Cell cycle arrest and biochemical changes accompanying cell death in harmful dinoflagellates following exposure to bacterial algicide IRI-160AA

Pokrzywinski, Kaytee L.; Tilney, Charles L.; Warner, Mark E.; Coyne, Kathryn J.

doi:10.1038/srep45102

Cited by 37 publications

(52 citation statements)

References 56 publications

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“…huxleyi cells appears to mirror previous studies in which cellular arrest has been observed in phytoplankton in response to bacterially derived chemical exposure 19,20,21,22,23 , as well as nutrient limitation 24,25,26 . Indeed, at the physiological level, the response of E. huxleyi to HHQ parallels phosphorus (P) limitation in phytoplankton (i.e.…”

Section: Cell Cyclesupporting

confidence: 85%

Bacterial quorum sensing signal arrests phytoplankton cell division and protects against virus-induced mortality

Pollara¹,

Becker²,

Nunn

et al. 2020

Preprint

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Interactions between phytoplankton and heterotrophic bacteria fundamentally shape marine ecosystems. These interactions are driven by the exchange of compounds, however, linking these chemical signals, their mechanisms of action, and resultant ecological consequences remains a fundamental challenge. The bacterial signal 2-heptyl-4-quinolone (HHQ), induces immediate cellular stasis in the coccolithophore, Emiliania huxleyi, however, the mechanism responsible remains unknown. Here, we show that HHQ exposure leads to the accumulation of DNA damage in phytoplankton and prevents its repair. While this effect is reversible, HHQ-exposed phytoplankton are also protected from viral mortality, ascribing a new role of quorum sensing signals in regulating multi-trophic interactions. Further results demonstrate global HHQ production potential and the first in situ measurements of HHQ which coincide with areas of enhanced micro- and nanoplankton biomass. Our results support bacterial communication signals as emerging players, providing a new mechanistic framework for how compounds may contribute to structure complex marine microbial communities.

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Section: Cell Cyclesupporting

confidence: 85%

Bacterial quorum sensing signal arrests phytoplankton cell division and protects against virus-induced mortality

Pollara¹,

Becker²,

Nunn

et al. 2020

Preprint

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“…PCD can be induced by either a direct action of the polyamines, through their regulatory effect on ion channels (K + , Ca 2+ ), or by an indirect action of their catabolism which produces intermediates such as reactive oxygen species (ROS) like H 2 O 2 , and aminoaldehydes [33]. Since recent work by Pokrwzynsky [23] provides evidence that exposure to IRI-160AA induces PCD to several dinoflagellates, indirect effects of polyamines may be suspected. In plants, the oxidation of putrescine mediated by diamine oxidase yields 4-aminobutanal, H 2 O 2 , and ammonium (NH 4 + ) [34], supporting the hypothesis of a catabolization of putrescine upon release into the medium by Shewanella sp.…”

Section: Discussionmentioning

confidence: 99%

“…Following the catabolization scheme and the metabolites identified in the algicide, toxic effects may thus be attributed to ammonium, H 2 O 2 or 4-aminobutanal. The concentration of hydrogen peroxide in the algicide was not significant according to experiments conducted by Pokrzywinski [23], and may not be further considered as the potential toxic metabolite. The toxicity of ammonium to phytoplanktonic cells has been reviewed by Collos and Harrison [35], and highlight the dinoflagellates as the most sensitive class of unicellular algae, with EC 50 values ranging from 30 to 2700 µM.…”

Section: Discussionmentioning

confidence: 99%

“…Pokrzywinski [16] found that the algicide produced by Shewanella was released into the growth medium. Exposure to this algicide, called IRI-160AA, induced a biochemical response consistent with programmed cell death (PCD) in several species of dinoflagellates [23], accompanied by significant morphological changes [24] and impacts on dinoflagellate photo-physiology [25]. In terms of basic features, IRI-160AA was listed as a “small, hydrophilic, and thermally stable compound” (i.e., SPC [16]), while further characterization of its structure remained unsuccessful.…”

Section: Introductionmentioning

confidence: 99%

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Small Polar Molecules: A Challenge in Marine Chemical Ecology

