Midgut microbiota affects the intestinal barrier by producing short-chain fatty acids in Apostichopus japonicus

Mingshan Song; Zhen Zhang; Yanan Li; Yangxi Xiang; Chenghua Li

doi:10.3389/fmicb.2023.1263731

Midgut microbiota affects the intestinal barrier by producing short-chain fatty acids in Apostichopus japonicus

Front Microbiol. 2023 Oct 17:14:1263731. doi: 10.3389/fmicb.2023.1263731. eCollection 2023.

Authors

Mingshan Song¹, Zhen Zhang¹, Yanan Li¹, Yangxi Xiang¹, Chenghua Li^{1

2}

Affiliations

¹ State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, China.
² Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China.

Abstract

Introduction: The intestinal microbiota participates in host physiology and pathology through metabolites, in which short-chain fatty acids (SCFAs) are considered principal products and have extensive influence on intestine homeostasis. It has been reported that skin ulceration syndrome (SUS), the disease of Apostichopus japonicus caused by Vibrio splendidus, is associated with the alteration of the intestinal microbiota composition.

Method: To investigate whether the intestinal microbiota affects A. japonicus health via SCFAs, in this study, we focus on the SCFA profiling and intestinal barrier function in A. japonicus treated with V. splendidus.

Results and discussion: We found that V. splendidus could destroy the mid-intestine integrity and downregulate the expression of tight junction proteins ZO-1 and occludin in A. japonicus, which further dramatically decreased microorganism abundance and altered SCFAs contents. Specifically, acetic acid is associated with the largest number of microorganisms and has a significant correlation with occludin and ZO-1 among the seven SCFAs. Furthermore, our findings showed that acetic acid could maintain the intestinal barrier function by increasing the expression of tight junction proteins and rearranging the tight junction structure by regulating F-actin in mid-intestine epithelial cells. Thus, our results provide insights into the effects of the gut microbiome and SCFAs on intestine barrier homeostasis and provide essential knowledge for intervening in SUS by targeting metabolites or the gut microbiota.

Keywords: Apostichopus japonicus; Vibrio splendidus; acetic acid; intestinal permeability; short-chain fatty acids.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was supported by the National Natural Science Foundation of China (42106122 and 32073003) and KC Wong Magna Fund in Ningbo University.