Molecular mechanism of nutrient uptake in developing embryos of oviparous cloudy catshark (Scyliorhinus torazame)

Yuki Honda; Nobuhiro Ogawa; Marty Kwok-Shing Wong; Kotaro Tokunaga; Shigehiro Kuraku; Susumu Hyodo; Wataru Takagi

doi:10.1371/journal.pone.0265428

Molecular mechanism of nutrient uptake in developing embryos of oviparous cloudy catshark (Scyliorhinus torazame)

PLoS One. 2022 Mar 15;17(3):e0265428. doi: 10.1371/journal.pone.0265428. eCollection 2022.

Authors

Yuki Honda¹, Nobuhiro Ogawa², Marty Kwok-Shing Wong¹, Kotaro Tokunaga³, Shigehiro Kuraku^{4

5

6}, Susumu Hyodo¹, Wataru Takagi¹

Affiliations

¹ Laboratory of physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan.
² Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan.
³ Ibaraki Prefectural Oarai Aquarium, Oarai, Ibaraki, Japan.
⁴ Laboratory for Phyloinformatics, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan.
⁵ Molecular Life History Laboratory, National Institute of Genetics, Mishima, Japan.
⁶ Department of Genetics, Sokendai (Graduate University for Advanced Studies), Mishima, Japan.

Abstract

Forms of embryonic nutrition are highly diverse in cartilaginous fishes, which contain oviparity, yolk-sac viviparity and several types of matrotrophic viviparity (histotrophy, oophagy, and placentotrophy). The molecular mechanisms of embryonic nutrition are poorly understood in these animals as few species are capable of reproducing in captivity. Oviparous cartilaginous fishes solely depend on yolk nutrients for their growth and development. In the present study, we compared the contribution to embryonic nutrition of the embryonic intestine with the yolk sac membrane (YSM). RNA-seq analysis was performed on the embryonic intestine and YSM of the oviparous cloudy catshark Scyliorhinus torazame to identify candidate genes involved in nutrient metabolism to further the understanding of nutrient utilization of developing embryos. RNA-seq discovery was subsequently confirmed by quantitative PCR analysis and we identified increases in several amino acid transporter genes (slc3a1, slc6a19, slc3a2, slc7a7) as well as genes involved in lipid absorption (apob and mtp) in the intestine after 'pre-hatching', which is a developmental event marked by an early opening of the egg case about 4 months before hatching. Although a reciprocal decrease in the nutritional role of YSM was expected after the intestine became functional, we observed similar increases in gene expression among amino acid transporters, lipid absorption molecules, and lysosomal cathepsins in the extraembryonic YSM in late developmental stages. Ultrastructure of the endodermal cells of YSM showed that yolk granules were incorporated by endocytosis, and the number of granules increased during development. Furthermore, the digestion of yolk granules in the YSM and nutrient transport through the basolateral membrane of the endodermal cells appeared to be enhanced after pre-hatching. These findings suggest that nutrient digestion and absorption is highly activated in both intestine and YSM after pre-hatching in catshark embryos, which supports the rapid growth at late developmental stages.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Elasmobranchii*
Fishes
Lipids
Nutrients
Oviparity*
Yolk Sac / metabolism

Substances

Lipids

Grants and funding

Supported by Grants-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (JSPS KAKENHI 19K22414) to S. Hyodo. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.