2018

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Due to increasing evidence of key chemically mediated interactions in marine ecosystems, a real interest in the characterization of the metabolites involved in such intra and interspecific interactions has emerged over the past decade. Nevertheless, only a small number of studies have succeeded in identifying the chemical structure of compounds of interest. One reason for this low success rate is the small size and extremely polar features of many of these chemical compounds. Indeed, a major challenge in the search for active metabolites is the extraction of small polar compounds from seawater. Yet, a full characterization of those metabolites is necessary to understand the interactions they mediate. In this context, the study presented here aims to provide a methodology for the characterization of highly polar, low molecular weight compounds in a seawater matrix that could provide guidance for marine ecologists in their efforts to identify active metabolites. This methodology was applied to the investigation of the chemical structure of an algicidal compound secreted by the bacteria Shewanella sp. IRI-160 that was previously shown to induce programmed cell death in dinoflagellates. The results suggest that the algicidal effects may be attributed to synergistic effects of small amines (ammonium, 4-aminobutanal) derived from the catabolization of putrescine produced in large quantities (0.05–6.5 fmol/cell) by Shewanella sp. IRI-160.

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“…Many algicidal bacteria, such as Acinetobacter (5), Alcaligenes (6), Bacillus (7,8), Deinococcus (9), Hahella (10,11), Mangrovimonas (12), Pseudoalteromonas (13), Pseudomonas (14,15), Streptomyces (16,17), and Vibrio (18,19) species, have the potential to decrease the intensity of HABs. Furthermore, a few algicidal bacteria exhibit broad host ranges and exert effects on a variety of algal species (11,(20)(21)(22).…”

mentioning

confidence: 99%

Algicidal Activity of Novel Marine Bacterium Paracoccus sp. Strain Y42 against a Harmful Algal-Bloom-Causing Dinoflagellate, Prorocentrum donghaiense

Zhang

Chen

et al. 2018

Appl Environ Microbiol

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blooms occur frequently in the Yangtze River estuary and the adjacent East China Sea. These blooms have damaged marine ecosystems and caused enormous economic losses over the past 2 decades. Thus, highly efficient, low-cost, ecofriendly approaches must be developed to control blooms. In this study, a bacterial strain (strain Y42) was identified as sp. and was used to lyse The supernatant of the strain Y42 culture was able to lyse, and the algicidal activity of this Y42 supernatant was stable with different temperatures and durations of light exposure and over a wide pH range. In addition to , Y42 showed high algicidal activity against, , and, suggesting that it targets primarily Pyrrophyta. To clarify the algicidal effects of Y42, we assessed algal lysis and determined the chlorophyll contents, photosynthetic activity, and malondialdehyde contents of after exposure to the Y42 supernatant. Scanning electron microscopy and transmission electron microscopy analyses showed that the Y42 supernatant disrupted membrane integrity and caused algal cell breakage at the megacytic zone. Photosynthetic pigment loss and significant declines in both photosynthetic efficiency and the electron transport rate indicated that the Y42 supernatant damaged the photosynthetic system of Malondialdehyde overproduction indicated that the Y42 supernatant caused lipid peroxidation and oxidative damage to membrane systems in the algal cell, ultimately leading to death. The findings of this study reveal the potential of Y42 to remove algal cells from blooms. is one of the most common dinoflagellate species that form harmful algal blooms, which frequently cause serious ecological pollution and pose health hazards to humans and other animals. Screening for bacteria with high algicidal activity against and studying their algicidal processes and characteristics will contribute to an understanding of their algicidal effects and provide a theoretical basis for preventing algal blooms and reducing their harm to the environment. This study reports the algicidal activity and characteristics of against The stability of the algicidal activity of in different environments (including different temperature, pH, and sunlight conditions) indicates its potential for use in the control of blooms.

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Cell cycle arrest and biochemical changes accompanying cell death in harmful dinoflagellates following exposure to bacterial algicide IRI-160AA

Cited by 37 publications

References 56 publications

Bacterial quorum sensing signal arrests phytoplankton cell division and protects against virus-induced mortality

Bacterial quorum sensing signal arrests phytoplankton cell division and protects against virus-induced mortality

Small Polar Molecules: A Challenge in Marine Chemical Ecology

Algicidal Activity of Novel Marine Bacterium Paracoccus sp. Strain Y42 against a Harmful Algal-Bloom-Causing Dinoflagellate, Prorocentrum donghaiense

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