RNA diversification by a self-reproducing ribozyme revealed by deep sequencing and kinetic modelling

Jeancolas, Cyrille; Matsubara, Yoshiya J.; Vybornyi, Mykhailo; Lambert, Camille N.; Blokhuis, Alex; Alline, Thomas; Griffiths, Andrew D.; Ameta, Sandeep; Krishna, Sandeep; Nghe, Philippe

doi:10.1039/d1cc02290c

Cited by 11 publications

(9 citation statements)

References 15 publications

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“…The broad representation of retrozymes in plant genomes is compatible with the origin of viroids via retrozyme escape in plants. Given their limited (currently known) host range, such escape seems to be the most likely scenario for the emergence of viroids, in accord with the prescient early hypothesis of Diener [53]. Conversely, the animal retrozymes potentially might have independently given rise to ribozyviruses, as an alternative to the horizontal transfer of viroids discussed above.…”

Section: Viroids: Ancient Relics or Recently Emerged Parasites?mentioning

confidence: 67%

“…Unlike the standard model of viroid replication, which is based on RCR, with monomers ligating to form antigenomic cccRNAs, the mechanism these replicators used bypasses ligation altogether: instead, the polymerase jumps from the 5′ end of the template back to the 3′ end. Recent research also demonstrates that viroid-like self-complementary cccRNAs are readily formed in autocatalytic RNA reaction networks [53]. These lines of research suggest that replicators with the structural hallmarks of viroids could potentially emerge de novo, at least in the presence of a suitable polymerase.…”

Section: Viroids: Ancient Relics or Recently Emerged Parasites?mentioning

confidence: 95%

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Viroids and Viroid-like Circular RNAs: Do They Descend from Primordial Replicators?

Lee

Koonin

2022

Life

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Viroids are a unique class of plant pathogens that consist of small circular RNA molecules, between 220 and 450 nucleotides in size. Viroids encode no proteins and are the smallest known infectious agents. Viroids replicate via the rolling circle mechanism, producing multimeric intermediates which are cleaved to unit length either by ribozymes formed from both polarities of the viroid genomic RNA or by coopted host RNAses. Many viroid-like small circular RNAs are satellites of plant RNA viruses. Ribozyviruses, represented by human hepatitis delta virus, are larger viroid-like circular RNAs that additionally encode the viral nucleocapsid protein. It has been proposed that viroids are direct descendants of primordial RNA replicons that were present in the hypothetical RNA world. We argue, however, that much later origin of viroids, possibly, from recently discovered mobile genetic elements known as retrozymes, is a far more parsimonious evolutionary scenario. Nevertheless, viroids and viroid-like circular RNAs are minimal replicators that are likely to be close to the theoretical lower limit of replicator size and arguably comprise the paradigm for replicator emergence. Thus, although viroid-like replicators are unlikely to be direct descendants of primordial RNA replicators, the study of the diversity and evolution of these ultimate genetic parasites can yield insights into the earliest stages of the evolution of life.

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Section: Viroids: Ancient Relics or Recently Emerged Parasites?mentioning

confidence: 67%

Section: Viroids: Ancient Relics or Recently Emerged Parasites?mentioning

confidence: 95%

Viroids and Viroid-like Circular RNAs: Do They Descend from Primordial Replicators?

Lee

Koonin

2022

Life

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“…Indeed, the E L ribozyme was able to generate RNA strands of > 500 nt in length, including circular species, and this activity was enhanced in terms of both rate and yield in (Lys) n coacervates. Although the observation of circular products in concatenation reactions has been previously reported in ribozyme systems 46 , the inhibition of this behaviour by coacervation is notable. Whilst the mechanism of this inhibition is unknown, the absence of circular products suggests that the ends of a substrate strand do not meet, hinting at a decrease in RNA mobility, increased chain stiffness or reduced release of ligated substrate from the ribozyme within the condensed phase compared to the bulk solution.…”

Section: Discussionmentioning

confidence: 79%

Ribozyme-phenotype coupling in peptide-based coacervate protocells

Vay

Salibi

Ghosh

et al. 2022

Preprint

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Condensed coacervate phases are now understood to be important features of modern cell biology, as well as valuable protocellular models in origin of life studies and synthetic biology. In each of these fields, the development of model systems with varied and tuneable material properties is of great importance for replicating properties of life. Here, we develop a ligase ribozyme system capable of concatenating short RNA fragments into extremely long chains. Our results show that formation of coacervate microdroplets with the ligase ribozyme and poly(L-lysine) enhances ribozyme rate and yield, which in turn increases the length of the anionic polymer component of the system and imparts specific physical properties to the droplets. Droplets containing active ribozyme sequences resist growth, do not wet or spread on unpassivated surfaces, and exhibit reduced transfer of RNA between droplets when compared to controls containing inactive sequences. These altered behaviours, which stem from RNA sequence and catalytic activity, constitute a specific phenotype and potential fitness advantage, opening the door to selection and evolution experiments based on a genotype – phenotype linkage.

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“…(ii) Each compositional state can be composed of a large number of chemical species. The Azoarcus ribozyme can catalyze not only the formation of itself but also the production of diverse RNA sequences [57]. Here, selfreproducing ribozymes (ACSs) correspond to the 'autocatalytic cores,' and the sequences produced by the ribozyme correspond to their 'peripheries' [25,58,59].…”

Section: Discussionmentioning

confidence: 99%

Robustness of compositional heredity to the growth and division dynamics of prebiotic compartments

Matsubara¹,

Ameta²,

Thutupalli³

et al. 2022

Preprint

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An important transition after the origin of life was the first emergence of a Darwinian population, self-reproducing entities exhibiting differential reproduction, phenotypic variation, and inheritance of phenotypic traits. The simplest system we can imagine to have these properties would consist of a compartmentalized autocatalytic reaction system that exhibits two growth states with different chemical compositions. Identifying the chemical composition as the phenotype, this accounts for two of the properties. However, it is not clear what are the necessary conditions for such a chemical system to exhibit inheritance of the compositional states upon growth and division of the compartment. We show that for a general class of autocatalytic chemical systems subject to serial dilution, the inheritance of compositional information only occurs when the time interval between dilutions is below a critical threshold that depends on the efficiency of the catalytic reactions. Further, we show that these thresholds provide rigorous bounds on the properties required for the inheritance of the chemical compositional state for general growth and division cycles. Our result suggests that a serial dilution experiment, which is much easier to set up in a laboratory, can be used to test whether a given autocatalytic chemical system can exhibit heredity. Lastly, we apply our results to a realistic autocatalytic system based on the Azoarcus ribozyme and suggest a protocol to experimentally test whether this system can exhibit heredity.

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RNA diversification by a self-reproducing ribozyme revealed by deep sequencing and kinetic modelling

Abstract: We demonstrate that a recombinase ribozyme achieves multiple functions in the same reaction network: self-reproduction, iterative elongation and circularization of other RNAs, leading to synthesis of diverse products predicted by...

Cited by 11 publications

References 15 publications

Viroids and Viroid-like Circular RNAs: Do They Descend from Primordial Replicators?

Viroids and Viroid-like Circular RNAs: Do They Descend from Primordial Replicators?

Ribozyme-phenotype coupling in peptide-based coacervate protocells

Robustness of compositional heredity to the growth and division dynamics of prebiotic compartments

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