Metabolome and Metagenome Signatures Underlying the Differential Resistance of Percocypris pingi, Crucian Carp, and Yellow Catfish to Ichthyophthirius multifiliis Infection

TL;DR

This study shows that a fish species called Percocypris pingi is highly resistant to a parasitic disease due to high antioxidants and a unique skin microbiome.

Contribution

The study reveals a synergistic role of antioxidants and microbiome in disease resistance in fish.

Findings

Percocypris pingi has significantly higher levels of glutathione and other antioxidants compared to susceptible fish species.

The skin microbiome of P. pingi is more diverse and lacks parasitic bacteria found in susceptible species.

The microbiome of P. pingi is enriched in fundamental metabolic pathways, while susceptible species show disease-related pathways.

Abstract

Some fish species are naturally more resistant to the parasitic disease “white spot” caused by Ichthyophthirius multifiliis, which is a major problem in fish farming. To understand why, we studied three fish species: the resistant Percocypris pingi and the more susceptible crucian carp and yellow catfish. We discovered that the skin of the resistant P. pingi has a unique combination of features. It contains very high levels of protective antioxidant molecules, especially glutathione, which was dozens of times more abundant than in the other species. At the same time, the community of microbes on its skin is different and more diverse, notably lacking certain parasitic bacteria that are common on the susceptible fish. We conclude that the remarkable disease resistance of P. pingi is due to this powerful one-two punch: a strong antioxidant system working together with a protective skin microbiome. These findings help us understand the natural defense mechanisms that fish can use to fight disease.

Ichthyophthirius multifiliis poses a significant threat to global aquaculture, yet some fish species exhibit remarkable resistance. This study employed a combined LC-MS-based metabolomics and 16S rRNA gene sequencing approach to investigate the intrinsic mechanisms underlying the differential susceptibility of Percocypris pingi, crucian carp, and yellow catfish. Our results revealed distinct skin molecular and microbial profiles in P. pingi associated with its enhanced resilience. Metabolomic analysis identified a significant upregulation of key antioxidants (L-Glutathione reduced, L-Glutathione oxidized, L-Cysteine-glutathione gisulfide, Uric acid, Histamine, N-Acetylhistamine, and scorbic acid) in P. pingi, most notably L-Glutathione reduced, which was 31- and 59-fold higher than in yellow catfish and crucian carp, respectively. Functional enrichment further highlighted the critical role of enhanced antioxidant capacity (centered on glutathione metabolism) and immune/inflammatory responses in the resistance to I. multifiliis of P. pingi. Concurrently, skin microbiome analysis showed that P. pingi hosted a microbial community distinct from the other two species, with significantly higher α-diversity. Notably, P. pingi skin was significantly depleted of the parasitic bacteria Candidatus_Megaira and Candidatus_Midichloria, which were highly abundant in the susceptible species. Furthermore, predicted metagenomic functions indicated that P. pingi’s microbiota was enriched in fundamental metabolic pathways, whereas the microbiota of crucian carp and yellow catfish was skewed towards disease- and immune-related pathways. In conclusion, our findings demonstrate that the superior resistance of P. pingi to I. multifiliis is likely conferred by a synergistic effect of a robust skin antioxidant capacity (primarily driven by glutathione) and a protective skin microbiome that excludes specific parasites. This study provides novel insights into the multi-faceted mechanisms of disease resistance in fish.

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