Expansion of the redox-sensitive proteome coincides with the plastid endosymbiosis

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.

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Figure 1: Examples of ancestral sequence reconstruction.
Figure 2: Cys gains along the ancestral lineages leading to P. tricornutum.
Figure 3: Prokaryotic gene ancestry of RSCys gains via gene origin in the six ancestral lineages.

References

  1. 1

    Embley, T. M. & Martin, W. Eukaryotic evolution, changes and challenges. Nature 440, 623–630 (2006).

    CAS  PubMed  Google Scholar 

  2. 2

    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).

    CAS  PubMed  Google Scholar 

  3. 3

    Archibald, J. M. The puzzle of plastid evolution. Curr. Biol. 19, R81–R88 (2009).

    CAS  PubMed  Google Scholar 

  4. 4

    Baurain, D. et al. Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol. Biol. Evol. 27, 1698–1709 (2010).

    CAS  PubMed  Google Scholar 

  5. 5

    Gould, S. B., Maier, U.-G. & Martin, W. F. Protein import and the origin of red complex plastids. Curr. Biol. 25, R515–R521 (2015).

    CAS  PubMed  Google Scholar 

  6. 6

    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).

    CAS  PubMed  Google Scholar 

  7. 7

    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).

    CAS  PubMed  Google Scholar 

  8. 8

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9

    Lane, N. & Martin, W. The energetics of genome complexity. Nature 467, 929–934 (2010).

    CAS  PubMed  Google Scholar 

  10. 10

    Mittler, R., Vanderauwera, S., Gollery, M. & Van Breusegem, F. Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490–498 (2004).

    CAS  PubMed  Google Scholar 

  11. 11

    Halliwell, B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol. 141, 312–322 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13

    Gadjev, I. et al. Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141, 436–445 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14

    Willems, P. et al. The ROS wheel: refining ROS transcriptional footprints. Plant Physiol. 171, 1720–1733 (2016).

    PubMed  PubMed Central  Google Scholar 

  15. 15

    Laloi, C., Apel, K. & Danon, A. Reactive oxygen signalling: the latest news. Curr. Opin. Plant Biol. 7, 323–328 (2004).

    CAS  PubMed  Google Scholar 

  16. 16

    Winterbourn, C. C. & Hampton, M. B. Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 45, 549–561 (2008).

    CAS  PubMed  Google Scholar 

  17. 17

    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).

    CAS  Google Scholar 

  18. 18

    Adl, S. M. et al. The revised classification of eukaryotes. J. Eukaryotic Microbiol. 59, 429–493 (2012).

    Google Scholar 

  19. 19

    Allen, A. E. et al. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473, 203–207 (2011).

    CAS  PubMed  Google Scholar 

  20. 20

    Bowler, C. et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239–244 (2008).

    CAS  PubMed  Google Scholar 

  21. 21

    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).

    CAS  PubMed  Google Scholar 

  22. 22

    Yang, Z., Kumar, S. & Nei, M. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141, 1641–1650 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23

    Yang, Z. Paml 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).

    CAS  PubMed  Google Scholar 

  24. 24

    Balmant, K. M. et al. Redox proteomics of tomato in response to Pseudomonas syringae infection. Hortic. Res. 2, 15043 (2015).

    PubMed  PubMed Central  Google Scholar 

  25. 25

    Queval, G. & Foyer, C. H. Redox regulation of photosynthetic gene expression. Philos. Trans. R Soc. Lond. B Biol. Sci. 367, 3475–3485 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26

    Ashburner, M. et al. Gene ontology: tool for the unification of biology. Nat. Genet. 25, 25–29 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 28

    Ku, C. et al. Endosymbiotic origin and differential loss of eukaryotic genes. Nature 524, 427–432 (2015).

    CAS  PubMed  Google Scholar 

  29. 29

    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).

    CAS  PubMed  Google Scholar 

  30. 30

    Schönknecht, G. et al. Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339, 1207–1210 (2013).

    PubMed  Google Scholar 

  31. 31

    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).

    CAS  PubMed  Google Scholar 

  32. 32

    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).

    PubMed  Google Scholar 

  33. 33

    Balsera, M., Uberegui, E., Schürmann, P. & Buchanan, B. B. Evolutionary development of redox regulation in chloroplasts. Antioxid. Redox. Signal. 21, 1327–1355 (2014).

    CAS  PubMed  Google Scholar 

  34. 34

    Scheibe, R. & Dietz, K.-J. Reduction–oxidation network for flexible adjustment of cellular metabolism in photoautotrophic cells. Plant Cell Environ. 35, 202–216 (2012).

    CAS  PubMed  Google Scholar 

  35. 35

    Imlay, J. A. What biological purpose is served by superoxide reductase? J. Biol. Inorg. Chem. 7, 659–663 (2002).

    CAS  PubMed  Google Scholar 

  36. 36

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. 37

    Susanti, D. et al. Thioredoxin targets fundamental processes in a methane producing archaeon. Methanocaldococcus jannaschii. Proc. Natl Acad. Sci. USA 111, 2608–2613 (2014).

    CAS  PubMed  Google Scholar 

  38. 38

    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).

    CAS  PubMed  Google Scholar 

  39. 39

    Poole, L. B. The basics of thiols and cysteines in redox biology and chemistry. Free Radic. Biol. Med. 80, 148–157 (2015).

    CAS  PubMed  Google Scholar 

  40. 40

    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).

    CAS  PubMed  Google Scholar 

  41. 41

    Federhen, S. The NCBI taxonomy database. Nucleic Acids Res. 40 (D1), D136–D143 (2012).

    CAS  PubMed  Google Scholar 

  42. 42

    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).

    PubMed  PubMed Central  Google Scholar 

  43. 43

    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).

    PubMed  PubMed Central  Google Scholar 

  44. 44

    Benson, D. A. et al. Genbank. Nucleic Acids Res. 43 (D1), D30–D35 (2015).

    CAS  PubMed  Google Scholar 

  45. 45

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. 46

    Kent, W. J. BLAT—the BLAST-like alignment tool. Genome Res. 12, 656–664 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. 47

    Camacho, C. et al. Blast+: architecture and applications. BMC Bioinformatics 10, 421 (2009).

    PubMed  PubMed Central  Google Scholar 

  48. 48

    Tatusov, R. L., Koonin, E. V. & Lipman, D. J. A genomic perspective on protein families. Science 278, 631–637 (1997).

    CAS  Google Scholar 

  49. 49

    Rice, P., Longden, I. & Bleasby, A. Emboss: the European molecular biology open software suite. Trends Genet. 16, 276–277 (2000).

    CAS  PubMed  Google Scholar 

  50. 50

    Katoh, K. & Standley, D. M. Mafft multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. 51

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52

    Guindon, S., Delsuc, F., Dufayard, J.-F. & Gascuel, O. Estimating maximum likelihood phylogenies with PhyML. Methods Mol. Biol. 537, 113–137 (2009).

    CAS  PubMed  Google Scholar 

  53. 53

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54

    Farris, J. S. Estimating phylogenetic trees from distance matrices. Am. Nat. (1972).

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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).

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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.

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Correspondence to Christian Woehle or Shilo Rosenwasser.

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The authors declare no competing financial interests.

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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

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