Ultrastructural and proteomic evidence for the presence of a putative nucleolus in an Archaeon
Nucleoli are subcellular compartments where transcription and maturation of pre-ribosomal RNAs occur. While the transcription of ribosomal RNAs is common to all living cells, the presence and ultrastructure of nucleoli has been only documented in eukaryotes. Asgard-Archaea, the closest prokaryotic r...
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| Format: | Article |
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Frontiers Media S.A.
2023-02-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1075071/full |
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| author | Parsifal F. Islas-Morales Parsifal F. Islas-Morales Parsifal F. Islas-Morales Anny Cárdenas Anny Cárdenas Anny Cárdenas María J. Mosqueira María J. Mosqueira Luis Felipe Jiménez-García Luis Felipe Jiménez-García Christian R. Voolstra Christian R. Voolstra |
| author_facet | Parsifal F. Islas-Morales Parsifal F. Islas-Morales Parsifal F. Islas-Morales Anny Cárdenas Anny Cárdenas Anny Cárdenas María J. Mosqueira María J. Mosqueira Luis Felipe Jiménez-García Luis Felipe Jiménez-García Christian R. Voolstra Christian R. Voolstra |
| author_sort | Parsifal F. Islas-Morales |
| collection | DOAJ |
| description | Nucleoli are subcellular compartments where transcription and maturation of pre-ribosomal RNAs occur. While the transcription of ribosomal RNAs is common to all living cells, the presence and ultrastructure of nucleoli has been only documented in eukaryotes. Asgard-Archaea, the closest prokaryotic relatives of eukaryotes, and their near relatives TACK-Archaea have homologs of nucleolar proteins and RNAs in their genome, but the cellular organization of both is largely unexplored. Here we provide ultrastructural and molecular evidence for the presence of putative nucleolus-like subcellular domains in the TACK crenarchaeon Saccharolobus solfataricus (formerly known as Sulfolobus solfataricus). Transmission electron microscopy (TEM) revealed consistent electron-dense fibro-granular compartments, also positive to the specific silver staining for nucleolar organizer regions (AgNOR). TEM also confirmed that ribosomal DNA (rDNA) is spatially distributed in non-random, clustered arrays underlying fine structures, as observed by ultrastructural in situ hybridization (UISH). To further explore these observations, proteomic sequencing of isolated bands from AgNOR-stained protein gels was conducted and compared against a compiled inventory of putative nucleolar homologs from the S. solfataricus P1 genome. Sequenced AgNOR-sensitive peptides encoded homologs of eukaryotic nucleoli proteins, enriched for nucleolus-related functions. Our results provide first evidence that subcellular domains of nucleolar-like nature are not exclusive to eukaryotes. Based on our data, we propose a model for a putative nucleolus in S. solfataricus. Whereas technical limitations and further aspects remain a matter for future functional studies, our data supports the origin of nucleoli within the common ancestor of Eukarya and TACK-Archaea, based on a two-domain tree of life. |
| first_indexed | 2024-04-10T18:17:04Z |
| format | Article |
| id | doaj.art-8c487b6e47d94a1d9a7f70d49988ea5f |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-10T18:17:04Z |
| publishDate | 2023-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-8c487b6e47d94a1d9a7f70d49988ea5f2023-02-02T08:33:14ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-02-011410.3389/fmicb.2023.10750711075071Ultrastructural and proteomic evidence for the presence of a putative nucleolus in an ArchaeonParsifal F. Islas-Morales0Parsifal F. Islas-Morales1Parsifal F. Islas-Morales2Anny Cárdenas3Anny Cárdenas4Anny Cárdenas5María J. Mosqueira6María J. Mosqueira7Luis Felipe Jiménez-García8Luis Felipe Jiménez-García9Christian R. Voolstra10Christian R. Voolstra11Programa de Doctorado en Ciencias Biomédicas, Facultad de Medicina, UNAM, Mexico City, MexicoUNESCO Chair on Science Diplomacy and Scientific Heritage, Instituto de Biología, UNAM, Mexico City, MexicoRed Sea Research Center (RSRC), Biological, Environmental Sciences, and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaRed Sea Research Center (RSRC), Biological, Environmental Sciences, and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaDepartment of Biology, University of Konstanz, Konstanz, GermanyDepartment of Biology, American University, Washington, DC, United StatesRed Sea Research Center (RSRC), Biological, Environmental Sciences, and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaNEOM, Saudi ArabiaPrograma de Doctorado en Ciencias Biomédicas, Facultad de Medicina, UNAM, Mexico City, MexicoDepartment of Cell Biology, Faculty of Sciences, UNAM, Mexico City, MexicoRed Sea Research Center (RSRC), Biological, Environmental Sciences, and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaDepartment of Biology, University of Konstanz, Konstanz, GermanyNucleoli are subcellular compartments where transcription and maturation of pre-ribosomal RNAs occur. While the transcription of ribosomal RNAs is common to all living cells, the presence and ultrastructure of nucleoli has been only documented in eukaryotes. Asgard-Archaea, the closest prokaryotic relatives of eukaryotes, and their near relatives TACK-Archaea have homologs of nucleolar proteins and RNAs in their genome, but the cellular organization of both is largely unexplored. Here we provide ultrastructural and molecular evidence for the presence of putative nucleolus-like subcellular domains in the TACK crenarchaeon Saccharolobus solfataricus (formerly known as Sulfolobus solfataricus). Transmission electron microscopy (TEM) revealed consistent electron-dense fibro-granular compartments, also positive to the specific silver staining for nucleolar organizer regions (AgNOR). TEM also confirmed that ribosomal DNA (rDNA) is spatially distributed in non-random, clustered arrays underlying fine structures, as observed by ultrastructural in situ hybridization (UISH). To further explore these observations, proteomic sequencing of isolated bands from AgNOR-stained protein gels was conducted and compared against a compiled inventory of putative nucleolar homologs from the S. solfataricus P1 genome. Sequenced AgNOR-sensitive peptides encoded homologs of eukaryotic nucleoli proteins, enriched for nucleolus-related functions. Our results provide first evidence that subcellular domains of nucleolar-like nature are not exclusive to eukaryotes. Based on our data, we propose a model for a putative nucleolus in S. solfataricus. Whereas technical limitations and further aspects remain a matter for future functional studies, our data supports the origin of nucleoli within the common ancestor of Eukarya and TACK-Archaea, based on a two-domain tree of life.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1075071/fullAgNORArchaeanucleolusevolutionproteomicsSaccharolobus |
| spellingShingle | Parsifal F. Islas-Morales Parsifal F. Islas-Morales Parsifal F. Islas-Morales Anny Cárdenas Anny Cárdenas Anny Cárdenas María J. Mosqueira María J. Mosqueira Luis Felipe Jiménez-García Luis Felipe Jiménez-García Christian R. Voolstra Christian R. Voolstra Ultrastructural and proteomic evidence for the presence of a putative nucleolus in an Archaeon Frontiers in Microbiology AgNOR Archaea nucleolus evolution proteomics Saccharolobus |
| title | Ultrastructural and proteomic evidence for the presence of a putative nucleolus in an Archaeon |
| title_full | Ultrastructural and proteomic evidence for the presence of a putative nucleolus in an Archaeon |
| title_fullStr | Ultrastructural and proteomic evidence for the presence of a putative nucleolus in an Archaeon |
| title_full_unstemmed | Ultrastructural and proteomic evidence for the presence of a putative nucleolus in an Archaeon |
| title_short | Ultrastructural and proteomic evidence for the presence of a putative nucleolus in an Archaeon |
| title_sort | ultrastructural and proteomic evidence for the presence of a putative nucleolus in an archaeon |
| topic | AgNOR Archaea nucleolus evolution proteomics Saccharolobus |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1075071/full |
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