Abstract
Hypoxia is amongst the most widespread and pressing problems in aquatic environments. Here we demonstrate that fish (Oryzias melastigma) exposed to hypoxia show reproductive impairments (retarded gonad development, decrease in sperm count and sperm motility) in F1 and F2 generations despite these progenies (and their germ cells) having never been exposed to hypoxia. We further show that the observed transgenerational reproductive impairments are associated with a differential methylation pattern of specific genes in sperm of both F0 and F2 coupled with relevant transcriptomic and proteomic alterations, which may impair spermatogenesis. The discovered transgenerational and epigenetic effects suggest that hypoxia might pose a dramatic and long-lasting threat to the sustainability of fish populations. Because the genes regulating spermatogenesis and epigenetic modifications are highly conserved among vertebrates, these results may also shed light on the potential transgenerational effects of hypoxia on other vertebrates, including humans.
Highlights
Hypoxia is amongst the most widespread and pressing problems in aquatic environments
Fertilized eggs were collected from the hypoxic treatment within 1 h post fertilization to eliminate any possible effects of hypoxia that are directly exerted on the primordial germ cells
The collected eggs were divided into two batches: one batch was returned to normoxia and raised for two generations; and the other batch was continuously raised under hypoxia for two generations
Summary
Hypoxia is amongst the most widespread and pressing problems in aquatic environments. More than 400 ‘dead zones’ have been found worldwide, and climate change will exacerbate the problem in future years Both laboratory and field studies have demonstrated that hypoxia can affect specific genes along the brain-pituitary-gonad axis, disrupt the synthesis and balance of sex hormones and lead to reproductive impairments and sex alteration in several fish species[4,5,6]. Epigenetic changes (for example, DNA methylation, histone modifications and non-coding microRNAs (miRNAs) interference) can be induced by endocrine disrupting chemicals, thereby leading to transgenerational effects[14,15]. Using the marine medaka fish (Oryzias melastigma) as a model, the present study tests the hypothesis that hypoxia causes epigenetic changes that perturb the transcriptomic and proteomic profiles of offspring, which lead to transgenerational reproductive impairments. This study focuses on epigenetic and transgenerational effects in males
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