Absence of fibroin H sequences and a significant divergence in the putative fibroin L homolog in Neomicropteryx cornuta (Micropterigidae) silk
Language English Country Great Britain, England Media electronic
Document type Journal Article
Grant support
BYCZ01-039
EC | Europski Fond za Regionalni Razvoj | Interreg
PubMed
40082689
PubMed Central
PMC11906653
DOI
10.1038/s42003-025-07801-w
PII: 10.1038/s42003-025-07801-w
Knihovny.cz E-resources
- MeSH
- Fibroins * genetics chemistry metabolism MeSH
- Phylogeny MeSH
- Silk * genetics chemistry metabolism MeSH
- Insect Proteins * genetics metabolism MeSH
- Lepidoptera * genetics metabolism MeSH
- Evolution, Molecular MeSH
- Moths * genetics metabolism MeSH
- Amino Acid Sequence MeSH
- Transcriptome MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Fibroins * MeSH
- Silk * MeSH
- Insect Proteins * MeSH
Micropterigidae is regarded as the sister group of all the other Lepidoptera, providing important insights into the evolution of Lepidoptera. However, the gene and protein profiles of silk from Micropterigidae have not yet been identified. In this study, we investigate the components of silk cocoons of the micropterigid species Neomicropteryx cornuta. Here we show that the protein fibroin heavy chain (FibH) is absent in the silk of N. cornuta and that the putative homolog of fibroin light chain (FibL) is also absent or severely altered. This is confirmed by transcriptome and genome analyses of the conserved regions in this species. The examination of the synteny around the fibH genes in several Lepidoptera and Trichoptera species shows that the genomic region containing this gene is absent in another micropterigid species, Micropterix aruncella. In contrast, we found putative orthologs of fibH and fibL in the representative transcripts of another distinct clade, Eriocraniidae. This study shows that the loss of FibH and the loss or severe divergence of FibL occurrs specifically in the family Micropterigidae and reveals dynamic evolutionary changes in silk composition during the early evolution of Lepidoptera. It also shows that silk proteins without FibH can form a solid cocoon.
Faculty of Science University of South Bohemia Ceske Budejovice 37005 Czech Republic
Kyoto University Graduate School of Science Kyoto 606 8502 Japan
See more in PubMed
Kenchington, W. Biological and chemical aspects of silks and silk-like materials produced by arthropods. S. Pac. J. Nat. Sci.5, 10–45 (1984).
Sutherland, T. D., Young, J. H., Weisman, S., Hayashi, C. Y. & Merritt, D. J. Insect silk: one name, many materials. Annu Rev. Entomol.55, 171–188 (2010). PubMed
Beutel, R. G., Friedrich, F., Ge, S.-Q. & Yang, X. K. Insect Morphology and Phylogeny: A Textbook For Students of Entomology Vol. 531 (De Gruyter, 2014).
Kristensen, N. P. e. Lepidoptera, Moths and butterflies. Vol. 1: Evolution, Systematics and Biogeography. Handbook of Zoology Vol. IV (De Gruyter, 1999).
Sehnal, F. & Zurovec, M. Construction of silk fiber core in lepidoptera. Biomacromolecules5, 666–674 (2004). PubMed
Akai, H. In Insect Ultrastructure (eds King, R. C. & Akai, H.) 323–364 (Plenum Press, New York, 1984).
Kludkiewicz, B. et al. The expansion of genes encoding soluble silk components in the greater wax moth, Galleria mellonella. Insect Biochem. Mol. Biol.106, 28–38 (2019). PubMed
Takasu, Y., Yamada, H. & Tsubouchi, K. Isolation of three main sericin components from the cocoon of the silkworm. Bombyx. Mori. Biosci. Biotech. Bioch.66, 2715–2718 (2002). PubMed
Rouhova, L. et al. Comprehensive analysis of silk proteins and gland compartments in Limnephilus lunatus, a case-making trichopteran. Bmc Genomics25, 472 (2024). PubMed PMC
Rouhova, L. et al. Using the multi-omics approach to reveal the silk composition in Plectrocnemia conspersa. Front Mol. Biosci.9, 945239 (2022). PubMed PMC
Fedic, R., Zurovec, M. & Sehnal, F. Correlation between fibroin amino acid sequence and physical silk properties. J. Biol. Chem.278, 35255–35264 (2003). PubMed
Heckenhauer, J. et al. Characterization of the primary structure of the major silk gene, h-fibroin, across caddisfly (Trichoptera) suborders. iScience26, 107253 (2023). PubMed PMC
Yonemura, N., Mita, K., Tamura, T. & Sehnal, F. Conservation of silk genes in Trichoptera and Lepidoptera. J. Mol. Evol.68, 641–653 (2009). PubMed PMC
Zurovec, M. et al. Functional conservation and structural diversification of silk sericins in two moth species. Biomacromolecules14, 1859–1866 (2013). PubMed
Regier, J. C. et al. A molecular phylogeny for the oldest (nonditrysian) lineages of extant Lepidoptera, with implications for classification, comparative morphology and life-history evolution. Syst. Entomol.40, 671–704 (2015).
