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PreprintCited by 1Silk-based biomaterials and applicationsSpider Taxonomy and Behavior StudiesSilkworms and Sericulture Research

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A Newly Evolved Small Secretory Peptide Enhances Mechanical Properties of Spider Silk

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Wang, Yi, Jia, Anqiang, Mao, Yudi, Yang, Tianfang, Zhang, Guoqing, Wang, Qingyuan, Hu, Wenbo, Dong, Zhaoming, Zhang, Zhisheng, Ma, Sanyuan·2025·Nature Communications
DOI 10.21203/rs.3.rs-6320776/v1PMC PMC12627769

Preprint — published as 10.1038/s41467-025-65026-1

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Abstract

The ability of spiders to spin foraging webs by silk from specialized glands represents a remarkable evolutionary innovation, yet the molecular evolution of silk glands remains poorly understood. Herein, we explored the evolution of silk glands in Araneoidea spiders through comprehensive genomic and transcriptomic mining. Following the divergence of ancestral Araneoidea clades, numerous new genes with simplified structures and constrained expression patterns emerged, expressed predominantly in silk glands and coexpressed with ancient genes to drive the evolution of silk glands. Among these, SpiCE-DS8 is a newly evolved small secretory peptide, which is incorporated into dragline silk and is involved in the MaSp network. SpiCE-DS8 originated de novo from intergenic regions of ancient genes and is an orphan gene unique to the Nephilinae subfamily. It interacts with the N-terminal region of MaSp1b, potentially aiding in silk protein solidification. In vitro wet-spinning experiments demonstrated that SpiCE-DS8 significantly improved fiber properties, including the β-sheet content and mechanical strength, with the conserved SpiCE-DS8-S showing even more pronounced effects. The enhanced silk properties allow spiders to arm their foraging webs for more efficient prey capture. This study highlights the pivotal role of new lineage-specific genes in silk gland evolution, providing new insights into the evolutionary mechanisms associated with foraging webs and for advancing synthetic silk material development.

