Ribosomal Protein Cluster Organization in Asgard Archaea - PubMed (original) (raw)

Ribosomal Protein Cluster Organization in Asgard Archaea

Madhan R Tirumalai et al. Archaea. 2023.

Abstract

It has been proposed that the superphylum of Asgard Archaea may represent a historical link between the Archaea and Eukarya. Following the discovery of the Archaea, it was soon appreciated that archaeal ribosomes were more similar to those of Eukarya rather than Bacteria. Coupled with other eukaryotic-like features, it has been suggested that the Asgard Archaea may be directly linked to eukaryotes. However, the genomes of Bacteria and non-Asgard Archaea generally organize ribosome-related genes into clusters that likely function as operons. In contrast, eukaryotes typically do not employ an operon strategy. To gain further insight into conservation of the r-protein genes, the genome order of conserved ribosomal protein (r-protein) coding genes was identified in 17 Asgard genomes (thirteen complete genomes and four genomes with less than 20 contigs) and compared with those found previously in non-Asgard archaeal and bacterial genomes. A universal core of two clusters of 14 and 4 cooccurring r-proteins, respectively, was identified in both the Asgard and non-Asgard Archaea. The equivalent genes in the E. coli version of the cluster are found in the S10 and spc operons. The large cluster of 14 r-protein genes (uS19-uL22-uS3-uL29-uS17 from the S10 operon and uL14-uL24-uL5-uS14-uS8-uL6-uL18-uS5-uL30-uL15 from the spc operon) occurs as a complete set in the genomes of thirteen Asgard genomes (five Lokiarchaeotes, three Heimdallarchaeotes, one Odinarchaeote, and four Thorarchaeotes). Four less conserved clusters with partial bacterial equivalents were found in the Asgard. These were the L30e (str operon in Bacteria) cluster, the L18e (alpha operon in Bacteria) cluster, the S24e-S27ae-rpoE1 cluster, and the L31e, L12..L1 cluster. Finally, a new cluster referred to as L7ae was identified. In many cases, r-protein gene clusters/operons are less conserved in their organization in the Asgard group than in other Archaea. If this is generally true for nonribosomal gene clusters, the results may have implications for the history of genome organization. In particular, there may have been an early transition to or from the operon approach to genome organization. Other nonribosomal cellular features may support different relationships. For this reason, it may be important to consider ribosome features separately.

Copyright © 2023 Madhan R. Tirumalai et al.

PubMed Disclaimer

Conflict of interest statement

All authors declare they have no competing interests. LAK and ELS were student volunteers on this work. LAK was a fresh graduate from Clements High School, and ELS had just completed his 10th grade at Obra D. Tompkins High School, who volunteered with the group of Dr. George E. Fox at the University of Houston.

Figures

Figure 1

Figure 1

(a) _Ψ_The orientation of all the genes in the entire cluster flipped for aligning with the other genomes. Each arrow represents a different location on a single complete scaffold; adjacent arrows do not indicate their order on the genome; genes within an arrow are contiguous. ¶Pseudogene; red diamond and red rectangle represent gene(s) absent in the corresponding genome/location; arrows within dashed red boxes are contiguous; HP: hypothetical protein; RNP1: ribonuclease P protein component 1; ORF: open reading frame/gene; #ORF(s) annotated as HP(s); Hsp20: heat shock protein 20; _ß_partial gene. (b) _Ψ_The orientation of all the genes in the entire cluster flipped for aligning with the other genomes. In Thorarchaeota and Heimdallarchaeota, each colored (blue, green, or red) box represents a different contig; adjacent arrows do not indicate their order on the genome unless they are within a dashed red box; genes within an arrow are contiguous. ¶Pseudogene; red diamond represents gene(s) absent in the corresponding genome/location; arrows within dashed red boxes are contiguous; HP: hypothetical protein; RNP1: ribonuclease P protein component 1; ORF: open reading frame/gene; #ORF(s) annotated as HP(s); Hsp20: heat shock protein 20; _ß_partial gene; IF Sui: protein translation factor SUI1 homolog; NCG: noncluster genes.

Figure 2

Figure 2

(a) _Ψ_The orientation of all the genes in the entire cluster flipped for aligning with the other genomes. Each arrow represents a different location on the single complete scaffold/genome; adjacent arrows do not indicate their order on the genome; arrows within dashed red boxes are contiguous; genes within an arrow are contiguous; red diamond represents gene(s) absent in the corresponding genome/location. ybaC: proline iminopeptidase; HP: hypothetical protein; #ORF(s) annotated as HP(s); gene in yellow color occurs outside the main cluster in that genome; _β_partial gene; _α_duplicate copies of the gene adjacent to each other. (b) _Ψ_The orientation of all the genes in the entire cluster flipped for aligning with the other genomes. Adjacent arrows do not indicate their order on the genome; arrows within dashed red boxes are contiguous; genes within an arrow are contiguous; red diamond and red rectangle represent gene(s) absent in the corresponding genome/location; in Heimdallarchaeote AC18, each colored (blue, green, or red) box represents a different contig; ybaC: proline iminopeptidase; HP: hypothetical protein; #ORF(s) annotated as HP(s); genes in yellow color occur outside the main cluster in that genome; _β_partial gene; _α_duplicate copies of the gene adjacent to each other; ccp: crenarchaeal conserved protein; ubiB: ubiquinone biosynthesis protein coding gene.

