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. 2022 Jul 18;43(4):648-665.
doi: 10.24272/j.issn.2095-8137.2022.159.

Prior exposure to ciprofloxacin disrupts intestinal homeostasis and predisposes ayu ( Plecoglossus altivelis) to subsequent Pseudomonas plecoglossicida-induced infection

Xiang-Yu Wu  1   2   3 , Jin-Bo Xiong  1   2   3 , Chen-Jie Fei  1   2   3 , Ting Dai  1   2   3 , Ting-Fang Zhu  1   2   3 , Zi-Yue Zhao  1   2   3 , Jing Pan  1   2   3 , Li Nie  1   2   4 , Jiong Chen  1   2   5
Affiliations

Prior exposure to ciprofloxacin disrupts intestinal homeostasis and predisposes ayu ( Plecoglossus altivelis) to subsequent Pseudomonas plecoglossicida-induced infection

Xiang-Yu Wu et al. Zool Res. .

Abstract
in English, Chinese

With the rapid development of intensive farming, the aquaculture industry uses a great many antibiotics for the prevention and treatment of bacterial diseases. Despite their therapeutic functions, the overuse and accumulation of antibiotics also pose a threat to aquaculture organisms. In the present study, ayu ( Plecoglossus altivelis) was used as a fish model to study the impacts of ciprofloxacin (CIP) overuse on intestinal homeostasis and immune response during subsequent Pseudomonas plecoglossicida infection. Based on 16S rRNA gene amplification and Illumina sequencing, we found that CIP pre-exposure caused significant variation in intestinal microbiota, including increased species richness, altered microbiota composition and interaction networks, and increased metabolic dysfunction. Furthermore, immunohistochemical analysis indicated that CIP pre-exposure resulted in severe mucosal layer damage, goblet cell reduction, and epithelial cell necrosis of the intestinal barrier in infected ayu. Quantitative real-time polymerase chain reaction (qRT-PCR) showed that disruption of intestinal homeostasis impaired systemic anti-infection immune responses in the intestine, gill, spleen, and head kidney, while inhibiting IL-1β, TNF-α, and IL-10 expression and promoting TGF-β expression. Our findings indicated that CIP administration can directly affect intestinal microbiota composition and intestinal integrity in ayu fish. This perturbation of intestinal homeostasis is likely responsible for the lower survival rate of hosts following subsequent infection as the capacity to mount an effective immune response is compromised. This study also provides preliminary clues for understanding the effects of antibiotic overuse on higher vertebrates through trophic transfer.

随着水产养殖规模的不断扩大，集约化程度不断提高，大面积细菌病的爆发已成为制约其健康可持续发展的因素之一。抗生素是目前水产养殖业病害防治的主要途径。然而，其过度使用和在水环境中的积累也对水生生物造成了巨大威胁。该研究利用香鱼为鱼类模型，采用广谱抗生素环丙沙星预处理香鱼后进行杀香鱼假单胞菌攻毒实验，探究水产养殖业环丙沙星的过度使用对香鱼肠道稳态和杀香鱼假单胞菌感染机体免疫应答的影响。基于16S rRNA 基因高通量测序发现，环丙沙星暴露会引起香鱼肠道微生物菌群的显著变化，包括：肠道菌群多样性增加，菌群组成、菌群的网络拓扑结构和代谢功能基因的改变。进一步免疫组化分析显示，环丙沙星暴露会导致杀香鱼假单胞菌感染香鱼肠道粘膜严重损伤、杯状细胞数目显著减少、肠道上皮细胞大量坏死。此外，损伤的肠道稳态还影响了感染香鱼主要免疫组织，肠道、鳃、脾脏及头肾免疫基因的表达，整体表现为 IL-1β, TNF-α 及 IL-10的表达被显著抑制， TGF-β的表达被显著诱导。综上，该研究系统阐明了环丙沙星暴露会直接影响香鱼肠道菌群的组成和肠道结构的完整性，并进一步导致被感染香鱼免疫应答的削弱及死亡率的增加。同时，该研究也将为后续评估水产养殖业抗生素过度使用对高等生物的影响提供新的角度。.

Keywords: Ayu; Ciprofloxacin; Immune responses; Intestinal barrier; Microbiota.

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Figures

Figure 1
Figure 1
Schematic showing specific procedures and sampling times of each group
Figure 2
Figure 2
CIP exposure affects survival and pathogen abundance of P. plecoglossicida-infected ayu
Figure 3
Figure 3
Effects of CIP exposure on alpha diversity of P. plecoglossicida-infected ayu microbiota
Figure 4
Figure 4
Effects of CIP exposure on intestinal microbial community in P. plecoglossicida-infected ayu
Figure 5
Figure 5
Effects of CIP exposure on the co-occurrence patterns of the intestinal microbiota in P. plecoglossicida-infected ayu
Figure 6
Figure 6
Interspecies interactions of pathogen-host taxa in ayu intestinal microbiota
Figure 7
Figure 7
Predicted functions of intestinal microbiota of ayu after CIP exposure and P. plecoglossicida infection
Figure 8
Figure 8
Intestinal histological changes in ayu after CIP and P. plecoglossicida administration
Figure 9
Figure 9
CIP exposure shapes immune responses of P. plecoglossicida-infected ayu
Figure 10
Figure 10
Effects of CIP contamination on intestinal homeostasis and immune responses of P. plecoglossicida-infected ayu
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