The Hunt for Ancient Prions: Archaeal Prion-Like Domains Form Amyloid-Based Epigenetic Elements

Abstract Prions, proteins that can convert between structurally and functionally distinct states and serve as non-Mendelian mechanisms of inheritance, were initially discovered and only known in eukaryotes, and consequently considered to likely be a relatively late evolutionary acquisition. However,...

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Veröffentlicht in:Molecular biology and evolution 2021-05, Vol.38 (5), p.2088-2103
Hauptverfasser: Zajkowski, Tomasz, Lee, Michael D, Mondal, Shamba S, Carbajal, Amanda, Dec, Robert, Brennock, Patrick D, Piast, Radoslaw W, Snyder, Jessica E, Bense, Nicholas B, Dzwolak, Wojciech, Jarosz, Daniel F, Rothschild, Lynn J
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container_end_page 2103
container_issue 5
container_start_page 2088
container_title Molecular biology and evolution
container_volume 38
creator Zajkowski, Tomasz
Lee, Michael D
Mondal, Shamba S
Carbajal, Amanda
Dec, Robert
Brennock, Patrick D
Piast, Radoslaw W
Snyder, Jessica E
Bense, Nicholas B
Dzwolak, Wojciech
Jarosz, Daniel F
Rothschild, Lynn J
description Abstract Prions, proteins that can convert between structurally and functionally distinct states and serve as non-Mendelian mechanisms of inheritance, were initially discovered and only known in eukaryotes, and consequently considered to likely be a relatively late evolutionary acquisition. However, the recent discovery of prions in bacteria and viruses has intimated a potentially more ancient evolutionary origin. Here, we provide evidence that prion-forming domains exist in the domain archaea, the last domain of life left unexplored with regard to prions. We searched for archaeal candidate prion-forming protein sequences computationally, described their taxonomic distribution and phylogeny, and analyzed their associated functional annotations. Using biophysical in vitro assays, cell-based and microscopic approaches, and dye-binding analyses, we tested select candidate prion-forming domains for prionogenic characteristics. Out of the 16 tested, eight formed amyloids, and six acted as protein-based elements of information transfer driving non-Mendelian patterns of inheritance. We also identified short peptides from our archaeal prion candidates that can form amyloid fibrils independently. Lastly, candidates that tested positively in our assays had significantly higher tyrosine and phenylalanine content than candidates that tested negatively, an observation that may help future archaeal prion predictions. Taken together, our discovery of functional prion-forming domains in archaea provides evidence that multiple archaeal proteins are capable of acting as prions—thus expanding our knowledge of this epigenetic phenomenon to the third and final domain of life and bolstering the possibility that they were present at the time of the last universal common ancestor.
doi_str_mv 10.1093/molbev/msab010
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subjects Amyloid - metabolism
Analysis
Archaea - genetics
Archaeal Proteins - genetics
Archaeal Proteins - metabolism
Discoveries
Epigenesis, Genetic
Epigenetic inheritance
Evolution
Genetics
Glycoproteins
Peptides
Phenylalanine
Phylogeny
Prions
Protein Domains
Proteome
Tyrosine
title The Hunt for Ancient Prions: Archaeal Prion-Like Domains Form Amyloid-Based Epigenetic Elements
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