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Transcriptomic Analysis Identifies Genes and Pathways Related to Myrmecophagy in the Malayan Pangolin ( Manis javanica)

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Transcriptomic Analysis Identifies Genes and Pathways Related to Myrmecophagy in the Malayan Pangolin ( Manis javanica)

Jing-E Ma et al. PeerJ.

Abstract

The Malayan pangolin (Manis javanica) is an unusual, scale-covered, toothless mammal that specializes in myrmecophagy. Due to their threatened status and continuing decline in the wild, concerted efforts have been made to conserve and rescue this species in captivity in China. Maintaining this species in captivity is a significant challenge, partly because little is known of the molecular mechanisms of its digestive system. Here, the first large-scale sequencing analyses of the salivary gland, liver and small intestine transcriptomes of an adult M. javanica genome were performed, and the results were compared with published liver transcriptome profiles for a pregnant M. javanica female. A total of 24,452 transcripts were obtained, among which 22,538 were annotated on the basis of seven databases. In addition, 3,373 new genes were predicted, of which 1,459 were annotated. Several pathways were found to be involved in myrmecophagy, including olfactory transduction, amino sugar and nucleotide sugar metabolism, lipid metabolism, and terpenoid and polyketide metabolism pathways. Many of the annotated transcripts were involved in digestive functions: 997 transcripts were related to sensory perception, 129 were related to digestive enzyme gene families, and 199 were related to molecular transporters. One transcript for an acidic mammalian chitinase was found in the annotated data, and this might be closely related to the unique digestive function of pangolins. These pathways and transcripts are involved in specialization processes related to myrmecophagy (a form of insectivory) and carbohydrate, protein and lipid digestive pathways, probably reflecting adaptations to myrmecophagy. Our study is the first to investigate the molecular mechanisms underlying myrmecophagy in M. javanica, and we hope that our results may play a role in the conservation of this species.

Keywords: Conservation; Digestion; Myrmecophagy; Pangolin.

Conflict of interest statement

The authors declare there are no competing interests.

Figures

Figure 1
Figure 1. The metabolic pathway analysis of transcripts from Manis javanica.
(A) Metabolism, (B) Carbohydrate metabolism, (C) Lipid metabolism, (D) Amino acid metabolism, (E) Cofactors and vitamin metabolism and terpenoid and polyketide metabolism. The x-axis shows the numbers of annotated transcripts in one class, and the y-axis shows the KEGG function classes.
Figure 2
Figure 2. Terpenoid backbone biosynthesis (KEGG map 00900).
Figure 3
Figure 3. Pairwise correlation between organs (A–F).
Figure 4
Figure 4. The transcripts related to metabolic pathways expressed in all three tissues.
The x-axis shows the number of transcripts with the KEGG function class, which was shown above the column, and the y-axis shows the KEGG function classes.
Figure 5
Figure 5. The numbers of transcripts related to metabolic pathways that are specifically expressed in the salivary glands, liver, and small intestine of adult female Malayan pangolin (Manis javanica).
The x-axis shows the KEGG function classes, and the y-axis shows the number of transcripts with the corresponding KEGG function class.

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Grant support

This project was supported by the Planning Funds of Scientific and Technological of Guangdong Province (2016B070701016 and 2017A050503005) and the Training Fund of Guangdong Institute of Applied Biological Resources for Postdoctoral Researchers (NO.GIABR-pyjj201601), the Funds for Environment Construction and Capacity Building of GDAS’ Research Platform (2016GDASPT-0107), GDAS Special Project of Science and Technology Development (2017GDASCX-0107), and the Natural Science Foundation of Guangdong Province, China (2017A030310425). There was no additional external funding received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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