Photosynthetic sea slugs induce protective changes to the light reactions of the chloroplasts they steal from algae

  1. Vesa Havurinne
  2. Esa Tyystjärvi  Is a corresponding author
  1. University of Turku, Finland

Abstract

Sacoglossan sea slugs are able to maintain functional chloroplasts inside their own cells, and mechanisms that allow preservation of the chloroplasts are unknown. We found that the slug Elysia timida induces changes to the photosynthetic light reactions of the chloroplasts it steals from the alga Acetabularia acetabulum. Working with a large continuous laboratory culture of both the slugs (>500 individuals) and their prey algae, we show that the plastoquinone pool of slug chloroplasts remains oxidized, which can suppress reactive oxygen species formation. Slug chloroplasts also rapidly build up a strong proton motive force upon a dark-to-light transition, which helps them to rapidly switch on photoprotective non-photochemical quenching of excitation energy. Finally, our results suggest that chloroplasts inside E. timida rely on oxygen-dependent electron sinks during rapid changes in light intensity. These photoprotective mechanisms are expected to contribute to the long-term functionality of the chloroplasts inside the slugs.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 2, 3, 4, Figure 4-figure supplement 1 and Figures 5, 6, 7B-E and 8.

Article and author information

Author details

  1. Vesa Havurinne

    Biochemistry, University of Turku, Turku, Finland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5213-0905
  2. Esa Tyystjärvi

    Biochemistry, University of Turku, Turku, Finland
    For correspondence
    esatyy@utu.fi
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6808-7470

Funding

Academy of Finland (307335)

  • Esa Tyystjärvi

Suomen Kulttuurirahasto (Graduate student grant)

  • Vesa Havurinne

Suomalainen Tiedeakatemia (Graduate student grant)

  • Vesa Havurinne

University of Turku graduate school, DPMLS (Graduate student grant)

  • Vesa Havurinne

Academy of Finland (333421)

  • Esa Tyystjärvi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in accordance with EU legislation and directives concerning scientific research on non-cephalopod invertebrates.

Copyright

© 2020, Havurinne & Tyystjärvi

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Vesa Havurinne
  2. Esa Tyystjärvi
(2020)
Photosynthetic sea slugs induce protective changes to the light reactions of the chloroplasts they steal from algae
eLife 9:e57389.
https://doi.org/10.7554/eLife.57389

Share this article

https://doi.org/10.7554/eLife.57389

Further reading

  1. Sea slugs steal from algae to harvest energy from sunlight

    1. Cell Biology
    2. Medicine
    Pengbo Chen, Bo Li ... Xinfeng Zheng
    Research Article

    Background:

    It has been reported that loss of PCBP2 led to increased reactive oxygen species (ROS) production and accelerated cell aging. Knockdown of PCBP2 in HCT116 cells leads to significant downregulation of fibroblast growth factor 2 (FGF2). Here, we tried to elucidate the intrinsic factors and potential mechanisms of bone marrow mesenchymal stromal cells (BMSCs) aging from the interactions among PCBP2, ROS, and FGF2.

    Methods:

    Unlabeled quantitative proteomics were performed to show differentially expressed proteins in the replicative senescent human bone marrow mesenchymal stromal cells (RS-hBMSCs). ROS and FGF2 were detected in the loss-and-gain cell function experiments of PCBP2. The functional recovery experiments were performed to verify whether PCBP2 regulates cell function through ROS/FGF2-dependent ways.

    Results:

    PCBP2 expression was significantly lower in P10-hBMSCs. Knocking down the expression of PCBP2 inhibited the proliferation while accentuated the apoptosis and cell arrest of RS-hBMSCs. PCBP2 silence could increase the production of ROS. On the contrary, overexpression of PCBP2 increased the viability of both P3-hBMSCs and P10-hBMSCs significantly. Meanwhile, overexpression of PCBP2 led to significantly reduced expression of FGF2. Overexpression of FGF2 significantly offset the effect of PCBP2 overexpression in P10-hBMSCs, leading to decreased cell proliferation, increased apoptosis, and reduced G0/G1 phase ratio of the cells.

    Conclusions:

    This study initially elucidates that PCBP2 as an intrinsic aging factor regulates the replicative senescence of hBMSCs through the ROS-FGF2 signaling axis.

    Funding:

    This study was supported by the National Natural Science Foundation of China (82172474).