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Multi-omics reveals mechanisms of total resistance to extreme illumination of a desert alga

Abstract

The unparalleled performance of Chlorella ohadii under irradiances of twice full sunlight underlines the gaps in our understanding of how the photosynthetic machinery operates, and what sets its upper functional limit. Rather than succumbing to photodamage under extreme irradiance, unique features of photosystem II function allow C. ohadii to maintain high rates of photosynthesis and growth, accompanied by major changes in composition and cellular structure. This remarkable resilience allowed us to investigate the systems response of photosynthesis and growth to extreme illumination in a metabolically active cell. Using redox proteomics, transcriptomics, metabolomics and lipidomics, we explored the cellular mechanisms that promote dissipation of excess redox energy, protein S-glutathionylation, inorganic carbon concentration, lipid and starch accumulation, and thylakoid stacking. C. ohadii possesses a readily available capacity to utilize a sudden excess of reducing power and carbon for growth and reserve formation, and post-translational redox regulation plays a pivotal role in this rapid response. Frequently the response in C. ohadii deviated from that of model species, reflecting its life history in desert sand crusts. Comparative global and case-specific analyses provided insights into the potential evolutionary role of effective reductant utilization in this extreme resistance of C. ohadii to extreme irradiation.

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Fig. 1: Growth and cellular protein levels of C. ohadii cells transferred to EIL.
Fig. 2: Changes of photosynthesis and respiration in EIL-exposed C. ohadii cells.
Fig. 3: C. ohadii metabolome response to EIL.
Fig. 4: Integration of polar metabolites, lipids and transcript responses with common light regimes.
Fig. 5: Multi-omics illustration of C. ohadii temporal responses of photosynthesis and central C metabolism to EIL treatments.

Data availability

Chorella ohadii genome annotation has been deposited in the NCBI/Genbank database with accession no. PRJNA573576. Mass spectrometry proteomics data have been deposited in the ProteomeXchange Consortium via the PRIDE partner repository, with the dataset identifier PXD015681. Metabolite and lipid profiling data are provided in the Supplementary Information as indicated in the main text.

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Acknowledgements

We thank B. Gontero from BIP-Marseille for constructive discussions regarding the CP12 protein. We thank the Technion Genome Centre (Haifa, Israel) for their support during transcriptome sequencing and analysis. We thank the Human Frontiers Scholarship programme for financial support given to H.T.

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Contributions

H.T. and M.S. designed the research. H.T., B.S., U.L. and A.E. performed research. H.T., O.M., A.E., U.A., Y.B., J.K., S.A.R. and J.S. analysed data. H.T. and M.S. wrote the article.

Corresponding author

Correspondence to Haim Treves.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks G. Charles Dismukes, Arthur Grossman the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 NADPH fluorescence in C. ohadii cultures under LL and EIL.

NADPH fluorescence measured at shifts from dark to 100, 1000 and 3000 µmol photons m−2 s−1, in LL (black) and t15EIL (red) treated C. ohadii cells. Similar results were obtained from 6 biologically independent replicates.

Extended Data Fig. 2 Principle Component analyses of nuclear-encoded transcripts, metabolites and lipids following shift to EIL.

Principle Component analyses of log2-normalized nuclear-encoded transcripts (a), metabolites (b) and lipids (c) following shift to EIL, and the corresponding loading analysis of individual traits (df). tXEIL indicate the minutes relative to time point zero under EIL, Cont. - continuous EIL, and LL, low light. For a given treatment, each biological replicate is shown separately (n = 3). The dashed line in d separates upper positive quartile of PC1.

Extended Data Fig. 3 C. ohadii genomic cysteine content analysis.

a, Enriched GO terms (Fisher’s exact test, P value < 0.05, corrected for multiple hypotheses testing by the Benjamini-Hochberg correction procedure) identified in the redox-responsive proteome (n = 4 biologically independent experiments) of t3EIL (red), using a reference (black) of the entire thiol enriched proteome. Values are presented as % of proteins associated with a given GO term from the entire list of proteins in the t3EIL redox-responsive proteome (test) and the entire thiol-enriched proteome (reference). b, Cysteine counts in 4341 shared by the 5 algae presented. c, Average cysteine counts per gene of different KOG categories in C. ohadii (red) and C. reinhardtii (black).

