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Journal of Molecular Evolution

, Volume 80, Issue 5–6, pp 278–291 | Cite as

A Proposal for the Evolution of Cathepsin and Silicatein in Sponges

  • Ana Riesgo
  • Manuel Maldonado
  • Susanna López-Legentil
  • Gonzalo Giribet
Original Article

Abstract

Cathepsins are enzymes capable of degrading proteins intracellularly. They occur ubiquitously in opisthokonts, but their potential to provide insight across the evolutionary transition from protists to metazoans remains poorly investigated. Here, we explore the evolution of cathepsins using comparative analyses of transcriptomic datasets, focusing on both, protists (closely related to metazoans), and early divergent animals (i.e., sponges). We retrieved DNA sequences of nine cathepsin types (B, C, D, F, H, L, O, Z, and silicatein) in the surveyed taxa. In choanoflagellates, only five types (B, C, L, O, Z) were identified, all of them being also found in sponges, indicating that while all cathepsins present in protists were conserved across metazoan lineages, cathepsins F and H (and probably D) are metazoan acquisitions. The phylogeny of cysteine protease cathepsins (excluding cathepsin D) revealed two major lineages: lineage B (cathepsins B and C) and lineage L (cathepsins F, H, L, O, Z). In the latter lineage, a mutation at the active site of cathepsin L gave rise to silicatein, an enzyme exclusively known to date from siliceous sponges and involved in the production of their silica spicules. However, we found that several sponges with siliceous spicules did not express silicatein genes and that, in contrast, several aspiculate sponges did contain silicatein genes. Our results suggest that the ability to silicify may have evolved independently within sponges, some of them losing this capacity secondarily. We also show that most phylogenies based on cathepsin and silicatein genes (except for that of cathepsin O) failed to recover the major lineages of sponges.

Keywords

Porifera Molecular evolution Phylogeny Next-generation sequencing Cysteine proteases 

Notes

Acknowledgments

We are grateful to Sergi Taboada, Joan Mora, and Alicia R. Pérez-Porro who helped with field sampling, and Sally Leys for providing data. This project was funded by a Marie Curie IOF Grant (PIOF-GA-2009-237219) and a Juan de la Cierva fellowship to AR, two grants (BFU2008-00227/BMC and CTM2012-37787) awarded by the Spanish Ministry of Economy and Competitiveness to MM, and the Catalan Government Grant 2014SGR-336 for Consolidated Research Groups. Illumina sequencing was supported by funds from the Museum of Comparative Zoology and by the Center from Systems Biology, Harvard University, to GG.

Supplementary material

239_2015_9682_MOESM1_ESM.xlsx (47 kb)
Primer sequences used to amplify silicatein genes in the selected sponges. Supplementary material 1 (XLSX 47 kb)
239_2015_9682_MOESM2_ESM.xlsx (32 kb)
Accession numbers from GenBank for the proteins used in the phylogenetic analysis. Sequences derived from the present analysis are highlighted in orange. Supplementary material 2 (XLSX 32 kb)
239_2015_9682_MOESM3_ESM.xlsx (92 kb)
Identity (yellow cells) and similarity (green cells) scores pairwise comparisons for all cathepsin and silicatein sequences of sponges. Values over 70 % are shown in bold letters, and maximum values for intra-group comparisons are also shown in red letters. Minimum values for intra-group comparisons are shown in blue letters. Abbreviations for sequence names are given at the end of the table. Supplementary material 3 (XLSX 92 kb)
239_2015_9682_MOESM4_ESM.xlsx (11 kb)
Metadata of the transcriptome assembly and annotation for the eight sponge species. Abbreviations: N, number; Avg., average; L, length; Max, maximum. Supplementary material 4 (XLSX 10 kb)
239_2015_9682_MOESM5_ESM.pdf (1.3 mb)
Phylogenetic analysis using maximum likelihood of cathepsin L and silicatein aminoacid sequences. Only bootstrap values over 50 are shown. Supplementary material 5 (PDF 1292 kb)
239_2015_9682_MOESM6_ESM.pdf (421 kb)
Aminoacid alignment of cathepsin and silicatein sequences showing the catalytic triad for both enzymes. Supplementary material 6 (PDF 421 kb)
239_2015_9682_MOESM7_ESM.pdf (309 kb)
Phylogenetic reconstruction of the cathepsins B, C, Z, F, H, O, L, and silicatein using Bayesian inference methods. Only posterior probabilities over 0.9 are shown. Sequences obtained in this study are in bold letters. Supplementary material 7 (PDF 308 kb)

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Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Ana Riesgo
    • 1
    • 2
  • Manuel Maldonado
    • 3
  • Susanna López-Legentil
    • 4
  • Gonzalo Giribet
    • 5
  1. 1.Department of Animal BiologyUniversity of BarcelonaBarcelonaSpain
  2. 2.Department of Life SciencesNatural History Museum of LondonLondonUK
  3. 3.Department of Marine EcologyCenter for Advanced Studies of Blanes (CEAB-CSIC)BlanesSpain
  4. 4.Department of Biology & Marine Biology, and Center for Marine ScienceUniversity of North Carolina WilmingtonWilmingtonUSA
  5. 5.Department of Organismic and Evolutionary Biology, Museum of Comparative ZoologyHarvard UniversityCambridgeUSA

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