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Fig. 1 Identification framework, distribution patterns, and sequence features of new genes in spiders. a Gene classification into different PS levels on the basis of an organized workflow. b The 16 PS levels of T. clavata, spanning from the genes of the most ancient cellular organisms to the most recent species-specific genes. RAGs refer to relatively ancient genes, while RYGs refer to relatively young genes. c Gene number distribution across the 16 PS levels in T. clavata. The Venn diagram in the lower-right corner shows that genes from PS13 to PS16 are annotated as genes of unknown function. d–f Box plots showing the transition of genes across the 16 PS levels from ancient to young genes, with decreases in the exon length and protein sequence length, and an increase in the Tau index. The Tau index measures the specificity or breadth of gene or transcript expression across analyzed tissues. The gene sets analyzed for each PS level (PS1–PS16) in d–f are identical to those quantified in c. Box plots display the median (center line), the 25th and 75th percentiles (box limits), and the minimum and maximum values within 1.5× the interquartile range (whiskers).
Fig. 1 Identification framework, distribution patterns, and sequence features of new genes in spiders. a Gene classification into different PS levels on the basis of an organized workflow. b The 16 PS levels of T. clavata, spanning from the genes of the most ancient cellular organisms to the most recent species-specific genes. RAGs refer to relatively ancient genes, while RYGs refer to relatively young genes. c Gene number distribution across the 16 PS levels in T. clavata. The Venn diagram in the lower-right corner shows that genes from PS13 to PS16 are annotated as genes of unknown function. d–f Box plots showing the transition of genes across the 16 PS levels from ancient to young genes, with decreases in the exon length and protein sequence length, and an increase in the Tau index. The Tau index measures the specificity or breadth of gene or transcript expression across analyzed tissues. The gene sets analyzed for each PS level (PS1–PS16) in d–f are identical to those quantified in c. Box plots display the median (center line), the 25th and 75th percentiles (box limits), and the minimum and maximum values within 1.5× the interquartile range (whiskers).CC BY-NC-ND · PubMed Central
Fig. 2 Coexpression network intertwining ancient and young genes. a Heatmap of gene expression correlations across the 16 PS levels, calculated using Pearson correlation, revealing a modular expression pattern. Tissue order in each PS heatmap (top-to-bottom, left-to-right) follows the arrow-indicated order in the legend. Correlation strength is shown by the blue-to-red gradient. b Distribution of silk gland-expressed genes and tissue-specific silk gland genes across the 16 PS levels. c Coexpression modules significantly correlated with Ma, Ag, Tu, and Py&Ac. Node size represents normalized expression (log2(TPM + 1)); bold borders indicate silk gland–specific spidroin genes. Pearson correlation coefficients (r) with two-tailed P-values are annotated at the top of the figure. Genes from PS1–PS12 and PS13–PS16 are distinguished by light and dark shading, respectively; tissues are colored as indicated in the legend. Ma major ampullate gland, Mi minor ampullate gland, Tu tubuliform gland, Fl flagelliform gland, Ag aggregate gland, Ac&Py mixed aciniform and pyriform gland, Hem hemolymph, Ped pedipalp, Leg legs, Epi epidermis, Ven venom gland, Fat fat body, Ova ovary.
Fig. 2 Coexpression network intertwining ancient and young genes. a Heatmap of gene expression correlations across the 16 PS levels, calculated using Pearson correlation, revealing a modular expression pattern. Tissue order in each PS heatmap (top-to-bottom, left-to-right) follows the arrow-indicated order in the legend. Correlation strength is shown by the blue-to-red gradient. b Distribution of silk gland-expressed genes and tissue-specific silk gland genes across the 16 PS levels. c Coexpression modules significantly correlated with Ma, Ag, Tu, and Py&Ac. Node size represents normalized expression (log2(TPM + 1)); bold borders indicate silk gland–specific spidroin genes. Pearson correlation coefficients (r) with two-tailed P-values are annotated at the top of the figure. Genes from PS1–PS12 and PS13–PS16 are distinguished by light and dark shading, respectively; tissues are colored as indicated in the legend. Ma major ampullate gland, Mi minor ampullate gland, Tu tubuliform gland, Fl flagelliform gland, Ag aggregate gland, Ac&Py mixed aciniform and pyriform gland, Hem hemolymph, Ped pedipalp, Leg legs, Epi epidermis, Ven venom gland, Fat fat body, Ova ovary.CC BY-NC-ND · PubMed Central
Fig. 3 Classification and expression patterns of RAYs. a ML phylogenetic tree of 16 spiders based on concatenated protein sequences of 144 single-copy genes. b Schematic diagram of genes classified as de novo, duplicate, or orphan genes. c Distribution of de novo, duplicate, and orphan genes in PS13–PS16 on the basis of genomic alignment. d Expression patterns of 232 Araneoidea-specific genes across 13 tissues of T. clavata. Trichonephila inaurata ma. refers to Trichonephila inaurata madagascariensis.
Fig. 3 Classification and expression patterns of RAYs. a ML phylogenetic tree of 16 spiders based on concatenated protein sequences of 144 single-copy genes. b Schematic diagram of genes classified as de novo, duplicate, or orphan genes. c Distribution of de novo, duplicate, and orphan genes in PS13–PS16 on the basis of genomic alignment. d Expression patterns of 232 Araneoidea-specific genes across 13 tissues of T. clavata. Trichonephila inaurata ma. refers to Trichonephila inaurata madagascariensis.CC BY-NC-ND · PubMed Central
Fig. 4 Transcriptomic and proteomic profiles and interaction networks of new genes associated with Ma tissue. a Upset plot of genes identified in dragline silk and the tail, sac, and duct proteomes of the Ma tissue. The numbers highlighted in red in the plot represent new genes identified in the three segments of the Ma gland or dragline silk. The genes SpiCE-DS5 and SpiCE-DS8, indicated by arrows, were also identified in dragline silk. b Transcriptomic and proteomic profiles of 14 new genes in the Ma gland and dragline silk. c Coexpression network of the SpiCE-DS5, SpiCE-DS8, and MaSp genes on the basis of expression profiles from 13 tissues. The RAGs and RYGs are represented in different colors, with the node size reflecting the normalized TPM expression values, which are calculated as log2(TPM + 1). d Gene coexpression network based on single-cell expression levels from the Ma gland. The top five genes of each module are displayed.
