<i>Vibrio splendidus</i> AJ01 Promotes Pathogenicity via L-Glutamic Acid

<i>Vibrio splendidus</i> is a pathogen that infects a wide range of hosts, especially the sea cucumber species <i>Apostichopus japonicus</i>. Previous studies showed that the level of L-glutamic acid (L-Glu) significantly increased under heat stress, and it was found to be on...

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Main Authors: Ya Li, Weibo Shi, Weiwei Zhang
Format: Article
Language:English
Published: MDPI AG 2023-09-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/11/9/2333
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author Ya Li
Weibo Shi
Weiwei Zhang
author_facet Ya Li
Weibo Shi
Weiwei Zhang
author_sort Ya Li
collection DOAJ
description <i>Vibrio splendidus</i> is a pathogen that infects a wide range of hosts, especially the sea cucumber species <i>Apostichopus japonicus</i>. Previous studies showed that the level of L-glutamic acid (L-Glu) significantly increased under heat stress, and it was found to be one of the best carbon sources used by <i>V. splendidus</i> AJ01. In this study, the effects of exogenous L-Glu on the coelomocyte viability, tissue status, and individual mortality of sea cucumbers were analyzed. The results showed that 10 mM of L-Glu decreased coelomocyte viability and increased individual mortality, with tissue rupture and pyknosis, while 0.1 mM of L-Glu slightly affected the survival of sea cucumbers without obvious damage at the cellular and tissue levels. Transcriptomic analysis showed that exogenous L-Glu upregulated 343 and downregulated 206 genes. Gene Ontology (GO) analysis showed that differentially expressed genes (DEGs) were mainly enriched in signaling and membrane formation, while a Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis showed that DEGs were significantly enriched in the upregulated endocytosis and downregulated lysosomal pathways. The coelomocyte viability further decreased by 20% in the simultaneous presence of exogenous L-Glu and <i>V. splendidus</i> AJ01 compared with that in the presence of <i>V. splendidus</i> AJ01 infection alone. Consequently, a higher sea cucumber mortality was also observed in the presence of exogenous L-Glu challenged by <i>V. splendidus</i> AJ01. Real-time reverse transcriptase PCR showed that L-Glu specifically upregulated the expression of the <i>fliC</i> gene coding the subunit protein of the flagellar filament, promoting the swimming motility activity of <i>V. splendidus</i>. Our results indicate that L-Glu should be kept in a state of equilibrium, and excess L-Glu at the host–pathogen interface prompts the virulence of <i>V. splendidus</i> via the increase of bacterial motility.
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spelling doaj.art-77dc7bd2bf1b4460aed3001f918477442023-11-19T12:03:53ZengMDPI AGMicroorganisms2076-26072023-09-01119233310.3390/microorganisms11092333<i>Vibrio splendidus</i> AJ01 Promotes Pathogenicity via L-Glutamic AcidYa Li0Weibo Shi1Weiwei Zhang2Collaborative Innovation Center for Zhejiang Marine High-Efficiency and Healthy Aquaculture, Ningbo University, Ningbo 315832, ChinaCollaborative Innovation Center for Zhejiang Marine High-Efficiency and Healthy Aquaculture, Ningbo University, Ningbo 315832, ChinaCollaborative Innovation Center for Zhejiang Marine High-Efficiency and Healthy Aquaculture, Ningbo University, Ningbo 315832, China<i>Vibrio splendidus</i> is a pathogen that infects a wide range of hosts, especially the sea cucumber species <i>Apostichopus japonicus</i>. Previous studies showed that the level of L-glutamic acid (L-Glu) significantly increased under heat stress, and it was found to be one of the best carbon sources used by <i>V. splendidus</i> AJ01. In this study, the effects of exogenous L-Glu on the coelomocyte viability, tissue status, and individual mortality of sea cucumbers were analyzed. The results showed that 10 mM of L-Glu decreased coelomocyte viability and increased individual mortality, with tissue rupture and pyknosis, while 0.1 mM of L-Glu slightly affected the survival of sea cucumbers without obvious damage at the cellular and tissue levels. Transcriptomic analysis showed that exogenous L-Glu upregulated 343 and downregulated 206 genes. Gene Ontology (GO) analysis showed that differentially expressed genes (DEGs) were mainly enriched in signaling and membrane formation, while a Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis showed that DEGs were significantly enriched in the upregulated endocytosis and downregulated lysosomal pathways. The coelomocyte viability further decreased by 20% in the simultaneous presence of exogenous L-Glu and <i>V. splendidus</i> AJ01 compared with that in the presence of <i>V. splendidus</i> AJ01 infection alone. Consequently, a higher sea cucumber mortality was also observed in the presence of exogenous L-Glu challenged by <i>V. splendidus</i> AJ01. Real-time reverse transcriptase PCR showed that L-Glu specifically upregulated the expression of the <i>fliC</i> gene coding the subunit protein of the flagellar filament, promoting the swimming motility activity of <i>V. splendidus</i>. Our results indicate that L-Glu should be kept in a state of equilibrium, and excess L-Glu at the host–pathogen interface prompts the virulence of <i>V. splendidus</i> via the increase of bacterial motility.https://www.mdpi.com/2076-2607/11/9/2333<i>Vibrio splendidus</i>L-Glutranscriptomic analysisvirulence
spellingShingle Ya Li
Weibo Shi
Weiwei Zhang
<i>Vibrio splendidus</i> AJ01 Promotes Pathogenicity via L-Glutamic Acid
Microorganisms
<i>Vibrio splendidus</i>
L-Glu
transcriptomic analysis
virulence
title <i>Vibrio splendidus</i> AJ01 Promotes Pathogenicity via L-Glutamic Acid
title_full <i>Vibrio splendidus</i> AJ01 Promotes Pathogenicity via L-Glutamic Acid
title_fullStr <i>Vibrio splendidus</i> AJ01 Promotes Pathogenicity via L-Glutamic Acid
title_full_unstemmed <i>Vibrio splendidus</i> AJ01 Promotes Pathogenicity via L-Glutamic Acid
title_short <i>Vibrio splendidus</i> AJ01 Promotes Pathogenicity via L-Glutamic Acid
title_sort i vibrio splendidus i aj01 promotes pathogenicity via l glutamic acid
topic <i>Vibrio splendidus</i>
L-Glu
transcriptomic analysis
virulence
url https://www.mdpi.com/2076-2607/11/9/2333
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