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Comparative analysis of the gut microbiota of wild wintering whooper swans (Cygnus Cygnus), captive black swans (Cygnus Atratus), and mute swans (Cygnus Olor) in Sanmenxia Swan National Wetland Park of China

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Abstract

The gastrointestinal microbiota, a complex ecosystem, is involved in the physiological activities of hosts and the development of diseases. Birds occupy a critical ecological niche in the ecosystem, performing a variety of ecological functions and possessing a complex gut microbiota composition. However, the gut microbiota of wild and captive birds has received less attention in the same region. We profiled the fecal gut microbiome of wild wintering whooper swans (Cygnus Cygnus; Cyg group, n = 25), captive black swans (Cygnus Atratus; Atr group, n = 20), and mute swans (Cygnus Olor; Olor group, n = 30) using 16S rRNA gene sequencing to reveal differences in the gut microbial ecology. The results revealed that the three species of swans differed significantly in terms of the alpha and beta diversity of their gut microbiota, as measured by ACE, Chao1, Simpson and Shannon indices, principal coordinates analysis (PCoA) and non-metricmulti-dimensional scaling (NMDS) respectively. Based on the results of the linear discriminant analysis effect size (LEfSe) and random forest analysis, we found that there were substantial differences in the relative abundance of Gottschalkia, Trichococcus, Enterococcus, and Kurthia among the three groups. Furthermore, an advantageous pattern of interactions between microorganisms was shown by the association network analysis. Among these, Gottschalkia had the higher area under curve (AUC), which was 0.939 (CI = 0.879–0.999), indicating that it might be used as a biomarker to distinguish between wild and captive black swans. Additionally, PICRUSt2 predictions indicated significant differences in gut microbiota functions between wild and captive trumpeter swans, with the gut microbiota functions of Cyg group focusing on carbohydrate metabolism, membrane transport, cofactor, and vitamin metabolism pathways, the Atr group on lipid metabolism, and the Olor group on cell motility, amino acid metabolism, and replication and repair pathways. These findings showed that the gut microbiota of wild and captive swans differed, which is beneficial to understand the gut microecology of swans and to improve regional wildlife conservation strategies.

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Data availability

The sequencing data generated in our study have been deposited in the SRA database and the BioProject ID is PRJNA921745.

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Funding

This study was supported by the National Natural Science Foundation of China (No. 32202876), and the Special Support Fund for High-level Talents of Henan Agricultural University (No. 30501374).

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Junxian Mi: experiment, conceptualization, literature review, and data curation. Kail Liu: experiment, and drafted the manuscript. Wenli Ding: data curation, revision. Minghui Zhang: materials, analysis. Xuefei Wang: reviewed the text. Aftab Shaukat: editing. Mujeeb Ur Rehman: resources. Xilan Jiao: collected the literature. Shucheng Huang: project administration, funding acquisition, review, and editing. All authors contributed to the article and approved the submitted version.

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Correspondence to Shu-Cheng Huang.

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Mi, JX., Liu, KL., Ding, WL. et al. Comparative analysis of the gut microbiota of wild wintering whooper swans (Cygnus Cygnus), captive black swans (Cygnus Atratus), and mute swans (Cygnus Olor) in Sanmenxia Swan National Wetland Park of China. Environ Sci Pollut Res 30, 93731–93743 (2023). https://doi.org/10.1007/s11356-023-28876-0

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  • DOI: https://doi.org/10.1007/s11356-023-28876-0

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