Identification of quorum sensing-regulated Vibrio fortis as potential pathogenic bacteria for coral bleaching and the effects on the microbial shift

Coastal pollution, global warming, ocean acidification, and other reasons lead to the imbalance of the coral reef ecosystem, resulting in the increasingly serious problem of coral degradation. Coral bleaching is often accompanied by structural abnormalities of coral symbiotic microbiota, among which...

Full description

Bibliographic Details
Main Authors: Xiaohui Sun, Yan Li, Qian Yang, Han Zhang, Nuo Xu, Zheng Tang, Shishi Wu, Yusheng Jiang, Hala F. Mohamed, Danyun Ou, Xinqing Zheng
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1116737/full
_version_ 1811173254182731776
author Xiaohui Sun
Yan Li
Qian Yang
Han Zhang
Nuo Xu
Zheng Tang
Shishi Wu
Yusheng Jiang
Hala F. Mohamed
Hala F. Mohamed
Danyun Ou
Danyun Ou
Xinqing Zheng
Xinqing Zheng
Xinqing Zheng
author_facet Xiaohui Sun
Yan Li
Qian Yang
Han Zhang
Nuo Xu
Zheng Tang
Shishi Wu
Yusheng Jiang
Hala F. Mohamed
Hala F. Mohamed
Danyun Ou
Danyun Ou
Xinqing Zheng
Xinqing Zheng
Xinqing Zheng
author_sort Xiaohui Sun
collection DOAJ
description Coastal pollution, global warming, ocean acidification, and other reasons lead to the imbalance of the coral reef ecosystem, resulting in the increasingly serious problem of coral degradation. Coral bleaching is often accompanied by structural abnormalities of coral symbiotic microbiota, among which Vibrio is highly concerned. In this study, Vibrio fortis S10-1 (MCCC 1H00104), isolated from sea cucumber, was used for the bacterial infection on coral Seriatopora guttatus and Pocillopora damicornis. The infection of S10-1 led to coral bleaching and a significant reduction of photosynthetic function in coral holobiont, and the pathogenicity of V. fortis was regulated by quorum sensing. Meanwhile, Vibrio infection also caused a shift of coral symbiotic microbial community, with significantly increased abundant Proteobacteria and Actinobacteria and significantly reduced abundant Firmicutes; on genus level, the abundance of Bacillus decreased significantly and the abundance of Rhodococcus, Ralstonia, and Burkholderia–Caballeronia–Paraburkholderia increased significantly; S10-1 infection also significantly impacted the water quality in the micro-ecosystem. In contrast, S10-1 infection showed less effect on the microbial community of the live stone, which reflected that the microbes in the epiphytic environment of the live stone might have a stronger ability of self-regulation; the algal symbionts mainly consisted of Cladocopium sp. and showed no significant effect by the Vibrio infection. This study verified that V. fortis is the primary pathogenic bacterium causing coral bleaching, revealed changes in the microbial community caused by its infection, provided strong evidence for the “bacterial bleaching” hypothesis, and provided an experimental experience for the exploration of the interaction mechanism among microbial communities, especially coral-associated Vibrio in the coral ecosystem, and potential probiotic strategy or QS regulation on further coral disease control.
first_indexed 2024-04-10T17:44:35Z
format Article
id doaj.art-ad8ac7b236754b05acf46306bdddd4e3
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-04-10T17:44:35Z
publishDate 2023-02-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-ad8ac7b236754b05acf46306bdddd4e32023-02-03T05:32:02ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-02-011410.3389/fmicb.2023.11167371116737Identification of quorum sensing-regulated Vibrio fortis as potential pathogenic bacteria for coral bleaching and the effects on the microbial shiftXiaohui Sun0Yan Li1Qian Yang2Han Zhang3Nuo Xu4Zheng Tang5Shishi Wu6Yusheng Jiang7Hala F. Mohamed8Hala F. Mohamed9Danyun Ou10Danyun Ou11Xinqing Zheng12Xinqing Zheng13Xinqing Zheng14College of Chemical Engineering, Huaqiao University, Xiamen, ChinaThird Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaCollege of Chemical Engineering, Huaqiao University, Xiamen, ChinaThird Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaCollege of Chemical Engineering, Huaqiao University, Xiamen, ChinaCollege of Chemical Engineering, Huaqiao University, Xiamen, ChinaCollege of Chemical Engineering, Huaqiao University, Xiamen, ChinaCollege of Chemical Engineering, Huaqiao University, Xiamen, ChinaThird Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaBotany and Microbiology Department (Girls Branch), Faculty of Science, Al-Azhar University, Cairo, EgyptThird Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaKey Laboratory of Marine Ecological Conservation and Restoration, Ministry of Natural Resources, Xiamen, ChinaThird Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaKey Laboratory of Marine Ecological Conservation and Restoration, Ministry of Natural Resources, Xiamen, ChinaObservation and Research Station of Coastal Wetland