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Dysbiosis of intestinal homeostasis contribute to Whitmania pigra edema disease
Authors:Caijiao Dai  Xin Chen  Shiyu Qian  Yihui Fan  Lijuan Li  Junfa Yuan
Institution:1. Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, China

National Aquatic Animal Diseases Para-reference laboratory (HZAU), Wuhan, China

Contribution: ?Investigation (lead), Writing - original draft (lead);2. Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, China

National Aquatic Animal Diseases Para-reference laboratory (HZAU), Wuhan, China

Contribution: ?Investigation (equal), Methodology (equal);3. Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, China

Hubei Engineering Research Centre for Aquatic Animal Diseases Control and Prevention, Wuhan, China

Contribution: Methodology (equal), Software (equal);4. Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, China

Hubei Engineering Research Centre for Aquatic Animal Diseases Control and Prevention, Wuhan, China

Contribution: Methodology (equal);5. Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, China

National Aquatic Animal Diseases Para-reference laboratory (HZAU), Wuhan, China

Hubei Engineering Research Centre for Aquatic Animal Diseases Control and Prevention, Wuhan, China

Contribution: Writing - review & editing (equal);6. Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, China

Abstract:Whitmania pigra is widely used in traditional Chinese medicine. However, W. pigra is being threatened by an edema disease with unknown causes (WPE). In this study, a comprehensive exploration of virome, microbiome, and metabolome aberrations in the intestine of W. pigra was performed to address the aetiology of WPE. Virome analysis indicated that eukaryotic viruses did not contribute to WPE, whereas an expansion of Caudovirales was observed in WPE. Compared to the control, the microbial richness and diversity in diseased W. pigra decreased remarkably. Nine genera, including Aeromonas, Anaerotruncus, Vibrio, Proteocatella, Acinetobacter, and Brachyspira were overrepresented in WPE, whereas eleven genera, including Bifidobacterium, Phascolarctobacterium, Lactobacillus, Bacillus and AF12, were enriched in healthy individuals. Furthermore, certain metabolites, especially amino acids, short-chain fatty acids, and bile acids, were found to be linked to intestinal microbiota alterations in WPE. An integration of the microbiome and metabolome in WPE found that dysbiosis of the gut microbiota or metabolites caused WPE. Notably, W. pigra accepted intestinal microbiota transplantation from WPE donors developed WPE clinical signs eventually, and the dysbiotic intestinal microbiota can be recharacterized in this recipient W. pigra. Strikingly, pathological features of metanephridium and uraemic toxin enrichment in the gut indicated a putative interconnection between the gut and metanephridium in WPE, which represents the prototype of the gut–kidney axis in mammals. These finding exemplify the conservation of “microecological Koch's postulates” from annelids to insects and other vertebrates, which provides a direction of prevention and treatment for WPE and opens a new insight into the pathogenesis of aquatic animal diseases from an ecological perspective.
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