Male differentiation in the marine copepod Oithona nana reveals the development of a new nervous ganglion linked to Lin12-Notch-Repeat protein-associated proteolysis

Abstract

AbstractBackgroundCopepods are among the most numerous animals, and play an essential role in the marine trophic web and biogeochemical cycles. The genus Oithona is described as having the highest density of copepods, and as being the most cosmopolite copepods. The Oithona male paradox describes the activity states of males, which are obliged to alternate between immobile and mobile phases for ambush feeding and mate searching, respectively, while the female is typically less mobile and often feeding. To characterize the molecular basis of this sexual dimorphism, we combined immunofluorescence, genomics, transcriptomics, and protein-protein interaction approaches.ResultsImmunofluorescence of β3- and α-tubulin revealed two male-specific nervous ganglia in the lateral first segment of the Oithona nana male’s prosome. In parallel, transcriptomic analysis showed male-specific enrichment for nervous system development-related transcripts. Twenty-seven Lin12-Notch Repeat domain-containing protein coding genes (LDPGs) of the 75 LDPGs identified in the genome were specifically expressed only in males. Furthermore, most of the LDPGs (27%) coded for proteins having predicted proteolytic activity, and non-LDPG proteolysis-associated transcripts showed a male-specific enrichment. Using yeast double–hybrid assays, we constructed a protein-protein interaction network involving two LDPs with proteases, extracellular matrix proteins, and neurogenesis-related proteins.ConclusionsFor the first time, our study describes the lateral nervous ganglia of O. nana males, unique to copepods. We also demonstrated a role of LDPGs and their associated proteolysis in male-specific physiology, and we hypothesize a role of the LDPGs in the development of the lateral ganglia through directed lysis of the extracellular matrix for the growth of neurites and genesis of synapses.