Sustainability of a Compartmentalized Host-Parasite Replicator System under Periodic Washout-Mixing Cycles

Furubayashi, Taro; Ichihashi, Norikazu

doi:10.3390/life8010003

Cited by 16 publications

(23 citation statements)

References 33 publications

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“…The emergence of parasitic replicators are believed to be inevitable and crucial in an evolving replicator system [6] as experimentally demonstrated in an artificial RNA replication system we have reported [22]. Theoretical studies have predicted that spatial structures, such as cell-like compartments, can allow survival of host replicators in the presence of parasites [23][24][25][26]. Recent experimental studies using the RNA replication system confirmed this; compartmentalization actually supported the survival of functional RNA replicators in the presence of spontaneously emerging parasitic RNA replicators [27][28][29].…”

Section: Introductionmentioning

confidence: 65%

Emergence and diversification of a host-parasite RNA ecosystem through Darwinian evolution

Furubayashi

Ueda

Bansho

et al. 2019

Preprint

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A crucial problem for primitive replicators before the origin of life is the appearance of parasitic or selfish replicators, which destabilize molecular cooperation and prevent the development of complexity. To date, theoretical and experimental studies have indicated that spatial structures, such as cell-like compartments, support sustainable replication of primitive replicators even in the presence of parasites. However, it is still a mystery how these host and parasitic replicators can evolve when they undergo long-term co-replication. Here, we investigated the coevolutionary process between an artificial RNA replicator (host RNA) and spontaneously appearing parasitic replicator (parasitic RNA) in artificial cell-like compartments. We performed a long-term replication experiment and found that the population dynamics of the host and parasitic RNAs gradually changed and novel types of hosts and parasites continued to appear. Competitive replication assays confirmed that parasite-resistant evolution of the host RNA and counter-adaptive evolution of the parasitic RNA occurred one after another. These results demonstrated that evolutionary arms races occur in this simple molecular system and generate a continuously-evolving molecular ecosystem. This coevolutionary process between host and parasitic molecules might play an important role in the open-ended evolution and development of complexity for primitive self-replication systems. ResultsRNA replication system. The RNA replication system used in this study consists of two types of singlestranded RNAs (host and parasitic RNAs) and a reconstituted translation system of E. coli [31] (Fig.1A). A distinctive feature between the host and parasitic RNAs is the capability of providing an RNA replicase (Qβ replicase). The host RNA provides the catalytic β-subunit of the replicase via translation, which forms active Fig.1 | Host and parasitic RNA replication system. (A) Replication scheme of the host and parasitic RNAs. The host RNA encodes Qβ replicase subunit, while the parasitic RNA does not. Both RNAs are replicated by the translated Qβ replicase in the reconstituted translation system of E. coli. (B) Replication-dilution cycle for a long-term replication experiment. The host RNA is encapsulated in water-in-oil droplets with approximately 2 μm diameter. The parasitic RNA spontaneously appears. (1) The droplets are incubated at 37 °C for 5 h for translation and replication. (2) 80 % of droplets are removed and (3) diluted with new droplets containing the translation system (i.e., 5-fold dilution). (4) Diluted dropletsare vigorously mixed to induce random fusion and division among the droplets. We repeated this cycle for 120 rounds.Reaction volume was 1 mL with 1% aqueous phase, corresponding to approximately 10 8 droplets.

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Section: Introductionmentioning

confidence: 65%

Emergence and diversification of a host-parasite RNA ecosystem through Darwinian evolution

Furubayashi

Ueda

Bansho

et al. 2019

Preprint

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“…However, when a hypercycle is compartmentalized appropriately, the parasitic replicators are isolated from other normal hypercycles, and hypercyclic replication can be sustained . This effect of compartmentalization to suppress parasitic replicators has also been investigated theoretically for other self‐replication systems by Szathmary's and Hogeweg's groups …”

Section: Compartmentalizationmentioning

confidence: 99%

“…[94][95][96] This effect of compartmentalization to suppress parasitic replicators has also been investigated theoretically for other self-replication systems by Szathmary's and Hogeweg's groups. [97][98][99][100][101][102][103] Experimental verification of compartmentalization has been reported. Since 1995, several groups have reported biochemical reactions in microscale compartments, such as lipid-bilayer vesicles (liposomes) or water-in-oil droplets.…”

Section: Compartmentalizationmentioning

confidence: 99%

What can we learn from the construction of in vitro replication systems?

Ichihashi

2019

Annals of the New York Academy of Sciences

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Replication is a central function of living organisms. Several types of replication systems have been constructed in vitro from various molecules, including peptides, DNA, RNA, and proteins. In this review, I summarize the progress in the construction of replication systems over the past few decades and discuss what we can learn from their construction. I introduce various types of replication systems, supporting the feasibility of the spontaneous appearance of replication early in Earth's history. In the latter part of the review, I focus on parasitic replicators, one of the largest obstacles for sustainable replication. Compartmentalization is discussed as a possible solution.

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“…As This class of multilevel selection describes several mechanisms proposed in scenarios for the origins of life, based on various types of compartments (e.g. lipid vesicles [20], pores [21,22], inorganic compartments [23], coacervates [2,4] or aerosols [24]) or various protocols of transient compartmentalization [25,26]. Particularly exciting is the recent experiment that demonstrated the mechanism for the first time, in which small droplets containing RNA in a microfluidic device [17] were used as compartments.…”

Section: Introductionmentioning

confidence: 99%

The generality of transient compartmentalization and its associated error thresholds

Blokhuis

Nghe

Peliti

et al. 2020

Journal of Theoretical Biology

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Can prelife proceed without cell division? A recently proposed mechanism suggests that transient compartmentalization could have preceded cell division in prebiotic scenarios. Here, we study transient compartmentalization dynamics in the presence of mutations and noise in replication, as both can be detrimental the survival of compartments. Our study comprises situations where compartments contain uncoupled autocatalytic reactions feeding on a common resource, and systems based on RNA molecules copied by replicases, following a recent experimental study.

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Sustainability of a Compartmentalized Host-Parasite Replicator System under Periodic Washout-Mixing Cycles

Cited by 16 publications

References 33 publications

Emergence and diversification of a host-parasite RNA ecosystem through Darwinian evolution

Emergence and diversification of a host-parasite RNA ecosystem through Darwinian evolution

What can we learn from the construction of in vitro replication systems?

The generality of transient compartmentalization and its associated error thresholds

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