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Effects of underwater and semi-aquatic environments on gut tissue and microbiota of the mudskipper Boleophthalmus pectinirostris

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Abstract

In both underwater and semi-aquatic environments, the gut microbiota is of particular physiological importance for amphibious animals, given that the gut tract is among those organs in direct communication with the external environment. In this study, we examined the effects of these contrasting environments on the dominant bacteria in the guts of the amphibious mudskipper Boleophthalmus pectinirostris. Compared with the guts of normal mudskippers, in which the dominant bacteria were identified as Vibrio and Faecalibacterium, we found that Acinetobacter, Shigella, and Bacillus predominated in their guts after exposure to the semi-aquatic environment, whereas Escherichia, Bacteroides, and Bacillus were more prevalent in the guts in the underwater environment. The total number of cultured gut bacteria decreased significantly in the semi-aquatic environment. In semi-aquatic mudskippers, we also detected reductions and increases in the length and width of gut villi, respectively, whereas the width of gut villi declined and the number of goblet cells increased significantly in mudskippers maintained underwater. The mRNA expression of multiple gut transporters for glucose, long-chain fatty acids, and amino acids was found to increase markedly in both underwater and semi-aquatic environments, with the expression of most transporters being significantly higher in those mudskippers exposed to an underwater environment. Furthermore, we detected significant increases in the mRNA expression of pro-inflammatory cytokine transcripts in the guts of both underwater and semi-aquatic mudskippers on days 2, 4, and 6 of exposure, whereas the expression of IL-10 and TGFβ mRNA was more pronounced on days 4 and 8, respectively. Comparatively, we found that expression levels of cytokines in the guts of underwater mudskipper were substantially higher than those in the guts of semi-aquatic mudskippers. Collectively, our findings revealed notable differences in the gut microbiota and energy metabolism requirements of mudskippers exposed to underwater and semi-aquatic conditions, thereby providing a theoretical basis explaining the maintenance of a homeostatic state in mudskippers that constantly transition between these contrasting amphibious habitats.

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Acknowledgements

This work was supported by the Natural Science Foundation of Zhejiang Province (NO. LY17C010001); Natural Science Foundation of Ningbo (NO. 2017A610287); Food Science and Engineering Key Discipline of Ningbo Higher Education (NO. 2019FSEKDNB001); Zhejiang Provincial Top Discipline of Biological Engineering (Level A) (NO. CX2019014); College Student Technological Creativity Program (NO. 2019R420015).

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  1. College of Biological and Environmental Sciences, Zhejiang Wanli University, Ningbo, 315100, Zhejiang, China

    Feng Guan, Liqin Shen, Zhuo Chen, Chen Yu, Jie Zhang & Yongjun Yuan

  2. Ningbo Academy of Product and Food Quality Inspection (Ningbo Fibre Inspection Institute), Ningbo, 315048, Zhejiang, China

    Xiaxia Zhou

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  1. Feng Guan
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Correspondence to Yongjun Yuan.

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Guan, F., Shen, L., Zhou, X. et al. Effects of underwater and semi-aquatic environments on gut tissue and microbiota of the mudskipper Boleophthalmus pectinirostris. J Comp Physiol B 191, 741–753 (2021). https://doi.org/10.1007/s00360-021-01380-y

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  • DOI: https://doi.org/10.1007/s00360-021-01380-y

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