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

In prebiotic evolution, molecular self-replicators are considered to develop into diverse, complex living organisms. The appearance of parasitic replicators is believed inevitable in this process. However, the role of parasitic replicators in prebiotic evolution remains elusive. Here, we demonstrated experimental coevolution of RNA self-replicators (host RNAs) and emerging parasitic replicators (parasitic RNAs) using an RNA-protein replication system we developed. During a long-term replication experiment, a clonal population of the host RNA turned into an evolving host-parasite ecosystem through the continuous emergence of new types of host and parasitic RNAs produced by replication errors. The host and parasitic RNAs diversified into at least two and three different lineages, respectively, and they exhibited evolutionary arms-race dynamics. The parasitic RNA accumulated unique mutations, thus adding a new genetic variation to the whole replicator ensemble. These results provide the first experimental evidence that the coevolutionary interplay between host-parasite molecules plays a key role in generating diversity and complexity in prebiotic molecular evolution.

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

10.1101/728659 ◽

2019 ◽

Cited By ~ 2

Author(s):

Taro Furubayashi ◽

Kensuke Ueda ◽

Yohsuke Bansho ◽

Daisuke Motooka ◽

Shota Nakamura ◽

...

Keyword(s):

Darwinian Evolution ◽

Prebiotic Evolution ◽

Clonal Population ◽

Replication Errors ◽

Replication Experiment ◽

Living Organisms ◽

Host Parasite ◽

First Time

AbstractIn the prebiotic evolution, molecular self-replicators are considered to develop into diverse, complex living organisms. The appearance of parasitic replicators is believed inevitable in this process. However, the role of parasitic replicators on prebiotic evolution remains elusive. Here, we demonstrated experimental coevolution of RNA self-replicators (host RNAs) and emerging parasitic replicators (parasitic RNAs) for the first time by using an RNA-protein replication system we had developed. During a long-term replication experiment, a clonal population of the host RNA turned into an evolving host-parasite ecosystem through the continuous emergence of new types of host and parasitic RNAs produced by replication errors. The diversified host and parasitic RNAs exhibited evolutionary arms-race dynamics. The parasitic RNA accumulated unique mutations that the host RNA had never acquired, thus adding a new genetic variation to the whole replicator ensemble. These results provide the first experimental evidence that the coevolutionary interplay between host-parasite molecules play a key role in generating diversity and complexity in prebiotic molecular evolution.

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Long-term genomic coevolution of host-parasite interaction in the natural environment

10.1101/101576 ◽

2017 ◽

Author(s):

Elina Laanto ◽

Ville Hoikkala ◽

Janne Ravantti ◽

Lotta-Riina Sundberg

Keyword(s):

Host Resistance ◽

Bacterial Resistance ◽

Arms Race ◽

Time Shift ◽

Phenotypic Characterization ◽

Relative Role ◽

Bacterial Host ◽

Host Parasite

AbstractThe antagonistic coevolution of parasite infectivity and host resistance alters the biological functionality of species, with effects spanning to communities and ecosystems. Still, studies describing long-term host-parasite coevolutionary dynamics in nature are largely missing. Furthermore, the role of host resistance mechanisms for parasite evolution is poorly understood, necessitating for the molecular and phenotypic characterization of both coevolving parasites and their hosts. We combined long-term field sampling (2007-2014), in vitro cross-infections and time-shift experiments with bacteriophage whole genome sequencing and bacterial (Flavobacterium columnare) CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats) profiling to show the molecular details of the phage-bacterium arms race in the environment. Bacteria were generally resistant to phages from the past and susceptible to phages in the future. The bacterial resistance selected for increased phage infectivity and host range, correlating directly with the expansion of phage genome size by 2656 bp. In the bacterial host, two CRISPR loci were identified: a type II-C locus and an RNA-targeting type VI-B locus. While maintaining a core set of conserved spacers, phage-matching spacers appeared in the variable end of both CRISPR loci over time. The appearance of these CRISPR spacers in the bacterial host often corresponded with arms race -manner molecular changes in the protospacers of the coevolving phage population. However, the phenotypic data indicated that the relative role of constitutive defence may be more important in high phage pressure, highlighting the importance of our findings for understanding microbial community ecology and in the development of phage therapy applications.

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Evolutionary transition from a single RNA replicator to a multiple replicator network

10.1101/2021.09.09.459571 ◽

2021 ◽

Author(s):

Ryo Mizuuchi ◽

Taro Furubayashi ◽

Norikazu Ichihashi

Keyword(s):

Long Term Evolution ◽

Darwinian Evolution ◽

Living Systems ◽

Prebiotic Evolution ◽

Evolutionary Transition ◽

Term Evolution ◽

Final Population ◽

Diverse Interactions ◽

Emergence Of Life

AbstractIn prebiotic evolution, self-replicating molecules are believed to have evolved into complex living systems by expanding their information and functions open-endedly. Theoretically, such evolutionary complexification could occur through successive appearance of novel replicators that interact with one another to form replication networks. Here we performed long-term evolution experiments using an RNA that replicates by a self-encoded RNA replicase. The RNA diversified into multiple coexisting host and parasite lineages, whose frequencies in the population initially fluctuated and gradually stabilized. The final population, comprising five RNA lineages, forms a replicator network with diverse interactions, including cooperation to help the replication of all other members. These results support the capability of molecular replicators to spontaneously develop complexity through Darwinian evolution, a critical step for the emergence of life.

