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.2023 Feb 2:14:1075071.
doi: 10.3389/fmicb.2023.1075071. eCollection 2023.

Ultrastructural and proteomic evidence for the presence of a putative nucleolus in an Archaeon

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Ultrastructural and proteomic evidence for the presence of a putative nucleolus in an Archaeon

Parsifal F Islas-Morales et al. Front Microbiol..

Abstract

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 crenarchaeonSaccharolobus solfataricus (formerly known asSulfolobus 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 ultrastructuralin 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 theS. 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 inS. 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.

Keywords: AgNOR; Archaea; Saccharolobus; TACK; evolution; microscopy; nucleolus; proteomics.

Copyright © 2023 Islas-Morales, Cárdenas, Mosqueira, Jiménez-García and Voolstra.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Light and electron microscopy observations support the presence of putative nucleolus-like domains in the crenarchaeonSaccharolobus solfataricus at the ultrastructural level.(A1) Light microscopy of the AgNOR reaction.(A2) Light microscopy of unstainedS. solfataricus cells (negative control).(B1) Transmission Electron Microscopy (TEM) ofS. solfataricus cells, with(B2) detail of discrete fibro-granular structures.(C1) Ultrastructural AgNOR impregnation of subcellular structures, with(C2) high magnification of AgNOR positive subcellular structures.(D1) UltrastructuralIn situ hybridization (UISH) of 16S and 23S rDNA clusters, with(D2) magnified image showing an underlying electron-dense region.
Figure 2
Figure 2
Transmission electron microscopy of fibro-granular, putative nucleolus-like domains in cells of the crenarchaeonS. solfataricus.(A) Arrows show electron dense regions, present in most cells at low magnification.(B) SingleS. solfataricus cell with an electron dense domain, in which a fibro-granular morphology is evident.(C) SingleS. solfataricus cell at high magnification. Arrows show the electron dense region where granules in the central part and fibers toward the outside can be observed. A differentiation of structural substrate is evident in comparison to the surrounding cytoplasm.
Figure 3
Figure 3
Molecular organization of the putative nucleolus ofS. solfataricus based on ultrastructural, molecular, and genomics evidence. Nucleolar elements identified in theS. solfataricus genome through homology search or by means of protein domain prediction are colored in blue boxes; proteins supported by proteomic evidence from sequencing of AgNOR fractions are highlighted in red.
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