Shimura, K., Kikuchi, A., Ohtomo, K., Katagata, Y. & A, H. Studies on silk fibroin of Bombyx mori. I. Fractionation of fibroin prepared from the posterior silk gland. J. Biochem.80, 693–702 (1976). PubMed
Kawahara, Y. et al. Comprehensive study on the formation of higher-order structure of bombyx mori silkworm fibers: influence of sericin fractions, modulation of spinning process, and metal ion interactions. J. Fiber Sci. Technol.74, 95–108 (2018).
Liao, C. Q. et al. Higher-level phylogeny and evolutionary history of nonditrysians (Lepidoptera) inferred from mitochondrial genome sequences. Zool. J. Linn. Soc. Lond.198, 476–493 (2023).
Hu, W. B., Lu, W., Wei, L. W., Zhang, Y. & Xia, Q. Y. Molecular nature of dominant naked pupa mutation reveals novel insights into silk production. Insect Biochem. Molec.109, 52–62 (2019). PubMed
Mase, K., Iizuka, T., Okada, E., Miyajima, T. & Yamamoto, T. A new silkworm race for sericin production, “SERICIN HOPE” and its product, “VIRGIN SERICIN”. J. Insect Biotechnol. Sericol.75, 85–88 (2006).
Wu, B. C. et al. Characterization of silk genes in Ephestia kuehniella and Galleria mellonella revealed duplication of sericin genes and highly divergent sequences encoding fibroin heavy chains. Front Mol. Biosci.9, 1023381 (2022). PubMed PMC
Teshome, A., Vollrath, F., Raina, S. K., Kabaru, J. M. & Onyari, J. Study on the microstructure of African wild silk cocoon shells and fibers. Int. J. Biol. Macromol.50, 63–68 (2012). PubMed
Davis, D. R. & Landry, J. F. A review of the North American genus Epimartyria (Lepidoptera, Micropterigidae) with a discussion of the larval plastron. Zookeys183, 37–83 (2012). PubMed PMC
Klausnitzer, B., Meyer, E., Kössler, W. & Eisenbeis, G. On the larval morphology of micropterix arincella (Scopoli, 1763). Beitrage Ent.52, 353–356 (2002).
Wang, X., Li, Y., Liu, Q., Xia, Q. & Zhao, P. Proteome profile of spinneret from the silkworm, Bombyx mori. Proteomics10.1002/pmic.201600301 (2017). PubMed
Heath, J. In Micropterigidae—Heliozelidae Vol. 1 The Moths and Butterflies of Great Britain and Ireland (eds Langmaid, J., Emmet, A. M., & Heath, J.) 151 (Harley Books, 1976).
Imada, Y., Kawakita, A. & Kato, M. Allopatric distribution and diversification without niche shift in a bryophyte-feeding basal moth lineage (Lepidoptera: Micropterigidae). P. Roy Soc. B. Biol. Sci.278, 3026–3033 (2011). PubMed PMC
Levine, J. D., Sauman, I., Imbalzano, M., Reppert, S. M. & Jackson, F. R. Period protein from the giant silkmoth Antheraea pernyi functions as a circadian clock element in Drosophila melanogaster. Neuron15, 147–157 (1995). PubMed
Rouhova, L. et al. Silk of the common clothes moth, Tineola bisselliella, a cosmopolitan pest belonging to the basal ditrysian moth line. Insect Biochem. Molec.130, 103527 (2021). PubMed
Afgan, E. et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res.46, W537–W544 (2018). PubMed PMC
Simao, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics31, 3210–3212 (2015). PubMed
Hughes, C. S. et al. Ultrasensitive proteome analysis using paramagnetic bead technology. Mol. Syst. Biol.10, 757 (2014). PubMed PMC
Rappsilber, J., Mann, M. & Ishihama, Y. Protocol for micro-purification, enrichment. Nat. Protoc.2, 1896–1906 (2007). PubMed
Cox, J. et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res.10, 1794–1805 (2011). PubMed
Hall, T. A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids. Symp. Ser.41, 95–98 (1999).
Stothard, P. The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques28, 1102 (2000). PubMed
Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol.33, 1870–1874 (2016). PubMed PMC
Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol.32, 268–274 (2015). PubMed PMC
Kalyaanamoorthy, S. et al. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods14, 587–589 (2017). PubMed PMC
Xie, J. M. et al. Tree visualization by one table (tvBOT): a web application for visualizing, modifying and annotating phylogenetic trees. Nucleic Acids Res.51, W587–W592 (2023). PubMed PMC
Li, X. et al. First annotated genome of a mandibulate moth, Neomicropteryx cornuta, generated using PacBio HiFi sequencing. Genome Biol. Evol.13, evab229 (2021). PubMed PMC