Fig. 4 Transcriptomic and proteomic profiles and interaction networks of new genes associated with Ma tissue. a Upset plot of genes identified in dragline silk and the tail, sac, and duct proteomes of the Ma tissue. The numbers highlighted in red in the plot represent new genes identified in the three segments of the Ma gland or dragline silk. The genes SpiCE-DS5 and SpiCE-DS8, indicated by arrows, were also identified in dragline silk. b Transcriptomic and proteomic profiles of 14 new genes in the Ma gland and dragline silk. c Coexpression network of the SpiCE-DS5, SpiCE-DS8, and MaSp genes on the basis of expression profiles from 13 tissues. The RAGs and RYGs are represented in different colors, with the node size reflecting the normalized TPM expression values, which are calculated as log2(TPM + 1). d Gene coexpression network based on single-cell expression levels from the Ma gland. The top five genes of each module are displayed.CC BY-NC-ND · PubMed Central
Fig. 5 Sequence evolution of the SpiCE-DS8 gene and its inferred 3D interaction structure with MaSp. a Multiple sequence alignment of SpiCE-DS8 across four spiders. b Phylogenetic relationships of SpiCE-DS8 genes and their flanking genes in 16 spiders. The phylogenetic tree was constructed via the maximum likelihood (ML) method on the basis of the sequences of 144 single-copy genes. c Prediction of the 3D structure and interaction model of MaSp1b and SpiCE-DS8-L/SpiCE-DS8-S. d Interaction heatmap showing the N-terminal interaction of SpiCE-DS8-L/SpiCE-DS8-S with MaSp1b. e SpiCE-DS8 interacts with MaSp1b and its N-terminal domain (MaSp1b-N). The input group represents total protein, while the IgG and IP groups represent proteins after immunoprecipitation. The prey protein signal was detected in the IP group but not in the IgG group, indicating an interaction between the two proteins. The bait protein signal was also detected in the IP group, confirming successful immunoprecipitation. These results were reproduced in three independent biological replicates with similar outcomes. Source data are provided as a Source data file.
Fig. 5 Sequence evolution of the SpiCE-DS8 gene and its inferred 3D interaction structure with MaSp. a Multiple sequence alignment of SpiCE-DS8 across four spiders. b Phylogenetic relationships of SpiCE-DS8 genes and their flanking genes in 16 spiders. The phylogenetic tree was constructed via the maximum likelihood (ML) method on the basis of the sequences of 144 single-copy genes. c Prediction of the 3D structure and interaction model of MaSp1b and SpiCE-DS8-L/SpiCE-DS8-S. d Interaction heatmap showing the N-terminal interaction of SpiCE-DS8-L/SpiCE-DS8-S with MaSp1b. e SpiCE-DS8 interacts with MaSp1b and its N-terminal domain (MaSp1b-N). The input group represents total protein, while the IgG and IP groups represent proteins after immunoprecipitation. The prey protein signal was detected in the IP group but not in the IgG group, indicating an interaction between the two proteins. The bait protein signal was also detected in the IP group, confirming successful immunoprecipitation. These results were reproduced in three independent biological replicates with similar outcomes. Source data are provided as a Source data file.CC BY-NC-ND · PubMed Central
Fig. 6 In vitro spinning enhanced the mechanical properties of silk fibroin with SpiCE-DS8. a Schematic of the in vitro spinning process for a silk fibroin and SpiCE-DS8 mixed solution. Image created with Adobe Illustrator 2020. b Scanning electron microscopy (SEM) image of spun silk fibers. This experiment was performed in three independent biological replicates, with similar results observed. c Determination of the secondary structure content of spun silk fibers using FTIR spectroscopy. d Stress‒strain curve of spun silk fibers. Fibroin represents the silk fibroin of silkworm cocoons, and SP2-KI represents cocoons of the spidroin-expressing silkworm. Data reflect measurements from 30 independent biological replicates (n = 30). Source data are provided as a Source data file.
Fig. 6 In vitro spinning enhanced the mechanical properties of silk fibroin with SpiCE-DS8. a Schematic of the in vitro spinning process for a silk fibroin and SpiCE-DS8 mixed solution. Image created with Adobe Illustrator 2020. b Scanning electron microscopy (SEM) image of spun silk fibers. This experiment was performed in three independent biological replicates, with similar results observed. c Determination of the secondary structure content of spun silk fibers using FTIR spectroscopy. d Stress‒strain curve of spun silk fibers. Fibroin represents the silk fibroin of silkworm cocoons, and SP2-KI represents cocoons of the spidroin-expressing silkworm. Data reflect measurements from 30 independent biological replicates (n = 30). Source data are provided as a Source data file.CC BY-NC-ND · PubMed Central
Fig. 7 Brief illustration of the silk performance enhancements in Araneoidea spiders. The curve at the bottom of the figure shows approximately 225 million years of global temperature changes, corresponding to temperatures on the right thermometer; this curve was drawn according to the study by Voosen61. The divergence time of Araneoidea was ~182 Mya according to TimeTree98. The timeline of angiosperms, insects, and spiders at the top of the figure relates to geological origins. The red line in the spider web represents the dragline silk, and the thin to thick lines represent the silk toughness enhancements. The green solid circle represents the aggregate glue. Image created with Adobe Illustrator 2020.
Fig. 7 Brief illustration of the silk performance enhancements in Araneoidea spiders. The curve at the bottom of the figure shows approximately 225 million years of global temperature changes, corresponding to temperatures on the right thermometer; this curve was drawn according to the study by Voosen61. The divergence time of Araneoidea was ~182 Mya according to TimeTree98. The timeline of angiosperms, insects, and spiders at the top of the figure relates to geological origins. The red line in the spider web represents the dragline silk, and the thin to thick lines represent the silk toughness enhancements. The green solid circle represents the aggregate glue. Image created with Adobe Illustrator 2020.CC BY-NC-ND · PubMed Central

