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Journal of Molecular Evolution

, Volume 82, Issue 6, pp 279–290 | Cite as

Evolution of the SOUL Heme-Binding Protein Superfamily Across Eukarya

  • Antonio Emidio FortunatoEmail author
  • Paolo Sordino
  • Nikos AndreakisEmail author
Original Article

Abstract

SOUL homologs constitute a heme-binding protein superfamily putatively involved in heme and tetrapyrrole metabolisms associated with a number of physiological processes. Despite their omnipresence across the tree of life and the biochemical characterization of many SOUL members, their functional role and the evolutionary events leading to such remarkable protein repertoire still remain cryptic. To explore SOUL evolution, we apply a computational phylogenetic approach, including a relevant number of SOUL homologs, to identify paralog forms and reconstruct their genealogy across the tree of life and within species. In animal lineages, multiple gene duplication or loss events and paralog functional specializations underlie SOUL evolution from the dawn of ancestral echinoderm and mollusc SOUL forms. In photosynthetic organisms, SOUL evolution is linked to the endosymbiosis events leading to plastid acquisition in eukaryotes. Derivative features, such as the F2L peptide and BH3 domain, evolved in vertebrates and provided innovative functionality to support immune response and apoptosis. The evolution of elements such as the N-terminal protein domain DUF2358, the His42 residue, or the tetrapyrrole heme-binding site is modern, and their functional implications still unresolved. This study represents the first in-depth analysis of SOUL protein evolution and provides novel insights in the understanding of their obscure physiological role.

Keywords

SOUL Evolution Heme binding Tetrapyrrole metabolism Light sensing Apoptosis 

Notes

Acknowledgments

This research was supported by an SZN-Funded University of Palermo PhD Program and a Travel Grant “Premio Brancaccio 2009” from Lions Club “Megaride” (Napoli, Italy) to AEF. PS is supported by a MIUR PON Grant (PONa3_00239) and a FIRB Grant (RBFR12QW4I). NA is funded through the National Environmental Research Program (NERP), an Australian Government Initiative supporting world class, public good research. The NERP Marine Biodiversity Hub is a collaborative partnership between the University of Tasmania, CSIRO Wealth from Oceans Flagship, Geoscience Australia, Australian Institute of Marine Science, Museum Victoria, Charles Darwin University, and the University of Western Australia (www.nerpmarine.edu.au).

Compliance with Ethical Standards

Conflict of interest

The authors declare that there is no conflict of interest that would prejudice the impartiality of this scientific work.

Supplementary material

239_2016_9745_MOESM1_ESM.pdf (310 kb)
Supplementary material 1 (PDF 309 kb) Genealogy of all SOUL homologs identified in this study. Unrooted ML phylogenetic hypothesis of SOUL protein sequences from metazoan, non-metazoan, and photosynthetic organisms. A1 and A2 refer to animal branches. Clusters A1 and A2 include all the sequences used to compute the phylogenetic hypotheses shown in Figs. 1, 2, S2 and S3. P denotes SOUL from primary endosymbionts (green branches, Archaeplastida). S indicates SOUL proteins from both primary and secondary endosymbionts (brown branches). Clusters P and S include all the sequences used for the phylogenetics hypothesis shown in Fig. 3. The two long black branches include the eight bacterial SOUL isoforms reported in Table 1
239_2016_9745_MOESM2_ESM.pdf (533 kb)
Supplementary material 2 (PDF 533 kb) SOUL genealogy inferred from vertebrates and selected invertebrate sequences. Maximum likelihood phylogenetic hypothesis of SOUL vertebrate and selected invertebrate homologous protein sequences. The positions of Ciona and Amphioxus are highlighted in gray. Color gradients denote bootstrap support distributed across the topology. A1 and A2 refer to animal branches
239_2016_9745_MOESM3_ESM.pdf (368 kb)
Supplementary material 3 (PDF 367 kb) SOUL genealogy in invertebrates. Maximum likelihood genealogical hypothesis of SOUL invertebrate homologous protein sequences. Color gradients denote bootstrap support distributed across the phylogeny. Cnidarian SOUL orthologs were used as outgroup
239_2016_9745_MOESM4_ESM.pdf (431 kb)
Supplementary material 4 (PDF 430 kb) Functional domain mapping in vertebrate SOUL proteins. Mapping the heme-binding site, His42, signal peptide, BH3 domain, and F2L peptide in selected vertebrate SOUL proteins based on the phylogenetic tree in Fig. 1. Filled and empty circles indicate the presence or absence, respectively, of a specific feature following the legend
239_2016_9745_MOESM5_ESM.pdf (509 kb)
Supplementary material 5 (PDF 509 kb) Functional domain mapping in SOUL mined from photosynthetic organisms. Mapping the domain DUF2458, the signal peptide, and the putative localization in selected SOUL proteins from photosynthetic organisms based on the phylogenetic tree in Fig. 3. Filled and empty circles indicate the presence or absence, respectively, of a specific feature following the legend
239_2016_9745_MOESM6_ESM.fas (66 kb)
Supplementary material 6 (FAS 67 kb) SOUL sequences alignment used for the “Global” tree
239_2016_9745_MOESM7_ESM.fas (27 kb)
Supplementary material 7 (FAS 27 kb) SOUL sequences alignment used for the “Vertebrate” tree
239_2016_9745_MOESM8_ESM.txt (10 kb)
Supplementary material 8 (TXT 10 kb) SOUL sequences alignment used for the “Invertebrate” tree
239_2016_9745_MOESM9_ESM.fas (29 kb)
Supplementary material 9 (FAS 30 kb) SOUL sequences alignment used for the “Vertebrate + Invertebrate” tree
239_2016_9745_MOESM10_ESM.txt (14 kb)
Supplementary material 10 (TXT 14 kb) SOUL sequences alignment used for the “Invertebrate + Vertebrate” tree
239_2016_9745_MOESM11_ESM.fas (33 kb)
Supplementary material 11 (FAS 34 kb) SOUL sequences alignment used for the “Photosynthetic organisms” tree
239_2016_9745_MOESM12_ESM.pdf (156 kb)
Supplementary material 12 (PDF 155 kb) SOUL sequences and their accession numbers used in this work

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Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Sorbonne Universités, UPMCInstitut de Biologie Paris-Seine, CNRS, Laboratoire de Biologie Computationnelle et Quantitative UMR 7238ParisFrance
  2. 2.Biology and Evolution of Marine OrganismsStazione Zoologica Anton DohrnNaplesItaly
  3. 3.Australian Institute of Marine ScienceTownsville MCAustralia
  4. 4.College of Marine and Environmental SciencesJames Cook UniversityTownsvilleAustralia

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