Origin, structure, and composition of the spider major ampullate silk fiber revealed by genomics, proteomics, and single-cell and spatial transcriptomics

Author:

Sonavane Sumalata1ORCID,Hassan Sameer2,Chatterjee Urmimala2ORCID,Soler Lucile34ORCID,Holm Lena1ORCID,Mollbrink Annelie5ORCID,Greco Gabriele1ORCID,Fereydouni Noah2ORCID,Vinnere Pettersson Olga6ORCID,Bunikis Ignas6,Churcher Allison7ORCID,Lantz Henrik34,Johansson Jan2,Reimegård Johan3ORCID,Rising Anna12ORCID

Affiliation:

1. Department of Animal Biosciences, Swedish University of Agricultural Sciences, Uppsala, Sweden.

2. Department of Biosciences and Nutrition, Karolinska Institutet, Neo, Huddinge, Sweden.

3. National Bioinformatics Infrastructure Sweden (NBIS), Science for Life Laboratory (SciLifeLab), Uppsala University, Uppsala, Sweden.

4. Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.

5. Department of Gene Technology, KTH Royal Institute of Technology, SciLifeLab, Stockholm, Sweden.

6. Department of Immunology, Genetics and Pathology, National Genomics Infrastructure, SciLifeLab, Uppsala, Sweden.

7. Department of Molecular Biology, NBIS, SciLifeLab, Umeå University, Umeå, Sweden.

Abstract

Spiders produce nature’s toughest fiber using renewable components at ambient temperatures and with water as solvent, making it highly interesting to replicate for the materials industry. Despite this, much remains to be understood about the bioprocessing and composition of spider silk fibers. Here, we identify 18 proteins that make up the spiders’ strongest silk type, the major ampullate fiber. Single-cell RNA sequencing and spatial transcriptomics revealed that the secretory epithelium of the gland harbors six cell types. These cell types are confined to three distinct glandular zones that produce specific combinations of silk proteins. Image analysis of histological sections showed that the secretions from the three zones do not mix, and proteomics analysis revealed that these secretions form layers in the final fiber. Using a multi-omics approach, we provide substantial advancements in the understanding of the structure and function of the major ampullate silk gland as well as of the architecture and composition of the fiber it produces.

Publisher

American Association for the Advancement of Science (AAAS)

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