The Evolutionary History of the Structure of 5S Ribosomal RNA

Sun, Feng; Caetano‐Anollés, Gustavo

doi:10.1007/s00239-009-9264-z

Cited by 50 publications

(55 citation statements)

References 87 publications

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“…Thus, the functional RNase P complex, originally thought a remnant of the ancient RNA world [Altman, 2009], appears to be a relatively recent evolving RNP ensemble. These results are noteworthy and are in line with an analysis of 5S rRNA and associated r-proteins that showed the existence of tight coevolution between proteins and nucleic acids in this small regulatory component of the ribosome [Sun and Caetano-Anollés, 2009]. …”

Section: Structural Phylogenomics Reveals a Coevolving World Of Protesupporting

confidence: 70%

“…Phylogenomic analyses also unfold the gradual evolutionary appearance of protein domains that are present in the viral and cellular world [Caetano-Anollés and Caetano-Anollés, 2003;Nasir et al, 2012]. Timelines of accretion of RNA structures [Caetano-Anollés, 2002] and protein domains were recently linked, showing tight coevolution between rRNA and r-proteins and an origin of the ensemble in ribosomal mechanics [Harish and CaetanoAnollés, 2012;Sun and Caetano-Anollés, 2009]. The evolutionary expansion of ribosomal structure by gradual accretion of both RNA helical structures and r-proteins is again incompatible with the RNA world-inspired hypothesis that the ribosome originated in the absence of proteins as a stand-alone biosynthetic ribozyme.…”

Section: The Rna World Hypothesis and Its Modern Contendersmentioning

confidence: 99%

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The Coevolutionary Roots of Biochemistry and Cellular Organization Challenge the RNA World Paradigm

Caetano‐Anollés¹,

Seufferheld²

2013

Microb Physiol

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The origin and evolution of modern biochemistry and cellular structure is a complex problem that has puzzled scientists for almost a century. While comparative, functional and structural genomics has unraveled considerable complexity at the molecular level, there is very little understanding of the origin, evolution and structure of the molecules responsible for cellular or viral features in life. Recent efforts, however, have dissected the emergence of the very early molecules that populated primordial cells. Deep historical signal was retrieved from a census of molecular structures and functions in thousands of nucleic acid and protein structures and hundreds of genomes using powerful phylogenomic methods. Together with structural, chemical and cell biology considerations, this information reveals that modern biochemistry is the result of the gradual evolutionary appearance and accretion of molecular parts and molecules. These patterns comply with the principle of continuity and lead to molecular and cellular complexity. Here, we review findings and report possible origins of molecular and cellular structure, the early rise of lipid biosynthetic pathways and components of cytoskeletal microstructures, the piecemeal accumulation of domains in ATP synthase complexes and the origin and evolution of the ribosome. Phylogenomic studies suggest the last universal common ancestor of life, the ‘urancestor', had already developed complex cellular structure and bioenergetics. Remarkably, our findings falsify the existence of an ancient RNA world. Instead they are compatible with gradually coevolving nucleic acids and proteins in interaction with increasingly complex cofactors, lipid membrane structures and other cellular components. This changes the perception we have of the rise of modern biochemistry and prompts further analysis of the emergence of biological complexity in an ever-expanding coevolving world of macromolecules.

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Section: Structural Phylogenomics Reveals a Coevolving World Of Protesupporting

confidence: 70%

Section: The Rna World Hypothesis and Its Modern Contendersmentioning

confidence: 99%

The Coevolutionary Roots of Biochemistry and Cellular Organization Challenge the RNA World Paradigm

Caetano‐Anollés¹,

Seufferheld²

2013

Microb Physiol

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“…3B) with exceptions in some positions due to SNP's. This lower accuracy in the 5S rRNA secondary structure prediction with respect to other RNA molecules has been reported previously 56 (and references therein). This could be due to possible interactions that are needed for the proper folding of the 5S rRNA.…”

