Low microbial abundance and community diversity in the egg capsule of the oviparous cloudy catshark (Scyliorhinus torazame) during oviposition.

Wataru Takagi, Ayami Masuda, Koya Shimoyama, Kotaro Tokunaga, Susumu Hyodo, Yuki Sato-Takabe
Author Information
  1. Wataru Takagi: Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan. ORCID
  2. Ayami Masuda: Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan.
  3. Koya Shimoyama: Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan. ORCID
  4. Kotaro Tokunaga: Ibaraki Prefectural Oarai Aquarium, Oarai, Ibaraki, Japan.
  5. Susumu Hyodo: Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan. ORCID
  6. Yuki Sato-Takabe: Marine Microbiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan. ORCID

Abstract

Vertebrate embryos are protected from bacterial infection by various maternally derived factors, yet little is known about the defence mechanisms in elasmobranchs. This study aimed to characterize the intracapsular environment of freshly laid eggs of the oviparous catshark (Scyliorhinus torazame) by investigating the microbial abundance and microbiota to understand its potential contribution to embryonic defence. The egg capsule of oviparous elasmobranchs is tightly sealed until pre-hatching, after which seawater flows into the capsule, exposing the embryos to the surrounding seawater. We found that early embryos were highly vulnerable to environmental pathogens, suggesting that the embryos are somehow protected from infection before pre-hatching. Indeed, the intracapsular environment of freshly laid eggs exhibited significantly low bacterial density, maintained until pre-hatching. Furthermore, the microbiome inside eggs just after oviposition differed markedly from those of rearing seawater and adult oviducal gland epithelia; these eggs were predominantly populated by an unidentified genus of Sphingomonadaceae. Overall, this study provides compelling evidence that early embryos of oviparous cloudy catshark are incubated in a clean intracapsular environment that potentially plays a significant role in embryonic development in oviparous elasmobranchs.

References

  1. FEMS Immunol Med Microbiol. 2004 Jun 1;41(2):101-7 [PMID: 15145453]
  2. Reprod Biol Endocrinol. 2003 Nov 28;1:116 [PMID: 14641912]
  3. Proc Natl Acad Sci U S A. 2018 Oct 16;115(42):10780-10785 [PMID: 30275316]
  4. Adv Exp Med Biol. 2017;1001:33-57 [PMID: 28980228]
  5. Nat Methods. 2016 Jul;13(7):581-3 [PMID: 27214047]
  6. PLoS Comput Biol. 2021 Nov 16;17(11):e1009442 [PMID: 34784344]
  7. Respir Physiol. 1971 Mar;11(3):265-78 [PMID: 5552766]
  8. J Exp Biol. 2020 Jul 7;223(Pt 13): [PMID: 32527960]
  9. PLoS One. 2018 Nov 6;13(11):e0206984 [PMID: 30399186]
  10. Front Microbiol. 2020 Dec 04;11:557035 [PMID: 33343514]
  11. Environ Microbiol Rep. 2024 Oct;16(5):e70025 [PMID: 39438677]
  12. Fish Shellfish Immunol. 2021 Nov;118:405-410 [PMID: 34582977]
  13. Nat Biotechnol. 2019 Aug;37(8):852-857 [PMID: 31341288]
  14. Anim Microbiome. 2021 Sep 15;3(1):61 [PMID: 34526135]
  15. Food Microbiol. 2016 Feb;53(Pt B):82-93 [PMID: 26678134]
  16. J Fish Biol. 2021 Jul;99(1):240-252 [PMID: 33651432]
  17. PLoS One. 2014 Oct 20;9(10):e109504 [PMID: 25329313]
  18. Microbes Environ. 2020;35(2): [PMID: 32493880]
  19. Experientia. 1978 Dec 15;34(12):1596-7 [PMID: 569596]
  20. J Fish Biol. 2024 May;104(5):1638-1644 [PMID: 38387880]
  21. Front Cell Infect Microbiol. 2022 Jun 16;12:869736 [PMID: 35782109]
  22. Poult Sci. 2006 Aug;85(8):1364-72 [PMID: 16903465]
  23. Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6 [PMID: 23193283]
  24. Dev Comp Immunol. 2005;29(5):417-30 [PMID: 15707663]
  25. Zoological Lett. 2023 May 30;9(1):13 [PMID: 37254194]
  26. Zoological Lett. 2021 Feb 15;7(1):3 [PMID: 33588955]
  27. Comp Biochem Physiol A Mol Integr Physiol. 2017 Sep;211:7-16 [PMID: 28579535]
  28. Proc Natl Acad Sci U S A. 2016 Nov 29;113(48):13833-13838 [PMID: 27849619]
  29. Dev Dyn. 2018 May;247(5):712-723 [PMID: 29396887]
  30. PLoS Comput Biol. 2021 Nov 8;17(11):e1009581 [PMID: 34748542]
  31. Anim Microbiome. 2021 Oct 13;3(1):72 [PMID: 34645528]
  32. Biochim Biophys Acta. 2012 Mar;1820(3):218-25 [PMID: 21854833]
  33. Arch Biochem Biophys. 1977 Oct;183(2):432-42 [PMID: 21616]
  34. Gen Comp Endocrinol. 2022 Oct 1;327:114076 [PMID: 35710034]
  35. Microb Ecol. 2023 Feb;85(2):747-764 [PMID: 35129649]

Grants

  1. G-2024-3-018/Institute for Fermentation, Osaka
  2. JP22K15153/Japan Society for the Promotion of Science

MeSH Term

Animals
Oviposition
Microbiota
Bacteria
Sharks
Female
Ovum
Seawater
RNA, Ribosomal, 16S
Oviparity
Phylogeny

Chemicals

RNA, Ribosomal, 16S

Word Cloud

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