Abstract
The redox-sensitive proteome (RSP) consists of protein thiols that undergo redox reactions, playing an important role in coordinating cellular processes. Here, we applied a large-scale phylogenomic reconstruction approach in the model diatom Phaeodactylum tricornutum to map the evolutionary origins of the eukaryotic RSP. The majority of P. tricornutum redox-sensitive cysteines (76%) is specific to eukaryotes, yet these are encoded in genes that are mostly of a prokaryotic origin (57%). Furthermore, we find a threefold enrichment in redox-sensitive cysteines in genes that were gained by endosymbiotic gene transfer during the primary plastid acquisition. The secondary endosymbiosis event coincides with frequent introduction of reactive cysteines into existing proteins. While the plastid acquisition imposed an increase in the production of reactive oxygen species, our results suggest that it was accompanied by significant expansion of the RSP, providing redox regulatory networks the ability to cope with fluctuating environmental conditions.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Embley, T. M. & Martin, W. Eukaryotic evolution, changes and challenges. Nature 440, 623–630 (2006).
Timmis, J. N., Ayliffe, M. A., Huang, C. Y. & Martin, W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5, 123–135 (2004).
Archibald, J. M. The puzzle of plastid evolution. Curr. Biol. 19, R81–R88 (2009).
Baurain, D. et al. Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol. Biol. Evol. 27, 1698–1709 (2010).
Gould, S. B., Maier, U.-G. & Martin, W. F. Protein import and the origin of red complex plastids. Curr. Biol. 25, R515–R521 (2015).
Esser, C. et al. A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol. Biol. Evol. 21, 1643–1660 (2004).
Deusch, O. et al. Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol. Biol. Evol. 25, 748–761 (2008).
Alvarez-Ponce, D. & McInerney, J. O. The human genome retains relics of its prokaryotic ancestry: human genes of archaebacterial and eubacterial origin exhibit remarkable differences. Genome Biol. Evol. 3, 782–790 (2011).
Lane, N. & Martin, W. The energetics of genome complexity. Nature 467, 929–934 (2010).
Mittler, R., Vanderauwera, S., Gollery, M. & Van Breusegem, F. Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490–498 (2004).
Halliwell, B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol. 141, 312–322 (2006).
Rosenwasser, S. et al. Rosmeter: a bioinformatic tool for the identification of transcriptomic imprints related to reactive oxygen species type and origin provides new insights into stress responses. Plant Physiol. 163, 1071–1083 (2013).
Gadjev, I. et al. Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141, 436–445 (2006).
Willems, P. et al. The ROS wheel: refining ROS transcriptional footprints. Plant Physiol. 171, 1720–1733 (2016).
Laloi, C., Apel, K. & Danon, A. Reactive oxygen signalling: the latest news. Curr. Opin. Plant Biol. 7, 323–328 (2004).
Winterbourn, C. C. & Hampton, M. B. Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 45, 549–561 (2008).
Nelson, D. M., Tréguer, P., Brzezinski, M. A., Leynaert, A. & Quéguiner, B. Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochem. Cycles 9, 359–372 (1995).
Adl, S. M. et al. The revised classification of eukaryotes. J. Eukaryotic Microbiol. 59, 429–493 (2012).
Allen, A. E. et al. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473, 203–207 (2011).
Bowler, C. et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239–244 (2008).
Rosenwasser, S. et al. Mapping the diatom redox-sensitive proteome provides insight into response to nitrogen stress in the marine environment. Proc. Natl Acad. Sci. USA 111, 2740–2745 (2014).
Yang, Z., Kumar, S. & Nei, M. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141, 1641–1650 (1995).
Yang, Z. Paml 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).
Balmant, K. M. et al. Redox proteomics of tomato in response to Pseudomonas syringae infection. Hortic. Res. 2, 15043 (2015).
Queval, G. & Foyer, C. H. Redox regulation of photosynthetic gene expression. Philos. Trans. R Soc. Lond. B Biol. Sci. 367, 3475–3485 (2012).
Ashburner, M. et al. Gene ontology: tool for the unification of biology. Nat. Genet. 25, 25–29 (2000).
Guo, J. et al. Proteome-wide light/dark modulation of thiol oxidation in cyanobacteria revealed by quantitative site-specific redox proteomics. Mol. Cell Proteomics 13, 3270–3285 (2014).
Ku, C. et al. Endosymbiotic origin and differential loss of eukaryotic genes. Nature 524, 427–432 (2015).
Koutsovoulos, G. et al. No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini. Proc. Natl Acad. Sci. USA 113, 5053–5058 (2016).
Schönknecht, G. et al. Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339, 1207–1210 (2013).
Boothby, T. C. et al. Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. Proc. Natl Acad. Sci. USA 112, 15976–15981 (2015).
