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 |
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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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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.</description><identifier>ISSN: 1537-1719</identifier><identifier>ISSN: 0737-4038</identifier><identifier>EISSN: 1537-1719</identifier><identifier>DOI: 10.1093/molbev/msab010</identifier><identifier>PMID: 33480998</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>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</subject><ispartof>Molecular biology and evolution, 2021-05, Vol.38 (5), p.2088-2103</ispartof><rights>Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution 2021. 2021</rights><rights>Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution 2021.</rights><rights>COPYRIGHT 2021 Oxford University Press</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c491t-25f5adf59904f4034e0e13786517fe7d79b70a46e8f85018a56e7648c1a208fd3</citedby><cites>FETCH-LOGICAL-c491t-25f5adf59904f4034e0e13786517fe7d79b70a46e8f85018a56e7648c1a208fd3</cites><orcidid>0000-0001-9433-6071</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8480180/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8480180/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,864,885,1604,27923,27924,53790,53792</link.rule.ids><linktorsrc>$$Uhttps://dx.doi.org/10.1093/molbev/msab010$$EView_record_in_Oxford_University_Press$$FView_record_in_$$GOxford_University_Press</linktorsrc><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33480998$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Pupko, Tal</contributor><creatorcontrib>Zajkowski, Tomasz</creatorcontrib><creatorcontrib>Lee, Michael D</creatorcontrib><creatorcontrib>Mondal, Shamba S</creatorcontrib><creatorcontrib>Carbajal, Amanda</creatorcontrib><creatorcontrib>Dec, Robert</creatorcontrib><creatorcontrib>Brennock, Patrick D</creatorcontrib><creatorcontrib>Piast, Radoslaw W</creatorcontrib><creatorcontrib>Snyder, Jessica E</creatorcontrib><creatorcontrib>Bense, Nicholas B</creatorcontrib><creatorcontrib>Dzwolak, Wojciech</creatorcontrib><creatorcontrib>Jarosz, Daniel F</creatorcontrib><creatorcontrib>Rothschild, Lynn J</creatorcontrib><title>The Hunt for Ancient Prions: Archaeal Prion-Like Domains Form Amyloid-Based Epigenetic Elements</title><title>Molecular biology and evolution</title><addtitle>Mol Biol Evol</addtitle><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.</description><subject>Amyloid - metabolism</subject><subject>Analysis</subject><subject>Archaea - genetics</subject><subject>Archaeal Proteins - genetics</subject><subject>Archaeal Proteins - metabolism</subject><subject>Discoveries</subject><subject>Epigenesis, Genetic</subject><subject>Epigenetic inheritance</subject><subject>Evolution</subject><subject>Genetics</subject><subject>Glycoproteins</subject><subject>Peptides</subject><subject>Phenylalanine</subject><subject>Phylogeny</subject><subject>Prions</subject><subject>Protein Domains</subject><subject>Proteome</subject><subject>Tyrosine</subject><issn>1537-1719</issn><issn>0737-4038</issn><issn>1537-1719</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1rFDEYh4NY7IdePcqAFz1Mm0wyk4wHYWy3rbBgD-05ZDNvdqP5WJOdQv97U2YtFQqSQ17ePHny8UPoPcGnBPf0zEe3gvszn9UKE_wKHZGW8ppw0r9-Vh-i45x_YkwY67o36JBSJnDfiyMkbzdQXU9hV5mYqiFoC6W-STaG_KUakt4oUG5u1Ev7C6qL6JUNubqMyVeDf3DRjvU3lWGsFlu7hgA7q6uFA19M-S06MMpleLefT9Dd5eL2_Lpe_rj6fj4sa816squb1rRqNG3fY2YYpgwwEMpF1xJugI-8X3GsWAfCiBYTodoOeMeEJqrBwoz0BH2dvdtp5WHU5eyknNwm61V6kFFZ-e9KsBu5jvdSlJ8gAhfBp70gxd8T5J30NmtwTgWIU5ZN4RreUNwW9OOMrpUDaYOJxagfcTlwzkTXY8oLdfoCVcYI3uoYwNjSf2mDTjHnBObp9gTLx7DlHLbch102fHj-5if8b7oF-DwDcdr-T_YHer-0zA</recordid><startdate>20210501</startdate><enddate>20210501</enddate><creator>Zajkowski, Tomasz</creator><creator>Lee, Michael