Phaeobacter inhibens induces apoptosis-like programmed cell death in calcifying Emiliania huxleyi

Bramucci, Anna R.; Case, Rebecca J.

doi:10.1038/s41598-018-36847-6

Cited by 29 publications

(30 citation statements)

References 83 publications

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“…S2). Taken together, HHQ-treated E. huxleyi cells appear to mirror previous studies in which cellular arrest has been observed in phytoplankton in response to bacterially derived chemical exposure (17,18,(27)(28)(29) as well as nutrient limitation (20)(21)(22). In order to elucidate if the observed cellular stasis is mechanistically similar to those observed previously in the literature, we conducted cell cycle, transcriptomic, and proteomic analyses of HHQ-exposed E. huxleyi.…”

Section: Resultssupporting

confidence: 75%

Bacterial Quorum-Sensing Signal Arrests Phytoplankton Cell Division and Impacts Virus-Induced Mortality

Pollara

Becker

Nunn

et al. 2021

mSphere

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Interactions between phytoplankton and heterotrophic bacteria fundamentally shape marine ecosystems by controlling primary production, structuring marine food webs, mediating carbon export, and influencing global climate. Phytoplankton-bacterium interactions are facilitated by secreted compounds; however, linking these chemical signals, their mechanisms of action, and their resultant ecological consequences remains a fundamental challenge. The bacterial quorum-sensing signal 2-heptyl-4-quinolone (HHQ) induces immediate, yet reversible, cellular stasis (no cell division or mortality) in the coccolithophore Emiliania huxleyi; however, the mechanism responsible remains unknown. Using transcriptomic and proteomic approaches in combination with diagnostic biochemical and fluorescent cell-based assays, we show that HHQ exposure leads to prolonged S-phase arrest in phytoplankton coincident with the accumulation of DNA damage and a lack of repair despite the induction of the DNA damage response (DDR). While this effect is reversible, HHQ-exposed phytoplankton were also protected from viral mortality, ascribing a new role of quorum-sensing signals in regulating multitrophic interactions. Furthermore, our data demonstrate that in situ measurements of HHQ coincide with areas of enhanced micro- and nanoplankton biomass. Our results suggest bacterial communication signals as emerging players that may be one of the contributing factors that help structure complex microbial communities throughout the ocean. IMPORTANCE Bacteria and phytoplankton form close associations in the ocean that are driven by the exchange of chemical compounds. The bacterial signal 2-heptyl-4-quinolone (HHQ) slows phytoplankton growth; 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 relieved of viral mortality, elevating the ecological consequences of this complex interaction. Further results indicate that HHQ may target phytoplankton proteins involved in nucleotide biosynthesis and DNA repair, both of which are crucial targets for viral success. Our results support microbial cues as emerging players in marine ecosystems, providing a new mechanistic framework for how bacterial communication signals mediate interspecies and interkingdom behaviors.

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Section: Resultssupporting

confidence: 75%

Bacterial Quorum-Sensing Signal Arrests Phytoplankton Cell Division and Impacts Virus-Induced Mortality

Pollara

Becker

Nunn

et al. 2021

mSphere

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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: 84%

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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“…Cell death is a third loss factor, but its quantification in marine systems, and aquatic systems in general, remains rare compared to the quantification of sinking and grazing losses. Phytoplankton cell death can be caused by pathogens (Bramucci and Case 2019;Schieler et al 2019) or physiological stress, and a handful of studies indicate that a considerable proportion of phytoplankton cells may not be viable (e.g. Brussaard et al 1995;Veldhuis et al 2001;Agustí 2004;Berman-Frank et al 2004;Rychtecký et al 2014).…”

Section: Introductionmentioning

confidence: 99%

Viability of pico- and nanophytoplankton in the Baltic Sea during spring

et al. 2019

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Phytoplankton cell death is an important process in marine food webs, but the viability of natural phytoplankton communities remains unexplored in many ecosystems. In this study, we measured the viability of natural pico-and nanophytoplankton communities in the central and southern parts of the Baltic Sea (55°21 0 N, 17°06 0 E-60°18 0 N, 19°14 0 E) during spring (4th-15th April 2016) to assess differences among phytoplankton groups and the potential relationship between cell death and temperature, and inorganic nutrient availability. Cell viability was determined by SYTOX Green cell staining and flow cytometry at a total of 27 stations representing differing hydrographic regimes. Three general groups of phytoplankton (picocyanobacteria, picoeukaryotes, and nanophytoplankton) were identified by cytometry using pigment fluorescence and light scatter characteristics. The picocyanobacteria and picoeukaryotes had significantly higher cell viability than the nanophytoplankton population at all depths throughout the study area. Viability correlated positively with the photosynthetic efficiency (F v /F m , maximum quantum yield of photosystem II) as measured on the total phytoplankton community. However, an anticipated correlation with dissolved organic carbon was not observed. We found that the abiotic factors suggested to affect phytoplankton viability in other marine ecosystems were not as important in the Baltic Sea, and other biotic processes, e.g. processes related to species succession could have a more pronounced role.

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Phaeobacter inhibens induces apoptosis-like programmed cell death in calcifying Emiliania huxleyi

Cited by 29 publications

References 83 publications

Bacterial Quorum-Sensing Signal Arrests Phytoplankton Cell Division and Impacts Virus-Induced Mortality

Bacterial Quorum-Sensing Signal Arrests Phytoplankton Cell Division and Impacts Virus-Induced Mortality

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

Viability of pico- and nanophytoplankton in the Baltic Sea during spring

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