Méheust, R., Zelzion, E., Bhattacharya, D., Lopez, P. & Bapteste, E. Protein networks identify novel symbiogenetic genes resulting from plastid endosymbiosis. Proc. Natl Acad. Sci. USA 113, 3579–3584 (2016).
Balsera, M., Uberegui, E., Schürmann, P. & Buchanan, B. B. Evolutionary development of redox regulation in chloroplasts. Antioxid. Redox. Signal. 21, 1327–1355 (2014).
Scheibe, R. & Dietz, K.-J. Reduction–oxidation network for flexible adjustment of cellular metabolism in photoautotrophic cells. Plant Cell Environ. 35, 202–216 (2012).
Imlay, J. A. What biological purpose is served by superoxide reductase? J. Biol. Inorg. Chem. 7, 659–663 (2002).
Slesak, I., Slesak, H. & Kruk, J. Oxygen and hydrogen peroxide in the early evolution of life on earth: in silico comparative analysis of biochemical pathways. Astrobiology 12, 775–784 (2012).
Susanti, D. et al. Thioredoxin targets fundamental processes in a methane producing archaeon. Methanocaldococcus jannaschii. Proc. Natl Acad. Sci. USA 111, 2608–2613 (2014).
Shimizu, T. et al. Sulfide-responsive transcriptional repressor SqrR functions as a master regulator of sulfide-dependent photosynthesis. Proc. Natl Acad. Sci. USA 114, 2355–2360 (2017).
Poole, L. B. The basics of thiols and cysteines in redox biology and chemistry. Free Radic. Biol. Med. 80, 148–157 (2015).
Bauer, S., Grossmann, S., Vingron, M. & Robinson, P. N. Ontologizer 2.0—a multifunctional tool for GO term enrichment analysis and data exploration. Bioinformatics 24, 1650–1651 (2008).
Federhen, S. The NCBI taxonomy database. Nucleic Acids Res. 40 (D1), D136–D143 (2012).
Okamoto, N., Chantangsi, C., Horák, A., Leander, B. S. & Keeling, P. J. Molecular phylogeny and description of the novel katablepharid Roombia truncata gen. et sp. nov., and establishment of the Hacrobia taxon nov. PLoS ONE 4, e7080 (2009).
O'Leary, N. A. et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44 (D1), D733–D745 (2015).
Benson, D. A. et al. Genbank. Nucleic Acids Res. 43 (D1), D30–D35 (2015).
Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152 (2012).
Kent, W. J. BLAT—the BLAST-like alignment tool. Genome Res. 12, 656–664 (2002).
Camacho, C. et al. Blast+: architecture and applications. BMC Bioinformatics 10, 421 (2009).
Tatusov, R. L., Koonin, E. V. & Lipman, D. J. A genomic perspective on protein families. Science 278, 631–637 (1997).
Rice, P., Longden, I. & Bleasby, A. Emboss: the European molecular biology open software suite. Trends Genet. 16, 276–277 (2000).
Katoh, K. & Standley, D. M. Mafft multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).
Guindon, S., Delsuc, F., Dufayard, J.-F. & Gascuel, O. Estimating maximum likelihood phylogenies with PhyML. Methods Mol. Biol. 537, 113–137 (2009).
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. Prottest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164–1165 (2011).
Farris, J. S. Estimating phylogenetic trees from distance matrices. Am. Nat. (1972).
Acknowledgements
The authors thank A. Kupzok, J. Ilhan, J. Weissenbach, C. Walda, A. Mrnjavac and T. Wein for critical comments on the manuscript. This project was supported by the European Research Council (Grant No. 281357 awarded to T.D. and 280991 awarded to A.V.), the Israeli Science Foundation (Grant 25 No. 712233 awarded to A.V.) and the cluster of excellence, The Future Ocean (funded within the framework of the Excellence Initiative by the Deutsche Forschungsgemeinschaft (DFG) on behalf of the German federal and state governments).
Author information
Authors and Affiliations
Contributions
C.W., G.L., S.R., A.V. and T.D. conceived the study. T.D., G.L. and C.W. designed the research strategy. C.W., G.L. and S.R. performed the analyses. All authors were involved in the interpretation of results and writing of the article.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
Supplementary Figures 1–3, Supplementary Tables 3 and 5. (PDF 2417 kb)
Supplementary Tables
Supplementary Tables 1, 2 and 4. (XLSX 67 kb)
Rights and permissions
About this article
Cite this article
Woehle, C., Dagan, T., Landan, G. et al. Expansion of the redox-sensitive proteome coincides with the plastid endosymbiosis. Nature Plants 3, 17066 (2017). https://doi.org/10.1038/nplants.2017.66
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/nplants.2017.66