Noctiluca scintillans bloom alters the composition and carbohydrate utilization of associated bacterial community and enriches potential pathogenic bacterium Vibrio anguillarum
Noctiluca scintillans (red) is a widely distributed heterotrophic dinoflagellate and a prominent red tide forming species. This study investigated the effects of Noctiluca blooms on marine microbial diversity and functionality using multi-omics approaches. Our findings revealed significant differenc...
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Published in | Water research (Oxford) Vol. 249; p. 120974 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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England
01.02.2024
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Abstract | Noctiluca scintillans (red) is a widely distributed heterotrophic dinoflagellate and a prominent red tide forming species. This study investigated the effects of Noctiluca blooms on marine microbial diversity and functionality using multi-omics approaches. Our findings revealed significant differences in the community composition of Noctiluca-associated bacteria compared to those associated with autotrophic plankton and free-living bacteria in the surrounding seawater. The dominant bacterial groups within the Noctiluca-associated community shifted at various bloom stages, which could be attributed to changes in prey composition of Noctiluca. During the non-bloom stage, Burkholderiaceae, Carnobacteriaceae, and Pseudomonadaceae dominated the community, while Vibrionaceae became dominant during the bloom stage, and Saprospiraceae, Crocinitomicaceae, and Pirellulaceae thrived during the post-bloom stage. Compared to the non-bloom stage, Noctiluca-associated bacterial community at the bloom stage exhibited significant down-regulation of genes related to complex carbohydrate metabolism, while up-regulation of genes related to glucose transportation and utilization. Furthermore, we identified Vibrio anguillarum, a potential pathogenic bacterium to marine fish, as a major component of the Vibrionaceae family during the bloom stage. The occurrence of V. anguillarum associated with Noctiluca blooms may be attributed to the increased availability of its preferred carbon sources and its high capabilities in glucose transportation, motility and chemotaxis. Moreover, the presence of Vibrio infection genes (hap, hlyA, rtxA) encoding vibriolysin, hemolysin, and RTX (Repeats-in-toxin) toxin in the V. anguillarum genome, with the hap gene showing high expression levels during Noctiluca blooms, indicates an elevated risk of infection. This study underscores the unique composition of the bacterial community associated with red tide forming heterotrophic dinoflagellates and suggests that Noctiluca cells may serve as reservoirs and vectors for pathogenic bacteria, potentially posing a threat to fish-farming and the health of other marine organisms. |
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AbstractList | Noctiluca scintillans (red) is a widely distributed heterotrophic dinoflagellate and a prominent red tide forming species. This study investigated the effects of Noctiluca blooms on marine microbial diversity and functionality using multi-omics approaches. Our findings revealed significant differences in the community composition of Noctiluca-associated bacteria compared to those associated with autotrophic plankton and free-living bacteria in the surrounding seawater. The dominant bacterial groups within the Noctiluca-associated community shifted at various bloom stages, which could be attributed to changes in prey composition of Noctiluca. During the non-bloom stage, Burkholderiaceae, Carnobacteriaceae, and Pseudomonadaceae dominated the community, while Vibrionaceae became dominant during the bloom stage, and Saprospiraceae, Crocinitomicaceae, and Pirellulaceae thrived during the post-bloom stage. Compared to the non-bloom stage, Noctiluca-associated bacterial community at the bloom stage exhibited significant down-regulation of genes related to complex carbohydrate metabolism, while up-regulation of genes related to glucose transportation and utilization. Furthermore, we identified Vibrio anguillarum, a potential pathogenic bacterium to marine fish, as a major component of the Vibrionaceae family during the bloom stage. The occurrence of V. anguillarum associated with Noctiluca blooms may be attributed to the increased availability of its preferred carbon sources and its high capabilities in glucose transportation, motility and chemotaxis. Moreover, the presence of Vibrio infection genes (hap, hlyA, rtxA) encoding vibriolysin, hemolysin, and RTX (Repeats-in-toxin) toxin in the V. anguillarum genome, with the hap gene showing high expression levels during Noctiluca blooms, indicates an elevated risk of infection. This study underscores the unique composition of the bacterial community associated with red tide forming heterotrophic dinoflagellates and suggests that Noctiluca cells may serve as reservoirs and vectors for pathogenic bacteria, potentially posing a threat to fish-farming and the health of other marine organisms. |
ArticleNumber | 120974 |
Author | Tan, Yehui Cheung, Shunyan Leung, Sze Ki Xu, Huo Lu, Yanhong Liu, Hongbin Zhang, Shuwen Xia, Xiaomin Gu, Bowei Li, Yang Shi, Zhiyuan Zeng, Huijun |
Author_xml | – sequence: 1 givenname: Xiaomin surname: Xia fullname: Xia, Xiaomin email: xiaxiaomin@scsio.ac.cn organization: Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China; University of Chinese Academy of Sciences, Beijing, China; Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, China. Electronic address: xiaxiaomin@scsio.ac.cn – sequence: 2 givenname: Shunyan surname: Cheung fullname: Cheung, Shunyan organization: Division of Life Science, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong SAR, China – sequence: 3 givenname: Shuwen surname: Zhang fullname: Zhang, Shuwen email: shuwen@m.scnu.edu.cn organization: Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, South China Normal University, Guangzhou, China. Electronic address: shuwen@m.scnu.edu.cn – sequence: 4 givenname: Yanhong surname: Lu fullname: Lu, Yanhong organization: Department of Ocean Science, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong SAR, China – sequence: 5 givenname: Sze Ki surname: Leung fullname: Leung, Sze Ki organization: Department of Ocean Science, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong SAR, China – sequence: 6 givenname: Zhiyuan surname: Shi fullname: Shi, Zhiyuan organization: Department of Ocean Science, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong SAR, China – sequence: 7 givenname: Huo surname: Xu fullname: Xu, Huo organization: Department of Ocean Science, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong SAR, China – sequence: 8 givenname: Bowei surname: Gu fullname: Gu, Bowei organization: Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China – sequence: 9 givenname: Yehui surname: Tan fullname: Tan, Yehui organization: Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China; University of Chinese Academy of Sciences, Beijing, China; Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, China – sequence: 10 givenname: Huijun surname: Zeng fullname: Zeng, Huijun organization: Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, South China Normal University, Guangzhou, China – sequence: 11 givenname: Yang surname: Li fullname: Li, Yang organization: Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, South China Normal University, Guangzhou, China – sequence: 12 givenname: Hongbin surname: Liu fullname: Liu, Hongbin email: liuhb@ust.hk organization: Division of Life Science, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong SAR, China; Department of Ocean Science, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong SAR, China. Electronic address: liuhb@ust.hk |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38101044$$D View this record in MEDLINE/PubMed |
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Keywords | Vibrio anguillarum Algal bloom Noctiluca scintillans Associated bacteria Pathogenic bacterium |
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