D</creator><creator>Mondal, Shamba S</creator><creator>Carbajal, Amanda</creator><creator>Dec, Robert</creator><creator>Brennock, Patrick D</creator><creator>Piast, Radoslaw W</creator><creator>Snyder, Jessica E</creator><creator>Bense, Nicholas B</creator><creator>Dzwolak, Wojciech</creator><creator>Jarosz, Daniel F</creator><creator>Rothschild, Lynn J</creator><general>Oxford University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9433-6071</orcidid></search><sort><creationdate>20210501</creationdate><title>The Hunt for Ancient Prions: Archaeal Prion-Like Domains Form Amyloid-Based Epigenetic Elements</title><author>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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c491t-25f5adf59904f4034e0e13786517fe7d79b70a46e8f85018a56e7648c1a208fd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Amyloid - metabolism</topic><topic>Analysis</topic><topic>Archaea - genetics</topic><topic>Archaeal Proteins - genetics</topic><topic>Archaeal Proteins - metabolism</topic><topic>Discoveries</topic><topic>Epigenesis, Genetic</topic><topic>Epigenetic inheritance</topic><topic>Evolution</topic><topic>Genetics</topic><topic>Glycoproteins</topic><topic>Peptides</topic><topic>Phenylalanine</topic><topic>Phylogeny</topic><topic>Prions</topic><topic>Protein Domains</topic><topic>Proteome</topic><topic>Tyrosine</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zajkowski, Tomasz</creatorcontrib><creatorcontrib>Lee, Michael D</creatorcontrib><creatorcontrib>Mondal, Shamba S</creatorcontrib><creatorcontrib>Carbajal, Amanda</creatorcontrib><creatorcontrib>Dec, Robert</creatorcontrib><creatorcontrib>Brennock, Patrick D</creatorcontrib><creatorcontrib>Piast, Radoslaw W</creatorcontrib><creatorcontrib>Snyder, Jessica E</creatorcontrib><creatorcontrib>Bense, Nicholas B</creatorcontrib><creatorcontrib>Dzwolak, Wojciech</creatorcontrib><creatorcontrib>Jarosz, Daniel F</creatorcontrib><creatorcontrib>Rothschild, Lynn J</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular biology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext_linktorsrc</fulltext></delivery><addata><au>Zajkowski, Tomasz</au><au>Lee, Michael D</au><au>Mondal, Shamba S</au><au>Carbajal, Amanda</au><au>Dec, Robert</au><au>Brennock, Patrick D</au><au>Piast, Radoslaw W</au><au>Snyder, Jessica E</au><au>Bense, Nicholas B</au><au>Dzwolak, Wojciech</au><au>Jarosz, Daniel F</au><au>Rothschild, Lynn J</au><au>Pupko, Tal</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Hunt for Ancient Prions: Archaeal Prion-Like Domains Form Amyloid-Based Epigenetic Elements</atitle><jtitle>Molecular biology and evolution</jtitle><addtitle>Mol Biol Evol</addtitle><date>2021-05-01</date><risdate>2021</risdate><volume>38</volume><issue>5</issue><spage>2088</spage><epage>2103</epage><pages>2088-2103</pages><issn>1537-1719</issn><issn>0737-4038</issn><eissn>1537-1719</eissn><abstract>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.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>33480998</pmid><doi>10.1093/molbev/msab010</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0001-9433-6071</orcidid><oa>free_for_read</oa></addata></record> |
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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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