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The presence and distribution of gamma-aminobutyric acid and dopamine during the developmental stages of the sea cucumber, Holothuria scabra, with emphasis on settlement organs

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Abstract

In the sea cucumber, Holothuria scabra, the competent larvae require main settlement organs (SOs), including the ciliary bands (CiBs), tentacles (Ts), podia (PDs), and cues from neurotransmitters, including gamma-aminobutyric acid (GABA) and dopamine (DA), for successful settlement. In the present study, we investigated the spatial distribution of GABA and DA in the developmental stages of H. scabra, with special emphasis on SOs by detecting immunoreactivity (-ir) against these two neurotransmitters. Strong GABA-ir and DA-ir cells and fibers were specifically detected in several SO structures, including CiBs, CiB cells (CiBCs), and long cilia (LCi), of H. scabra larvae. Additionally, we found intense GABA-ir and DA-ir cells in the epithelial lining of bud-papillae (BP) and mesothelium (Me) in the stem (S) region of Ts in larvae and juveniles. Intense GABA-ir and DA-ir were observed in the epineural nerve plexus (ENP) and hyponeural nerve plexus (HNP) of Ts in H. scabra pentactula and juvenile stages. Staining for these two neurotransmitters was particularly intense in the PDs and their nerve fibers. We also found significant changes in the numbers of GABA-ir and DA-ir-positive cells and intensities in the CiBs, Ts, and PDs during the developmental stages. Taken together, we are the first to report on the existence and distribution of GABAergic and dopaminergic systems in structures associated with the settlement. Our findings provide new and important insights into the possible functions of these two neurotransmitters in regulating the settlement of this sea cucumber species.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

We are grateful to Asst. Prof. Dr. Worawit Suphamungmee and Asst. Prof. Dr. Jaruwan Poljaroen, for their useful comments and suggestions. We thank the Center of Nanoimaging (CNI) and the Central Instrument Facility (CIF), Faculty of Science, Mahidol University, for the use of a confocal microscope and instrumental support.

Funding

This research was financially supported by the Agricultural Research Development Agency (public organization). This research project was supported by Mahidol University (Basic Research Fund: fiscal year 2022) (Grant no: BRF1-052/2565) to YT., the Thailand Research Fund (TRF), Thailand Science Research and Innovation, and Mahidol University (TRF Mid-Career Research Grant, RSA6280057) to YT. This work was partially supported by the Graduate Student Thesis Grant of Graduate Studies of Mahidol University Alumni Association, Faculty of Graduate Studies, Mahidol University to NN and YT. This work was financially supported by the Faculty of Science, Mahidol University to YT and RT. This research project was supported by Mahidol University to RT.

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Authors and Affiliations

  1. Department of Anatomy, Faculty of Science, Mahidol University, Ratchathewi District, 272 Rama VI Road, Bangkok, 10400, Thailand

    Nittiya Nontunha, Prasert Sobhon & Yotsawan Tinikul

  2. Department of Biochemistry and Center for Excellence in Protein and Enzyme Technology, Faculty of Science, Mahidol University, Bangkok, 10400, Thailand

    Ruchanok Tinikul

  3. The Coastal Fisheries Research and Development Center, Klong Wan, Muang, Prachuap Khiri Khan, 77000, Thailand

    Supakant Chaichotranunt

  4. Inland Aquaculture Research and Development Division, Department of Fisheries, Phahonyothin Rd, Lat Yao, Chatuchak, Bangkok, 10900, Thailand

    Tanes Poomtong

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  1. Nittiya Nontunha
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Contributions

NN and YT: methodology, investigation, validation, formal analysis, writing original draft, and review and editing. SC and TP: resources. YT, PS, and RN: conceptualization, supervision, research design, data analysis, writing review and editing, project administration, and funding acquisition.

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Correspondence to Yotsawan Tinikul.

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Handling and laboratory protocols involving these sea cucumbers in the present study were carefully performed following the regulations and approval by the Animal Ethics Committee, Faculty of Science, Mahidol University (Animal Protocol number: MUSC62-026–490). All possible effort was made to minimize the number of animals used in this study.

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Nontunha, N., Tinikul, R., Chaichotranunt, S. et al. The presence and distribution of gamma-aminobutyric acid and dopamine during the developmental stages of the sea cucumber, Holothuria scabra, with emphasis on settlement organs. Cell Tissue Res 391, 457–483 (2023). https://doi.org/10.1007/s00441-023-03739-9

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