Abstract

Photosynthetic organisms have adapted to survive a myriad of extreme environments from the earth’s deserts to its poles, yet the proteins that carry out the light reactions of photosynthesis are highly conserved from the cyanobacteria to modern day crops. To investigate adaptations of the photosynthetic machinery in cyanobacteria to excessive light stress, we isolated a new strain of cyanobacteria, Cyanobacterium aponinum 0216, from the extreme light environment of the Sonoran Desert. Here we report the biochemical characterization and the 2.7 Å resolution structure of trimeric photosystem I from this high-light tolerant cyanobacterium. The structure shows a new conformation of the PsaL C-terminus that supports trimer formation of cyanobacterial photosystem Ipectroscopic analysis of this photosystem I revealed a decrease in far-red absorption, which is attributed to a decrease in the number of long wavelength chlorophylls. Using these findings, we constructed two chimeric PSIs in Synechocystis sp. PCC 6803 demonstrating how unique structural features in photosynthetic complexes can change spectroscopic properties, allowing organisms to thrive under different environmental stresses.

Data availability

The final model (PDBID 6VPV) and map (EMD-21320) were deposited in the Protein Databank and Electron Microscopy Database, respectively.C. aponinum genomic DNA was deposited in NCBI genebank under NCBI:txid2676140.

The following data sets were generated

Article and author information

Author details

  1. Zachary Dobson

    School of Molecular Sciences., Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Safa Ahad

    Department of Chemistry, Purdue University, West Lafayette, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jackson Vanlandingham

    School of Molecular Sciences., Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Hila Toporik

    School of Molecular Sciences., Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Natalie Vaughn

    School of Molecular Sciences., Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Michael Vaughn

    School of Molecular Sciences., Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9357-094X
  7. Dewight Williams

    John M. Cowley Center for High Resolution Electron Microscopy, Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Michael Reppert

    Department of Chemistry, Purdue University, West Lafayette, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Petra Fromme

    John M. Cowley Center for High Resolution Electron Microscopy, Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Yuval Mazor

    School of Molecular Sciences., Arizona State University, Tempe, United States
    For correspondence
    yuval.mazor@asu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5072-0928

Funding

National Institute of Food and Agriculture (2020-67034-31742)

  • Zachary Dobson

Biodesign, Center of Applied Structural Discovery. (1)

  • Zachary Dobson

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

Reviewing Editor

  1. David M Kramer, Michigan State University, United States

Version history

  1. Received: February 13, 2021
  2. Accepted: August 25, 2021
  3. Accepted Manuscript published: August 26, 2021 (version 1)
  4. Version of Record published: September 9, 2021 (version 2)

Copyright

© 2021, Dobson et al.

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.

Metrics

  • 2,043
    Page views
  • 348
    Downloads
  • 13
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Zachary Dobson
  2. Safa Ahad
  3. Jackson Vanlandingham
  4. Hila Toporik
  5. Natalie Vaughn
  6. Michael Vaughn
  7. Dewight Williams
  8. Michael Reppert
  9. Petra Fromme
  10. Yuval Mazor
(2021)
The structure of photosystem I from a high-light tolerant Cyanobacteria
eLife 10:e67518.
https://doi.org/10.7554/eLife.67518

Share this article

https://doi.org/10.7554/eLife.67518

Further reading

    1. Plant Biology
    Daniel S Yu, Megan A Outram ... Simon J Williams
    Research Article

    Plant pathogens secrete proteins, known as effectors, that function in the apoplast or inside plant cells to promote virulence. Effector recognition by cell-surface or cytosolic receptors results in the activation of defence pathways and plant immunity. Despite their importance, our general understanding of fungal effector function and recognition by immunity receptors remains poor. One complication often associated with effectors is their high sequence diversity and lack of identifiable sequence motifs precluding prediction of structure or function. In recent years, several studies have demonstrated that fungal effectors can be grouped into structural classes, despite significant sequence variation and existence across taxonomic groups. Using protein X-ray crystallography, we identify a new structural class of effectors hidden within the secreted in xylem (SIX) effectors from Fusarium oxysporum f. sp. lycopersici (Fol). The recognised effectors Avr1 (SIX4) and Avr3 (SIX1) represent the founding members of the Fol dual-domain (FOLD) effector class, with members containing two distinct domains. Using AlphaFold2, we predicted the full SIX effector repertoire of Fol and show that SIX6 and SIX13 are also FOLD effectors, which we validated experimentally for SIX6. Based on structural prediction and comparisons, we show that FOLD effectors are present within three divisions of fungi and are expanded in pathogens and symbionts. Further structural comparisons demonstrate that Fol secretes effectors that adopt a limited number of structural folds during infection of tomato. This analysis also revealed a structural relationship between transcriptionally co-regulated effector pairs. We make use of the Avr1 structure to understand its recognition by the I receptor, which leads to disease resistance in tomato. This study represents an important advance in our understanding of Fol-tomato, and by extension plant–fungal interactions, which will assist in the development of novel control and engineering strategies to combat plant pathogens.

    1. Ecology
    2. Plant Biology
    Jamie Mitchel Waterman, Tristan Michael Cofer ... Matthias Erb
    Research Article

    Volatiles emitted by herbivore-attacked plants (senders) can enhance defenses in neighboring plants (receivers), however, the temporal dynamics of this phenomenon remain poorly studied. Using a custom-built, high-throughput proton transfer reaction time-of-flight mass spectrometry (PTR-ToF-MS) system, we explored temporal patterns of volatile transfer and responses between herbivore-attacked and undamaged maize plants. We found that continuous exposure to natural blends of herbivore-induced volatiles results in clocked temporal response patterns in neighboring plants, characterized by an induced terpene burst at the onset of the second day of exposure. This delayed burst is not explained by terpene accumulation during the night, but coincides with delayed jasmonate accumulation in receiver plants. The delayed burst occurs independent of day:night light transitions and cannot be fully explained by sender volatile dynamics. Instead, it is the result of a stress memory from volatile exposure during the first day and secondary exposure to bioactive volatiles on the second day. Our study reveals that prolonged exposure to natural blends of stress-induced volatiles results in a response that integrates priming and direct induction into a distinct and predictable temporal response pattern. This provides an answer to the long-standing question of whether stress volatiles predominantly induce or prime plant defenses in neighboring plants, by revealing that they can do both in sequence.