Figure 3

Figure 3

(a) _Ψ_The orientation of all the genes in the entire cluster flipped for aligning with the other genomes. Adjacent arrows do not indicate their order on the genome; genes within an arrow are contiguous; red diamond and red rectangle represent gene(s) absent in the corresponding genome/location; arrows within dashed red boxes are contiguous; genes in white color (black background) are not in the order as found in the other genomes; genes in green color occur outside the main cluster in that genome; #ORF(s) annotated as HP(s); ¶pseudogene. (b) _Ψ_The orientation of all the genes in the entire cluster flipped for aligning with the other genomes. Adjacent arrows do not indicate their order on the genome; ^begins a contig; genes within an arrow are contiguous; red diamond and red rectangle represent gene(s) absent in the corresponding genome/location; arrows within dashed red boxes are contiguous; in Thorarchaeote BC and Heimdallarchaeotes AC18 and SZ_4_bin2.246, each colored (blue, green, or red) box represents a different contig; genes in white color (black background) are not in the order as found in the other genomes; ¶pseudogene; genes in green color occur outside the main cluster in that genome; #ORF(s) annotated as HP(s).

Figure 4

Figure 4

(a) S24e-S27ae-rpoE1 cluster. _Ψ_The orientation of all the genes in the entire cluster flipped for aligning with the other genomes. Adjacent arrows do not indicate their order on the genome except when they are boxed inside dashed red boxes; genes within an arrow are contiguous; red diamond and red rectangle represent gene(s) absent in corresponding genome/location; arrows within dashed red boxes are contiguous. HP: hypothetical protein; pNP: noncanonical purine NTP pyrophosphatase; InfB: translation initiation factor IF-2; ndk: nucleoside diphosphate kinase; Utp24: 30S proteasome protein; #ORF(s) annotated as HP(s); gcp: bifunctional tRNA threonylcarbamoyladenosine biosynthesis protein; fni-ipk-mvk: archaeal lipid pathway genes; _ß_partial gene. (b) S24e-S27ae-rpoE1 cluster. _Ψ_The orientation of all the genes in the entire cluster flipped for aligning with the other genomes. Adjacent arrows do not indicate their order on the genome except when they are boxed inside dashed red boxes; genes within an arrow are contiguous; red diamond and red rectangle represent gene(s) absent in corresponding genome/location; arrows within dashed red boxes are contiguous; in Heimdallarchaeotes AC18 and SZ_4_bin2.246, each colored (blue, green, or red) box represents a different contig. HP: hypothetical protein; pNP: noncanonical purine NTP pyrophosphatase; InfB: translation initiation factor IF-2; ndk: nucleoside diphosphate kinase; Utp24: 30S proteasome protein; #ORF(s) annotated as HP(s); gcp: bifunctional tRNA threonylcarbamoyladenosine biosynthesis protein; fni-ipk-mvk: archaeal lipid pathway genes.

Figure 5

Figure 5

(a) L31e and L12-L10-L11-L1 cluster. _Ψ_The orientation of all the genes in the entire cluster flipped for aligning with the other genomes. Adjacent arrows do not indicate their order on the genome except when they are boxed inside dashed red boxes; genes within an arrow are contiguous; red diamond represents gene(s) absent in the corresponding genome/location; arrows within dashed red boxes are contiguous; genes/ORFs not colored are not the usual components of this cluster. TP: trimeric intracellular cation-selective channel proteinellular cation-selective channel protein; HP: hypothetical protein; ∗gene begins or terminates a contig; RNP: ribonuclease P protein component 4; RBP: RNA binding protein; nep1: ribosomal RNA small subunit methyltransferase gene; #ORF(s) annotated as HP(s); TR: transcriptional regulator; genes in yellow color occur outside the core/cluster. (b) L31e and L12-L10-L11-L1 cluster. _Ψ_The orientation of all the genes in the entire cluster flipped for aligning with the other genomes. Adjacent arrows do not indicate their order on the genome except when they are boxed inside dashed red boxes; genes within an arrow are contiguous; red diamond represents gene(s) absent in the corresponding genome/location; arrows within dashed red boxes are contiguous; genes/ORFs not colored are not the usual components of this cluster; in the two Heimdallarchaeotes, each colored (blue, green, or red) box represents a different contig. TP: trimeric intracellular cation-selective channel protein; HP: hypothetical protein; ∗genes begins or terminates a contig; RNP: ribonuclease P protein component 4; RBP: RNA binding protein; nep1: ribosomal RNA small subunit methyltransferase gene; #ORF(s) annotated as HP(s); genes in white (black background) are part of the big S10-spc cluster, but occurring with the secE-spt5-L11 segment in the Thaumarchaeote N. aquarius AQ6f; TR: transcriptional regulator; genes in yellow color occur outside the core/cluster.

Similar articles

Cited by

References

    1. Woese C. R., Fox G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proceedings of the National Academy of Sciences . 1977;74(11):5088–5090. doi: 10.1073/pnas.74.11.5088. - DOI - PMC - PubMed
    1. Baker B. J., De Anda V., Seitz K. W., Dombrowski N., Santoro A. E., Lloyd K. G. Diversity, ecology and evolution of Archaea. Nature Microbiology . 2020;5(7):887–900. doi: 10.1038/s41564-020-0715-z. - DOI - PubMed
    1. Forterre P. Archaea. Methods in Molecular Biology, vol 2522 . New York, NY: Humana; 2022. Archaea: a goldmine for molecular biologists and evolutionists; pp. 1–21. - DOI - PubMed
    1. Medina-Chávez N. O., Travisano M. Archaeal communities: the microbial phylogenomic frontier. Frontiers in Genetics . 2022;12 doi: 10.3389/fgene.2021.693193. - DOI - PMC - PubMed
    1. Castelle C. J., Banfield J. F. Major new microbial groups expand diversity and alter our understanding of the tree of life. Cell . 2018;172(6):1181–1197. doi: 10.1016/j.cell.2018.02.016. - DOI - PubMed

Publication types

MeSH terms

Substances

LinkOut - more resources