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Plastoquinone synthesis inhibition by tetrabromo biphenyldiol as a widespread algicidal mechanism of marine bacteria.

ABSTRACT: Algae and bacteria have complex and intimate interactions in the ocean. Besides mutualism, bacteria have evolved a variety of molecular-based anti-algal strategies. However, limited by the unknown mechanism of synthesis and action of these molecules, these strategies and their global prevalence remain unknown. Here we identify a novel strategy through which a marine representative of the Gammaproteobacteria produced 3,3',5,5'-tetrabromo-2,2'-biphenyldiol (4-BP), that kills or inhibits diverse phytoplankton by inhibiting plastoquinone synthesis and its effect cascades to many other key metabolic processes of the algae. Through comparative genomic analysis between the 4-BP-producing bacterium and its algicidally inactive mutant, combined with gene function verification, we identified the gene cluster responsible for 4-BP synthesis, which contains genes encoding chorismate lyase, flavin-dependent halogenase and cytochrome P450. We demonstrated that in near in situ simulated algal blooming seawater, even low concentrations of 4-BP can cause changes in overall phytoplankton community structure with a decline in dinoflagellates and diatoms. Further analyses of the gene sequences from the Tara Oceans expeditions and 2750 whole genome sequences confirmed the ubiquitous presence of 4-BP synthetic genes in diverse bacterial members in the global ocean, suggesting that it is a bacterial tool potentially widely used in global oceans to mediate bacteria-algae antagonistic relationships.

SUBMITTER: Zhang Z

PROVIDER: S-EPMC10579414 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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Plastoquinone synthesis inhibition by tetrabromo biphenyldiol as a widespread algicidal mechanism of marine bacteria.

Zhang Zenghu Z Li Dehai D Xie Ruize R Guo Ruoyu R Nair Shailesh S Han Huan H Zhang Guojian G Zhao Qun Q Zhang Lihua L Jiao Nianzhi N Zhang Yongyu Y

The ISME journal 20230908 11

Algae and bacteria have complex and intimate interactions in the ocean. Besides mutualism, bacteria have evolved a variety of molecular-based anti-algal strategies. However, limited by the unknown mechanism of synthesis and action of these molecules, these strategies and their global prevalence remain unknown. Here we identify a novel strategy through which a marine representative of the Gammaproteobacteria produced 3,3',5,5'-tetrabromo-2,2'-biphenyldiol (4-BP), that kills or inhibits diverse ph ...[more]

PMID: 37679430

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Project description:BackgroundReciprocal exchanges of metabolites between phytoplankton and bacteria influence the fitness of these microorganisms which ultimately shapes the productivity of marine ecosystems. Recent evidence suggests that plant growth-promoting hormones may be key metabolites within mutualistic phytoplankton-bacteria partnerships, but very little is known about the diversity of plant growth-promoting hormones produced by marine bacteria and their specific effects on phytoplankton growth. Here, we aimed to investigate the capacity of marine bacteria to produce 7 plant growth-promoting hormones and the effects of these hormones on Actinocyclus sp. growth.ResultsWe examined the plant growth-promoting hormone synthesis capabilities of 14 bacterial strains that enhance the growth of the common diatom Actinocyclus. Plant growth-promoting hormone biosynthesis was ubiquitous among the bacteria tested. Indeed all 14 strains displayed the genomic potential to synthesise multiple hormones, and mass-spectrometry confirmed that each strain produced at least 6 out of the 7 tested plant growth-promoting hormones. Some of the plant growth-promoting hormones identified here, such as brassinolide and trans-zeatin, have never been reported in marine microorganisms. Importantly, all strains produced the hormone indole-3 acetic acid (IAA) in high concentrations and released it into their surroundings. Furthermore, indole-3 acetic acid extracellular concentrations were positively correlated with the ability of each strain to promote Actinocyclus growth. When inoculated with axenic Actinocyclus cultures, only indole-3 acetic acid and gibberellic acid enhanced the growth of the diatom, with cultures exposed to indole-3 acetic acid exhibiting a two-fold increase in cell numbers.ConclusionOur results reveal that marine bacteria produce a much broader range of plant growth-promoting hormones than previously suspected and that some of these compounds enhance the growth of a marine diatom. These findings suggest plant growth-promoting hormones play a large role in microbial communication and broaden our knowledge of their fuctions in the marine environment. Video Abstract.

Dataset Information

Plastoquinone synthesis inhibition by tetrabromo biphenyldiol as a widespread algicidal mechanism of marine bacteria.

Publications

Plastoquinone synthesis inhibition by tetrabromo biphenyldiol as a widespread algicidal mechanism of marine bacteria.

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