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

Scott B. Pollara, Jamie W. Becker, Brook L. Nunn, Rene Boiteau, Daniel Repeta, Miranda C. Mudge, Grayton Downing, Davis Chase, Elizabeth L. Harvey, Kristen E. Whalen

Research output: Contribution to journalArticlepeer-review

15 Scopus citations

Abstract

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 quorumsensing 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.

Original languageEnglish (US)
Article numbere00009-21
Pages (from-to)1-17
Number of pages17
JournalmSphere
Volume6
Issue number3
DOIs
StatePublished - May 2021
Externally publishedYes

Bibliographical note

Funding Information:
We acknowledge the support from the Electron Microscopy Resource Laboratory at the University of Pennsylvania for TEM sample processing. We thank Kay Bidle for thoughtful feedback on a previous draft of the manuscript and the viral cultures, Vinayak Agarwal for homology modeling support and discussions, Bradley Moore for tetrabromopyrrole, and Katie Barott for flow cytometry support. We thank members of the Whalen laboratory, including Ellysia Overton, Yongjie Gao, Carlotta Pazzi, Megan Coolahan, Shreya Kishore, and Lucy Zhao, for assistance in phytoplankton sampling for RNA and protein isolation and constructive discussions. We thank the Georgia Genomics and Bioinformatics Core Facility for RNA sequencing. Funding for this work was supported by an NSF grant (OCE-1657808) awarded to K.E.W. and E.L.H. K.E.W. was also supported by a faculty research grant from Haverford College as well as funding from the Koshland Integrated Natural Science Center and Green Fund at Haverford College. E.L.H. was also supported by a Sloan Foundation research fellowship. B.L.N. was supported by an NSF grant (OCE-1633939). M.C.M. was supported by an NIH training grant (T32 HG000035). Mass spectrometry was partially supported by the University of Washington Proteomics Resource (UWPR95794). D.R. was supported by funding through the Gordon and Betty Moore Foundation (grant 6000), a Simons Collaboration for Ocean Processes and Ecology grant (329108), and an NSF grant (OCE-1736280). R.B. was supported by an NSF graduate research fellowship and an NSF grant (OCE-1829761). We declare no competing interests.

Funding Information:
We acknowledge the support from the Electron Microscopy Resource Laboratory at the University of Pennsylvania for TEM sample processing. We thank Kay Bidle for thoughtful feedback on a previous draft of the manuscript and the viral cultures, Vinayak Agarwal for homology modeling support and discussions, Bradley Moore for tetrabromopyrrole, and Katie Barott for flow cytometry support. We thank members of the Whalen laboratory, including Ellysia Overton, Yongjie Gao, Carlotta Pazzi, Megan Coolahan, Shreya Kishore, and Lucy Zhao, for assistance in phytoplankton sampling for RNA and protein isolation and constructive discussions. We thank the Georgia Genomics and Bioinformatics Core Facility for RNA sequencing.

Funding Information:
Funding for this work was supported by an NSF grant (OCE-1657808) awarded to K.E.W. and E.L.H. K.E.W. was also supported by a faculty research grant from Haverford College as well as funding from the Koshland Integrated Natural Science Center and

Publisher Copyright:
Copyright © 2021 Pollara et al. This is an openaccess article distributed under the terms of the Creative Commons Attribution 4.0 International license.

Keywords

  • cell cycle
  • HHQ
  • phytoplankton
  • Pseudoalteromonas
  • quorum sensing
  • virus-host interactions

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