Impact of Polyonchobothrium magnum on health and gut microbial ecology of African catfish (Clarias gariepinus): Insights from morphological, molecular, and microbiological analyses.

Abstract

Parasites pose significant challenges to aquaculture and fisheries industries. Our study focuses on the Polyonchobothrium magnum and African catfish to address a potential health issue in aquaculture, explore host-parasite interactions that can help develop effective management practices to ensure fish health and industry sustainability. P. magnum was isolated from the stomach of African catfish (Clarias gariepinus) as the primary site of infection, with a prevalence of 10%. Most affected fish were heavily infected (8 out of 10). Infection was confirmed by sequencing the PCR-targeted region of the nicotinamide adenine dinucleotide dehydrogenase subunit 1 (ND1) gene, along with light and scanning electron microscopes. The parasite had an elongated scolex with deep bothria, a prominent apical disc wider than the scolex itself, and a four-lobed appearance. The scolex contained a central rostellum divided into two semicircles, bearing 26-30 hooks, with an average of 28. The apical disc had large hooks arranged in four quadrants, with 6-8 hooks each, averaging 7 per quadrant. No neck was observed. Phylogenetic analysis of our sequence showed a 100% match with isolates from Guangzhou, China. In infected fish, the anterior kidney showed increased expression levels of nuclear factor kappa B and lysozyme, but decreased levels of in major histocompatibility complex antigen II. Plasma analysis revealed a significant drop in superoxide dismutase, a rise in interleukin-1 beta, and lower IgM levels compared to non-infected controls. Non-infected fish displayed greater gut microbiota diversity, with dominant families including Moraxellaceae, Enterobacteriaceae, Fusobacteriaceae, and Caulobacteraceae, and prevalent genera such as Acinetobacter, Cetobacterium, and Brevundimonas. In contrast, infected fish exhibited very low diversity, with significantly higher proportions of Enterobacteriaceae (45.99%) and Aeromonadaceae (41.79%) compared to non-infected fish, which had 13.76% and 3.64% respectively. Cetobacterium somerae was prevalent in non-infected fish, while infected fish harboured Aeromonas fluvialis, Plesiomonas shigelloides, and Gallaecimonas xiamenensis. Overall, P. magnum disrupted the immune status and gut microbiota of the host, thereby impacting its health.