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Psychoactive contaminants alter fish sperm function via neurotransmitter signaling

ABSTRACT: The widespread occurrence of psychoactive pollutants in surface waters raises concerns for aquatic ecosystems, yet impacts beyond behavioral disruption remain poorly understood. Designed to target neurotransmitter (NT) systems in humans, these contaminants may also interfere with conserved NT pathways in fish. Here we provide the first evidence that fish sperm contain NTs and their receptors, indicating an active NT-mediated signaling system essential for sperm function. Using European perch (Perca fluviatilis) exposed to environmentally relevant concentrations of methamphetamine, we quantified NTs in brain, gonads, and sperm, assessed tissue-specific bioaccumulation, and evaluated sperm performance. Methamphetamine accumulated across tissues, modified NT profiles, and altered sperm motility and velocity. These findings reveal a previously unrecognized pathway of reproductive vulnerability, identifying NT signaling in sperm as a novel target of psychoactive pollutants with potential implications for fertilization success and population resilience in aquatic ecosystems.

INSTRUMENT(S):

ORGANISM(S): Perca Fluviatilis

TISSUE(S): Eye, Spermatozoon, Brain, Gonad

SUBMITTER: Filip Dyčka

LAB HEAD: Ganna Fedorova

PROVIDER: PXD061699 | Pride | 2025-12-11

REPOSITORIES: Pride

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Source:

			Action	DRS
	Perca_20240905.fasta	Fasta
	ProteomeTable.xls	Xls
	maxquant_brain_eye_gonad_sperm_241205_fish_brains_241220_12h00m00s_txt.zip	Other
	maxquant_methamphetamine_gonad_240927_fish_241009_11h06m29s_txt.zip	Other
	maxquant_methamphetamine_sperm_241119_fish_sperm_241201_13h11m32s_txt.zip	Other

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Project description:In mature human sperm, genes of importance for embryo development (i.e. transcription factors) lack DNA methylation and bear nucleosomes with distinctive histone modifications, suggesting the specialized packaging of these developmental genes in the germline. Here, we explored the tractable zebrafish model and found conceptual conservation as well as several new features. Biochemical and mass spectrometric approaches reveal the zebrafish sperm genome packaged in nucleosomes and histone variants (and not protamine), and we find linker histones high and H4K16ac absent - key factors which may contribute to genome condensation. We examined several activating (H3K4me2/3, H3K14ac, H2AFV) and repressing (H3K27me3, H3K36me3, H3K9me3, hypoacetylation) modifications/compositions genome-wide, and find developmental genes packaged in large blocks of chromatin with coincident activating and repressing marks and DNA hypomethylation, revealing complex ‘multivalent’ chromatin. Notably, genes that acquire DNA methylation in the soma (muscle) are enriched in transcription factors for alternative cell fates. Remarkably, we find H3K36me3 located in ‘silent’ developmental gene promoters, and not present at the 3’ ends of coding regions of genes heavily transcribed during sperm maturation, suggesting different rules for H3K36me3 in the germline and soma. We also reveal the chromatin patterns of transposons, rDNA, and tRNAs. Finally, high levels of H3K4me3 and H3K14ac in sperm are correlated with genes activated in embryos prior to the mid-blastula transition (MBT), whereas multivalent genes are correlated with activation at or after MBT. Taken together, gene sets with particular functions in the embryo are packaged by distinctive types of complex and often atypical chromatin in sperm. [DNA profiling]: H3K4me3, H3K4me2, H3K14ac, H3K36me3, H3K27me3, H3K9me3, and H2AFV ChIP-chip in zebrafish sperm; DNA methylation in zebrafish sperm and muscle by MeDIP-chip. (two replicates and dye-swaps for all experiments). Antibodies: H3K4me3 (Abcam ab8580 and Active Motif 39159), H3K4me2 (Abcam ab7766), H3K14Ac (Upstate 07-353), H2AZ (Abcam ab4174), H3K27me3 (Upstate 07-449), H3K9me3 (Active Motif 39161), H3K36me3 (Abcam ab9050), 5-methylcytidine (Eurogentec BI-MECY-1000). Supplementary files: Processed data files reporting calculated enrichment log2 ratio (mean ChIP/mean Input in the log2 ratio). Note: For analysis, "mean Input" from H3K4me3-rep1 ch1, H3K4me2-rep1 ch2, and H3K36me3-rep2 ch1 for all ChIP eluates. [mRNA profiling]: Transcripts in zebrafish mature sperm using zebrafish expression microarray from Agilent. (two replicates)

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Psychoactive contaminants alter fish sperm function via neurotransmitter signaling

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