Comparative Genomics

Evolution of silk biosynthesis and associated behavior in caddisflies

Foto: Wolfgang Graf

Institution: Senckenberg Gesellschaft für Naturforschung

SUMMARY

The properties of caddisfly silk (polymerizes in aquatic environments, high tensile strength and extensibility) make it an interesting material for potential application, e.g. in surgery. Caddisfly larvae use silk in many different ways, e.g. as underwater life lines, to build filtering nets or living retreats, and even to “glue together” mineral or organic particles to build portable cases. This diverse net- and case-making behavior allows them to exploit a range of ecological niches. In our TBG project we aim to study the genomic basis of different uses and characteristics of caddisfly silk and how these evolved. We aim to accomplish this by (1) sequencing genomes of all caddisfly groups with deviating silk use behavior and (2) comparing the sections of the genome that are responsible for silk production among closely related species of caddisflies that use silk in different ways, e.g. those that build cases made purely of silk with those that build cases with mineral particles.

The major protein components of caddisfly silks are heavy chain (h-) and light chain (l) fibroins. The identification of h-fibroingene sequences has been difficult because of their length (>20 kbp) and their highly repetitive regions. However, sequencing and assembling the entire the repetitive central region of the h-fibroin is a crucial step towards understanding how phenotypes are encoded genetically, as the repetitive regions are responsible for the strength and elasticity properties of silk fibers. We used high-quality long-read sequencing to assembly full-length h-fibroin gene sequences and characterize the primary structure of the h-fibroin across the order. We also show that there is extensive variation—both in terms of length and repeat motif order—between alleles of silk genes within individual arthropods.

Comparison of the major silk protein, h-fibroin across caddisfly (Trichoptera) suborders

The h-fibroins have conserved termini and basic motif structure with high variation in repeating modules as well as variation in the percentage of amino acids, mainly proline. This finding might be linked to differences in mechanical properties related to the different silk usage and sets a starting point for future studies to screen and correlate amino acid motifs and other sequence features with quantifiable silk properties.

TBG group members

  • Prof. Dr. Steffen Pauls (PI)
  • Jacqueline Heckenhauer, Ph.D.
  • Xiling Deng
  • Dr. Julio Schneider 
  • external: Prof. Paul Frandsen (Brigham Young University)

Group expertise / Methods

  • whole genome de novo assembly and annotation
  • population genetics
  • phylogenetics
  • anchored hybrid enrichment

Fotos: Sven Tränkner

Genomes Sequenced

25 de novo genomes of different caddisfly species (Trichoptera).

PUBLICATIONS

Paul B Frandsen, Scott Hotaling, Ashlyn Powell, Jacqueline Heckenhauer, Akito Y Kawahara, Richard H Baker, Cheryl Y Hayashi, Blanca Ríos-Touma, Ralph Holzenthal, Steffen U Pauls, Russell J Stewart (2023). Allelic resolution of insect and spider silk genes reveals hidden genetic diversity, PNAS 120 (18): e2221528120.

Scott Hotaling, Edward R Wilcox, Jacqueline Heckenhauer, Russell J Stewart, Paul B Frandsen (2023). Highly accurate long reads are crucial for realizing the potential of biodiversity genomics, BMC genomics 24 (1):1-9.

Russell J Stewart, Paul B Frandsen, Steffen U Pauls, Jacqueline Heckenhauer (2022). Conservation of three-dimensional structure of Lepidoptera and Trichoptera L-Fibroins for 290 million years, Molecules 27 (18): 5945.

Jacqueline Heckenhauer, Paul B Frandsen, John S Sproul, Zheng Li, Juraj Paule, Amanda M Larracuente, Peter J Maughan, Michael S Barker, Julio V Schneider, Russell J Stewart, Steffen U Pauls (2022). Genome size evolution in the diverse insect order Trichoptera, GigaScience 11: giac011, https://doi.org/10.1093/gigascience/giac011.

Blanca Ríos-Touma, Ralph W Holzenthal, Ernesto Rázuri-Gonzales, Jacqueline Heckenhauer, Steffen U Pauls, Caroline G Storer, Paul B Frandsen (2022). De novo genome assembly and annotation of an Andean caddisfly, Atopsyche davidsoni Sykora, 1991, a model for genome research of high-elevation adaptations, Genome Biology and Evolution 14 (1): evab286, https://doi.org/10.1093/gbe/evab286.

Xuankun Li, Emily Ellis, David Plotkin, Yume Imada, Masaya Yago, Jacqueline Heckenhauer, Timothy P Cleland, Rebecca B Dikow, Torsten Dikow, Caroline G Storer, Akito Y Kawahara, Paul B Frandsen (2021): First annotated genome of a mandibulate moth, Neomicropteryx cornuta, generated using PacBio HiFi sequencing, Genome Biology and Evolution 13 (10): evab229, https://doi.org/10.1093/gbe/evab229.

Scott Hotaling, John S Sproul, Jacqueline Heckenhauer, Ashlyn Powell, Amanda M Larracuente, Steffen U Pauls, Joanna L Kelley, Paul B Frandsen (2021). Long reads are revolutionizing 20 years of insect genome sequencing, Genome Biology and Evolution 13 (8): evab138, https://doi.org/10.1093/gbe/evab138.

Lindsey K Olsen*, Jacqueline Heckenhauer*, John S Sproul, Rebecca B Dikow, Vanessa L Gonzalez, Matthew P Kweskin, Adam M Taylor, Seth B Wilson, Russell J Stewart, Xin Zhou, Ralph Holzenthal, Steffen U Pauls, Paul B Frandsen (2021). Draft genome assemblies and annotations of Agrypnia vestita Walker, and Hesperophylax magnus Banks reveal substantial repetitive element expansion in tube case-making Caddisflies (Insecta: Trichoptera). Genome Biology and Evolution, 13(3), evab013.

Jacqueline Heckenhauer, Steffen U. Pauls (2021). Faszinierende Unterwasserarchitekten. Natur Forschung Museum 151: 74-76.

Jacqueline Heckenhauer, Paul B Frandsen, Deepak K Gupta, Juraj Paule, Stefan Prost, Tilman Schell, Julio V Schneider, Russell J Stewart, Steffen U Pauls (2019). Annotated draft genomes of two caddisfly species Plectrocnemia conspersa CURTIS and Hydropsyche tenuis NAVAS (Insecta:Trichoptera). Genome Biology and Evolution 11 (12): 3445-3451. https://doi.org/10.1093/gbe/evz264

Press Releases


Die Vielfalt der Seide. Das Gen zur Seidenproduktion bei Insekten und Spinnen zeigt individuelle Strukturen (In German)

Unlocking the Secrets of Silk Gene Evolution – Hidden variations illuminated in the diversity of silk production for the first time