Differential distribution of eicosanoids and polyunsaturated fatty acids in the Penaeus monodon male reproductive tract and their effects on total sperm counts

PLoS One. 2022 Sep 22;17(9):e0275134. doi: 10.1371/journal.pone.0275134. eCollection 2022.

Abstract

Eicosanoids, which are oxygenated derivatives of polyunsaturated fatty acids (PUFAs), serve as signaling molecules that regulate spermatogenesis in mammals. However, their roles in crustacean sperm development remain unknown. In this study, the testis and vas deferens of the black tiger shrimp Penaeus monodon were analyzed using ultra-high performance liquid chromatography coupled with Orbitrap high resolution mass spectrometry. This led to the identification of three PUFAs and ten eicosanoids, including 15-deoxy-Δ12,14-prostaglandin J2 (15d-PGJ2) and (±)15-hydroxyeicosapentaenoic acid ((±)15-HEPE), both of which have not previously been reported in crustaceans. The comparison between wild-caught and domesticated shrimp revealed that wild-caught shrimp had higher sperm counts, higher levels of (±)8-HEPE in testes, and higher levels of prostaglandin E2 (PGE2) and prostaglandin F2α in vas deferens than domesticated shrimp. In contrast, domesticated shrimp contained higher levels of (±)12-HEPE, (±)18-HEPE, and eicosapentaenoic acid (EPA) in testes and higher levels of 15d-PGJ2, (±)12-HEPE, EPA, arachidonic acid (ARA), and docosahexaenoic acid (DHA) in vas deferens than wild-caught shrimp. To improve total sperm counts in domesticated shrimp, these broodstocks were fed with polychaetes, which contained higher levels of PUFAs than commercial feed pellets. Polychaete-fed shrimp produced higher total sperm counts and higher levels of PGE2 in vas deferens than pellet-fed shrimp. In contrast, pellet-fed shrimp contained higher levels of (±)12-HEPE, (±)18-HEPE, and EPA in testes and higher levels of (±)12-HEPE in vas deferens than polychaete-fed shrimp. These data suggest a positive correlation between high levels of PGE2 in vas deferens and high total sperm counts as well as a negative correlation between (±)12-HEPE in both shrimp testis and vas deferens and total sperm counts. Our analysis not only confirms the presence of PUFAs and eicosanoids in crustacean male reproductive organs, but also suggests that the eicosanoid biosynthesis pathway may serve as a potential target to improve sperm production in shrimp.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arachidonic Acid
  • Dinoprost
  • Dinoprostone / metabolism
  • Docosahexaenoic Acids
  • Eicosanoids
  • Eicosapentaenoic Acid
  • Fatty Acids, Unsaturated
  • Male
  • Mammals / metabolism
  • Penaeidae*
  • Prostaglandins E
  • Semen / metabolism
  • Sperm Count
  • Spermatozoa / metabolism

Substances

  • Eicosanoids
  • Fatty Acids, Unsaturated
  • Prostaglandins E
  • Docosahexaenoic Acids
  • Arachidonic Acid
  • Eicosapentaenoic Acid
  • Dinoprost
  • Dinoprostone

Grants and funding

This research has received funding supports from the National Center for Genetic Engineering and Biotechnology, Thailand [grant numbers P-17-50566 to WW]; the National Science and Technology Development Agency [grant number P14-50357 to RL], and the NSRF via the Program Management Unit for Human Resources & Institutional Development, Research and Innovation [grant number B05F640184 to WW]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.