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 inWater research (Oxford) Vol. 249; p. 120974
Main Authors Xia, Xiaomin, Cheung, Shunyan, Zhang, Shuwen, Lu, Yanhong, Leung, Sze Ki, Shi, Zhiyuan, Xu, Huo, Gu, Bowei, Tan, Yehui, Zeng, Huijun, Li, Yang, Liu, Hongbin
Format Journal Article
LanguageEnglish
Published 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.
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
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  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
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  givenname: Sze Ki
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  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
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Keywords Vibrio anguillarum
Algal bloom
Noctiluca scintillans
Associated bacteria
Pathogenic bacterium
Language English
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Snippet Noctiluca scintillans (red) is a widely distributed heterotrophic dinoflagellate and a prominent red tide forming species. This study investigated the effects...
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Title Noctiluca scintillans bloom alters the composition and carbohydrate utilization of associated bacterial community and enriches potential pathogenic bacterium Vibrio anguillarum
URI https://www.ncbi.nlm.nih.gov/pubmed/38101044
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