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Living with Two Genomes: Grafting and Its Implications for Plant Genome-to-Genome Interactions, Phenotypic Variation, and Evolution

Annual Review of Genetics ◽

10.1146/annurev-genet-112618-043545 ◽

2019 ◽

Vol 53 (1) ◽

pp. 195-215 ◽

Cited By ~ 7

Author(s):

Brandon S. Gaut ◽

Allison J. Miller ◽

Danelle K. Seymour

Keyword(s):

Host Resistance ◽

Arms Race ◽

Plant Genome ◽

Long Term Effects ◽

Evolutionary Innovation ◽

Host Parasite Interactions ◽

Artificial Grafts ◽

Genome Interactions ◽

Host Parasite

Plant genomes interact when genetically distinct individuals join, or are joined, together. Individuals can fuse in three contexts: artificial grafts, natural grafts, and host–parasite interactions. Artificial grafts have been studied for decades and are important platforms for studying the movement of RNA, DNA, and protein. Yet several mysteries about artificial grafts remain, including the factors that contribute to graft incompatibility, the prevalence of genetic and epigenetic modifications caused by exchanges between graft partners, and the long-term effects of these modifications on phenotype. Host–parasite interactions also lead to the exchange of materials, and RNA exchange actively contributes to an ongoing arms race between parasite virulence and host resistance. Little is known about natural grafts except that they can be frequent and may provide opportunities for evolutionary innovation through genome exchange. In this review, we survey our current understanding about these three mechanisms of contact, the genomic interactions that result, and the potential evolutionary implications.

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A symbiotic aphid selfishly manipulates attending ants via dopamine in honeydew

Scientific Reports ◽

10.1038/s41598-021-97666-w ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Tatsumi Kudo ◽

Hitoshi Aonuma ◽

Eisuke Hasegawa

Keyword(s):

Reproductive Rate ◽

Arms Race ◽

Maintenance Cost ◽

High Quality ◽

Symbiotic Relationships ◽

Host Parasite ◽

To Receive ◽

Aphid Honeydew ◽

Ant Aggressiveness

AbstractSymbiotic relationships are widespread in nature, but the mechanisms maintaining these relationships remain to be elucidated because symbiosis incurs a maintenance cost to each participant, which lowers its reproductive rate. In host-parasite relationships, parasites are known to manipulate the host's behavior selfishly, and there is an arms race between them. Selfish manipulations also occur in symbiosis, but the effects of selfish manipulations on symbiosis are not fully understood. Here, we show that an ant-associated aphid manipulates attending ants to receive stronger protection. Aphid honeydew regurgitated by ants contains dopamine (DA). The ants showed low aggressiveness before contact with the aphids, but it rose after contact. Administration of DA to the ants increased ant aggressiveness as the concentration increased, while an antagonist of DA inhibited this effect. The other 3 amines showed no effect on aggressiveness. A previous study showed that attending ants selfishly manipulate aphids by increasing the reproductive rate of green morph to obtain high-quality honeydew. These results suggest that mutual selfish manipulation benefits both participants and is likely to strengthen symbiosis. The selfishness of each participant may contribute to sustaining this symbiosis because their selfishness increases their long-term fitness.

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Nutrient stoichiometry shapes microbial coevolution

10.1101/183657 ◽

2017 ◽

Author(s):

Megan L. Larsen ◽

Steven W. Wilhelm ◽

Jay T. Lennon

Keyword(s):

Arms Race ◽

Lytic Phage ◽

Nutrient Stoichiometry ◽

P Limitation ◽

Host Parasite Interactions ◽

Negative Frequency Dependent Selection ◽

Selection For ◽

The Stability ◽

Host Parasite

ABSTRACTCoevolution is a force contributing to the generation and maintenance of biodiversity. It is influenced by environmental conditions including the scarcity of essential resources, which can drive the evolution of defense and virulence traits. We conducted a long-term chemostat experiment where the marine cyanobacterium Synechococcus was challenged with a lytic phage under nitrogen (N) or phosphorus (P) limitation. This manipulation of nutrient stoichiometry altered the stability of host-parasite interactions and the underlying mode of coevolution. By assessing infectivity with >18,000 pairwise challenges, we documented directional selection for increased phage resistance, consistent with arms-race dynamics while phage infectivity fluctuated through time, as expected when coevolution is driven by negative frequency-dependent selection. The resulting infection networks were 50 % less modular under N-versus P-limitation reflecting host-range contraction and asymmetric coevolutionary trajectories. Nutrient stoichiometry affects eco-evolutionary feedbacks in ways that may alter the dynamics and functioning of environmental and host-associated microbial communities.

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