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Metadata

Authors
Wang, Y., Jia, A., Mao, Y., Yang, T., Zhang, G., Wang, Q., Hu, W., Dong, Z., Zhang, Z., & Ma, S.
Affiliations
  • Southwest University (CN)
  • Southwest University
Corresponding author
  • Wang, Yi
  • Ma, Sanyuan
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2025-04-18
Volume
16
Issue
1
Pages
10071-10071
ISSN
2041-1723 (ISSN-L)
DOI
10.21203/rs.3.rs-6320776/v1
PMC
PMC12627769
OpenAlex
W4416334188
Cited by
1
References
1
Citations by year
2026: 1
FWCI
0.21
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by-nc-nd)
  • Research Square (acceptedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Jiangsu University
  • Southwest University
  • Jiangsu University of Science and Technology
  • Centre Scientifique et Technique du Bâtiment
  • National Key Research and Development Program of China (2023YFF0713900)
  • Fundamental Research Funds for the Central Universities (Swu‐XDJH202309)
Topics
  • Physical Sciences › Materials Science › Biomaterials › Silk-based biomaterials and applications
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Spider Taxonomy and Behavior Studies
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Silkworms and Sericulture Research
Keywords
spider silk, Araneoidea, secretory peptides, spider dragline silk, silk mechanical properties, wet spinning, prey capture, synthetic silk, gene co-expression
MeSH terms
Amino Acid Sequence, Animals, Fibroins, Peptides, Phylogeny, Spiders, Evolution, Molecular, Silk, Transcriptome

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This page
CoChat. (2026). Citation check: A Newly Evolved Small Secretory Peptide Enhances Mechanical Properties of Spider Silk. https://app.cochat.ai/papers/10.21203/rs.3.rs-6320776/v1
The paper
Wang, Y., Jia, A., Mao, Y., Yang, T., Zhang, G., Wang, Q., Hu, W., Dong, Z., Zhang, Z., & Ma, S. (2025). A Newly Evolved Small Secretory Peptide Enhances Mechanical Properties of Spider Silk. Nature Communications. https://doi.org/10.21203/rs.3.rs-6320776/v1