Ecosystem in Beibu Gulf, Ministry of Natural Resources, Xiamen, ChinaCoastal pollution, global warming, ocean acidification, and other reasons lead to the imbalance of the coral reef ecosystem, resulting in the increasingly serious problem of coral degradation. Coral bleaching is often accompanied by structural abnormalities of coral symbiotic microbiota, among which Vibrio is highly concerned. In this study, Vibrio fortis S10-1 (MCCC 1H00104), isolated from sea cucumber, was used for the bacterial infection on coral Seriatopora guttatus and Pocillopora damicornis. The infection of S10-1 led to coral bleaching and a significant reduction of photosynthetic function in coral holobiont, and the pathogenicity of V. fortis was regulated by quorum sensing. Meanwhile, Vibrio infection also caused a shift of coral symbiotic microbial community, with significantly increased abundant Proteobacteria and Actinobacteria and significantly reduced abundant Firmicutes; on genus level, the abundance of Bacillus decreased significantly and the abundance of Rhodococcus, Ralstonia, and Burkholderia–Caballeronia–Paraburkholderia increased significantly; S10-1 infection also significantly impacted the water quality in the micro-ecosystem. In contrast, S10-1 infection showed less effect on the microbial community of the live stone, which reflected that the microbes in the epiphytic environment of the live stone might have a stronger ability of self-regulation; the algal symbionts mainly consisted of Cladocopium sp. and showed no significant effect by the Vibrio infection. This study verified that V. fortis is the primary pathogenic bacterium causing coral bleaching, revealed changes in the microbial community caused by its infection, provided strong evidence for the “bacterial bleaching” hypothesis, and provided an experimental experience for the exploration of the interaction mechanism among microbial communities, especially coral-associated Vibrio in the coral ecosystem, and potential probiotic strategy or QS regulation on further coral disease control.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1116737/fullcoral bleachingVibrio fortissymbiotic microbesbacterial infectionmicrobial shift
spellingShingle Xiaohui Sun
Yan Li
Qian Yang
Han Zhang
Nuo Xu
Zheng Tang
Shishi Wu
Yusheng Jiang
Hala F. Mohamed
Hala F. Mohamed
Danyun Ou
Danyun Ou
Xinqing Zheng
Xinqing Zheng
Xinqing Zheng
Identification of quorum sensing-regulated Vibrio fortis as potential pathogenic bacteria for coral bleaching and the effects on the microbial shift
Frontiers in Microbiology
coral bleaching
Vibrio fortis
symbiotic microbes
bacterial infection
microbial shift
title Identification of quorum sensing-regulated Vibrio fortis as potential pathogenic bacteria for coral bleaching and the effects on the microbial shift
title_full Identification of quorum sensing-regulated Vibrio fortis as potential pathogenic bacteria for coral bleaching and the effects on the microbial shift
title_fullStr Identification of quorum sensing-regulated Vibrio fortis as potential pathogenic bacteria for coral bleaching and the effects on the microbial shift
title_full_unstemmed Identification of quorum sensing-regulated Vibrio fortis as potential pathogenic bacteria for coral bleaching and the effects on the microbial shift
title_short Identification of quorum sensing-regulated Vibrio fortis as potential pathogenic bacteria for coral bleaching and the effects on the microbial shift
title_sort identification of quorum sensing regulated vibrio fortis as potential pathogenic bacteria for coral bleaching and the effects on the microbial shift
topic coral bleaching
Vibrio fortis
symbiotic microbes
bacterial infection
microbial shift
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1116737/full
work_keys_str_mv AT xiaohuisun identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT yanli identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT qianyang identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT hanzhang identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT nuoxu identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT zhengtang identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT shishiwu identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT yushengjiang identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT halafmohamed identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT halafmohamed identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT danyunou identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT danyunou identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT xinqingzheng identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT xinqingzheng identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift
AT xinqingzheng identificationofquorumsensingregulatedvibriofortisaspotentialpathogenicbacteriaforcoralbleachingandtheeffectsonthemicrobialshift