Extended Data Fig. 4 Functional analysis of changes in the transcriptome.

ac, Gene ontology (GO) bias word clouds (biological process). Word clouds of genes upregulated (n = 3 biologically independent experiments) in t15EIL (a), t120EIL (b) and continuous EIL (c). Font size correlates with significance (see Supplementary Table 4); red terms are depleted and green terms enriched (Fisher’s exact test, P value < 0.05, corrected for multiple hypotheses testing by the Benjamini-Hochberg correction procedure).

Extended Data Fig. 5 Changes of primary metabolites levels in C. ohadii cultures under LL and EIL.

Changes of primary metabolites levels - Heatmap representation of metabolite levels of C. ohadii cells at LL, t120EIL and continuous EIL. Hierarchical clustering was performed on log-transformed, mean-centered and unit variance-scaled data using Pearson’s correlation optimized for sample and metabolite leaf order (see methods). Only significantly changing metabolites were considered (n = 3 biologically independent experiments, one-way ANOVA <0.05). The row Z-score value of each metabolite is plotted in redblue color scale. GAP statistics indicated 5 metabolite clusters (Supplementary Fig. 2), which are indicated by transparent blue triangles.

Extended Data Fig. 6 Detailed relative metabolites levels in C. ohadii cultures under LL and EIL.

Detailed Log2 normalized values of detected metabolites at LL (blue), t120EIL (orange) and continuous EIL (red). Data are mean ± SD (n = 3 biologically independent experiments, paired two-tailed t-test; one asterisk, P < 0.05; two asterisks, P < 0.01; three asterisks, P < 0.001).

Extended Data Fig. 7 Photorespiratory gene expression in C. ohadii cultures under LL and EIL.

Log2 normalized fold change of expression of photorespiratory genes between t15EIL (yellow), t120EIL (orange) and continuous EIL (red) to LL (n = 3 biologically independent experiments, Cuffdiff, T-statistics, Benjamini-Hochberg corrected P values are presented; one asterisk, P < 0.05; two asterisks, P < 0.01). Expression and corrected P values are further detailed in Supplementary Table 7.

Extended Data Fig. 8 C. ohadii morphology after mid-term exposure to EIL and during growth in continuous EIL.

C. ohadii morphology after mid-term exposure to EIL and during growth in continuous EIL. a, Electron micrographs showing C. ohadii cells grown in TAP (Tris, acetate, phosphate) medium at 35 °C under LL (center), t120EIL (left panel) and continuous EIL (right panel). Bar indicates 500 nm. b, Higher magnifications of C. ohadii continuous EIL treated cells. Arrows indicate altered morphology of pyrenoid starch sheath where in several other cells sheath is absent. Large amounts of starch are also deposited at other sites in the plastid. Similar results were obtained from 3 biologically independent replicates. Bars indicate 2000 and 1000 nm in the upper and lower panels, respectively.

Extended Data Fig. 9 Multi-omics illustration of C. ohadii response to EIL.

Multi-omics illustration of C. ohadii temporal responses to EIL treatments associated with thylakoid morphology. Genes, proteins, metabolites and lipids presented showed significantly higher (red) or lower (blue) levels of expression, redox-response, and accumulation, respectively. Arrows illustrate potential positive (red) and negative (blue), direct (solid line), and indirect (dashed line) effects, according to the model suggested in the discussion.

Extended Data Fig. 10 Desert BSC diurnal cycle.

Schematic view of desert BSC diurnal cycle. Main water supply is by dew formation during the night, followed by morning dehydration. Through most of the day, crusts are dry and exposed to ~2000 µmol photons m−2 s−1.

Supplementary information

Supplementary Information

Supplementary text, Figs. 1–11 and Tables 1, 3 and 5–9.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–10. Legends are provided for each table within each tab in the collated file.

Supplementary Data 1

Comparative cysteine count in C. ohadii proteins with homologues in other algae. Gene names and descriptions are detailed in accession no. PRJNA573576 (NCBI).

Supplementary Data 2

NADP-MDH sequence alignment.

Supplementary Data 3

Cytosolic aldolase sequence alignment.

Supplementary Data 4

NADP-GAPDH sequence alignment.

Supplementary Data 5

NADP-ME sequence alignment.

Supplementary Data 6

LPAT sequence alignment.

Supplementary Data 7

DGAT2 sequence alignment.

Supplementary Data 8

CP47 sequence alignment.

Supplementary Data 9

Cytochrome f sequence alignment.

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Treves, H., Siemiatkowska, B., Luzarowska, U. et al. Multi-omics reveals mechanisms of total resistance to extreme illumination of a desert alga. Nat. Plants 6, 1031–1043 (2020). https://doi.org/10.1038/s41477-020-0729-9

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