Proteolysis and neurogenesis modulated by LNR domain proteins explosion support male differentiation and sacrificial behaviour in the iteroparous crustacean Oithona nana.

Abstract

Copepods are 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 numerical density, as the most cosmopolite copepod and iteroparous. The Oithona male paradox obliges it to alternate feeding (immobile) and mating (mobile) phases. As the molecular basis of this trade-off is unknown, we investigated this sexual dimorphism at the molecular level by integrating genomic, transcriptomic and protein-protein interaction analyses.\n\nWhile a ZW sex-determination system was predicted in O. nana, a fifteen-year time-series in the Toulon Little Bay showed a biased sex ratio toward females (male / female ratio < 0.15{+/-}0.11) highlighting a higher mortality in male. Here, the transcriptomic analysis of the five different developmental stages showed enrichment of Lin12-Notch Repeat (LNR) domains-containing proteins coding genes (LDPGs) in male transcripts. The male also showed enrichment in transcripts involved in proteolysis, nervous system development, synapse assembly and functioning and also amino acid conversion to glutamate. Moreover, several male down-regulated genes were involved in the increase of food uptake and digestion. The formation of LDP complexes was detected by yeast two-hybrid, with interactions involving proteases, extracellular matrix proteins and neurogenesis related proteins.\n\nTogether, these results suggest that the O. nana male hypermotility is sustained by LDP-modulated proteolysis allowing the releases and conversions of amino acid into the excitatory neurotransmitter glutamate. This process could permit new axons and dendrites formation suggesting a sexual nervous system dimorphism. This could support the hypothesis of a sacrificial behaviour in males at the metabolic level.