Section: Evolutionsupporting

confidence: 50%

Molecular organization of the 5S rDNA gene type II in elasmobranchs

et al. 2015

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The 5S rDNA gene is a non-coding RNA that can be found in 2 copies (type I and type II) in bony and cartilaginous fish. Previous studies have pointed out that type II gene is a paralog derived from type I. We analyzed the molecular organization of 5S rDNA type II in elasmobranchs. Although the structure of the 5S rDNA is supposed to be highly conserved, our results show that the secondary structure in this group possesses some variability and is different than the consensus secondary structure. One of these differences in Selachii is an internal loop at nucleotides 7 and 112. These mutations observed in the transcribed region suggest an independent origin of the gene among Batoids and Selachii. All promoters were highly conserved with the exception of BoxA, possibly due to its affinity to polymerase III. This latter enzyme recognizes a dT 4 sequence as stop signal, however in Rajiformes this signal was doubled in length to dT 8. This could be an adaptation toward a higher efficiency in the termination process. Our results suggest that there is no TATA box in elasmobranchs in the NTS region. We also provide some evidence suggesting that the complexity of the microsatellites present in the NTS region play an important role in the 5S rRNA gene since it is significantly correlated with the length of the NTS.

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“…We have showcased this progression with proteins but expect nucleic acids will follow a similar progressive trend. In fact, we see the gradual formation of structure unfold for example in phylogenetic analysis of tRNA (Sun and Caetano-Anollés 2008b), RNase P RNA (Sun and Caetano-Anollés 2010), 5S RNA (Sun and Caetano-Anollés 2009), and the small and large subunits of rRNA (Harish and Caetano-Anollés 2011). We also reveal progressive growth in biological information.…”

Section: Discussionmentioning

confidence: 93%

“…A historical account of domain appearance ) matched rings of gene neighbors derived from an analysis of physical clustering of conserved genes in bacterial genomes (Danchin et al 2007). Furthermore, we have shown that the age of domains in ribosomal proteins coevolves tightly with the age of rRNA substructures, uncovering recruitment and accretion patterns, and revealing the relatively late molecular origins of the ribosome (Sun and Caetano-Anollés 2009;Harish and CaetanoAnollés 2011). Here, we focus on a historical account of domains defined at FF level and study the emergence of the most ancient molecular functions.…”

Section: Introductionmentioning

confidence: 97%

The Phylogenomic Roots of Modern Biochemistry: Origins of Proteins, Cofactors and Protein Biosynthesis

2012

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The complexity of modern biochemistry developed gradually on early Earth as new molecules and structures populated the emerging cellular systems. Here, we generate a historical account of the gradual discovery of primordial proteins, cofactors, and molecular functions using phylogenomic information in the sequence of 420 genomes. We focus on structural and functional annotations of the 54 most ancient protein domains. We show how primordial functions are linked to folded structures and how their interaction with cofactors expanded the functional repertoire. We also reveal protocell membranes played a crucial role in early protein evolution and show translation started with RNA and thioester cofactor-mediated aminoacylation. Our findings allow elaboration of an evolutionary model of early biochemistry that is firmly grounded in phylogenomic information and biochemical, biophysical, and structural knowledge. The model describes how primordial α-helical bundles stabilized membranes, how these were decorated by layered arrangements of β-sheets and α-helices, and how these arrangements became globular. Ancient forms of aminoacyl-tRNA synthetase (aaRS) catalytic domains and ancient non-ribosomal protein synthetase (NRPS) modules gave rise to primordial protein synthesis and the ability to generate a code for specificity in their active sites. These structures diversified producing cofactor-binding molecular switches and barrel structures. Accretion of domains and molecules gave rise to modern aaRSs, NRPS, and ribosomal ensembles, first organized around novel emerging cofactors (tRNA and carrier proteins) and then more complex cofactor structures (rRNA). The model explains how the generation of protein structures acted as scaffold for nucleic acids and resulted in crystallization of modern translation.

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The Evolutionary History of the Structure of 5S Ribosomal RNA

Cited by 50 publications

References 87 publications

The Coevolutionary Roots of Biochemistry and Cellular Organization Challenge the RNA World Paradigm

The Coevolutionary Roots of Biochemistry and Cellular Organization Challenge the RNA World Paradigm

Molecular organization of the 5S rDNA gene type II in elasmobranchs

The Phylogenomic Roots of Modern Biochemistry: Origins of Proteins, Cofactors and Protein Biosynthesis

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