatively highly expressed genes were recruited. Number of genes from each tissue is shown below the tissue name with the percentage of total genes recruited in parentheses.

  • Figure 3

    Genetic changes in the rumen ketone body metabolism genes and pathways. A, Genes annotated in the ketone body metabolism are labeled with different color to indicate rumen relatively highly expressed genes (blue), positively selected genes in ruminant (orange) and differentially expressed genes between rumen and other FC stomachs (purple). The solid arrows represent ketone body metabolism pathways. The dashed arrows indicate the process of material transport from rumen to other tissues. B, Top panels: Structural domains of the HMGCS2 protein and the location of the ruminant specific mutations. Lower panel: Peptide sequence alignment of HMGCS2. The species is followed a yellow circle belonging to the ruminant. The red highlighting indicates ruminant-specific amino acid mutations. C, Predicted tertiary structures of the HMGCS2 of ruminant (blue) and other mammals (orange), respectively. D, Enzyme activities of HMGCS2 compared with those of sheep and human in vitro. Non-Rumen: human, Non-Rumen-5R: human HMGCS2 with five ruminant aa replacements, Rumen: sheep, Rumen-5H: sheep HMGCS2 with five human aa replacements. **P<0.01, ***P<0.001 calculated from the t test. Data are shown as mean±SD.

  • Figure 4

    Microbial management of the rumen. A, Rumen relatively highly expressed genes (blue), differentially expressed genes between rumen and other FC stomachs (purple), positively selected genes in ruminant (orange), differentially expressed genes between rumen and esophagus (red), newly evolved genes (cyan) and RSCNE-associated rumen core genes (green) involved in IL17 signaling pathway and Staphylococcus aureus infection. The antibacterial ability of (B) DEFB1 and (C) LYZ1. Inhibition zone assays on agarose plates with Escherichia coli (ATCC 25922) and Staphylococcus aureus (ATCC 29213).

  • Figure 5

    Genetic changes related to rumen epithelium transportation and absorption. A, Diagram of rumen epithelial cell proteins involved in epithelium permeability identified in the common ancestor of the ruminants. Rumen relatively highly expressed genes (blue), positively selected genes in ruminants (orange), differentially expressed genes between rumen and other FC stomachs (purple), differentially expressed genes between rumen and esophagus (red), and RSCNE-associated rumen core genes (green). Note the junction structure (desmosome) between keratinocytes of the ruminal epithelium has been degraded, instead the enlarged intercellular space with copious blood supply enables metabolites absorption in the ruminal epithelium (Steven et al., 1970). B, Gene structure of WDR66 based on the NCBI Oar_v4.0 annotation shown above. Green boxes represent exons. Purple bars indicate ruminant-specific conserved non-exonic elements (RSCNEs). Red and blue bars indicate ATAC-seq peaks of the ruminal and esophageal epithelium cell, respectively. The grey rectangle box is the overlapping element of RSCNE and ATAC-seq which is located in the intron region. C, The luciferase activity of the pGL3-Promoter (WT) and the pGL3-Promoter with the RSCNE (●A). *P<0.05 calculated from the t test. Data are shown as mean±SD.

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