Histone methylation-associated transgenerational inheritance of reproductive defects in Caenorhabditis elegans exposed to crude oil under various exposure scenarios

Abstract

As part of a study to explore the long-term effects of the Hebei Spirit oil spill accident, transgenerational toxicity and associated epigenetic changes were investigated in the nematode Caenorhabditis elegans. Under experimental conditions, worms were exposed to Iranian heavy crude oil (IHC) under three different scenarios: partial early-life exposure (PE), partial late-life exposure (PL), and whole-life exposure (WE). Growth, reproduction, and histone methylation were monitored in the exposed parental worms (P0) and in three consecutive unexposed offspring generations (F1-3). Reproductive potential in the exposed P0 generation in the WE treatment group was reduced; additionally, it was inhibited in the unexposed offspring generations of the P0 worms. This suggests that there was transgenerational inheritance of defective reproduction. Comparison of developmental periods of exposure showed that IHC-treated worms in the PL group had a greater reduction in reproductive capacity than those in the PE group. Decreased methylation of histone H3 (H3K9) was found in the IHC-exposed parental generation. A heritable reduction in reproductive capacity occurred in wildtype N2 but was not found in a H3K9 histone methyltransferase (HMT) mutant, met-2(n4256), suggesting a potential role for HMT in transgenerational toxicity. Our results suggest that the reproductive toxicity after IHC exposure could be heritable and that histone methylation is associated with the transmission of the inherited phenotype.