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Petrone, M. E.

Publications and source records attributed to Petrone, M. E..

6 recordsLinked to original sources

Metagenomic resolution of spotted-fever group Rickettsia tasmanensis and novel DNA viruses in Australian wildlife ticks, with spatial modelling of Rickettsia exposure zones.

Australia's spotted fever group (SFG) rickettsiae cause significant illness, yet microbial diversity in wildlife ticks remains incompletely understood. Metagenomic sequencing of nine tick pools representing three Ixodidae species, Ixodes tasmani, I. holocyclus, and Haemaphysalis bancrofti, from Australian wildlife revealed a genome of a novel SFG Rickettsia species from I. tasmani ticks collected from koalas in New South Wales. Phylogenomic analysis confirmed this as a distinct species closely related to Rickettsia tasmaniensis fragments previously reported from Tasmanian devils. Additionally, we discovered four novel DNA Anellovirus species forming a new genus 'Sintorquevirus' and one Circovirus from likely vertebrate blood meals, revealing wildlife viral diversity. Species distribution modelling of I. tasmani for assessing Rickettsia risk revealed suitable habitat along Australia's eastern coastlines, with overlap between vector distribution, marsupial hosts, and population centres. This identified potential Candidatus R. tasmanensis exposure zones in coastal regions where positive samples originated, highlighting areas for surveillance.

microbiology↗

Tunicate metatranscriptomes reveal ancient virus-host co-divergence and inter-order recombination in the evolutionary history of disease-causing viruses

Tunicates are a key transitional taxon in animal evolution as the closest extant invertebrate relatives of the vertebrates. Their viruses may also reflect this transitional state. Yet, it is not known whether tunicate viruses are more closely related to vertebrate- or invertebrate-infecting viral lineages. We analysed primary and publicly available RNA libraries to extend the known diversity of tunicate-associated viruses and determine their relationship to viruses of other animals. We present evidence that influenza viruses, alphaviruses, and some mononegaviruses emerged prior to the evolution of vertebrates. We also show that the recombination of glycoproteins between different orders of RNA viruses, including between positive- and negative-sense viruses, may have shaped the evolution of multiple lineages. Our study reveals that some disease-causing RNA virus lineages were present in early chordates and highlights that the evolution of structural genes may be incongruent with that of the highly conserved RNA-dependent RNA polymerase.

microbiology↗

A virus associated with the zoonotic pathogen Plasmodium knowlesi causing human malaria is a member of a diverse and unclassified viral taxon

Apicomplexa are single-celled eukaryotes that can infect humans and include the mosquito-borne parasite Plasmodium, the cause of malaria. Increasing rates of drug resistance in human-only Plasmodium species are reducing the efficacy of control efforts and antimalarial treatments. There are also rising cases of P. knowlesi, the only zoonotic Plasmodium species that causes severe disease and death in humans. Thus, there is a need to develop additional innovative strategies to combat malaria. Viruses that infect non-Plasmodium spp. disease-causing protozoa have been shown to affect pathogen life cycle and disease outcomes. However, only one virus (Matryoshka RNA virus 1) has been identified in Plasmodium, and none have been identified in zoonotic Plasmodium species. The rapid expansion of the known RNA virosphere using structure- and artificial intelligence-based methods suggests that this dearth is due to the divergent nature of RNA viruses that infect protozoa. We leveraged these newly uncovered data sets to explore the virome of human-infecting Plasmodium species collected in Sabah, east (Borneo) Malaysia. We identified a highly divergent RNA virus in two human-infecting P. knowlesi isolates that is related to the unclassified group ormycoviruses. By characterising fifteen additional ormycoviruses identified in the transcriptomes of arthropods we show that this group of viruses exhibits a complex ecology at the arthropod-mammal interface. Through the application of artificial intelligence methods, we then demonstrate that the ormycoviruses are part of a diverse and unclassified viral taxon. This is the first observation of an RNA virus in a zoonotic Plasmodium species. By linking small-scale experimental data to large-scale virus discovery advances, we characterise the diversity and genomic architecture of an unclassified viral taxon. This approach should be used to further explore the virome of disease-causing Apicomplexa and better understand how protozoa-infecting viruses may affect parasite fitness, pathobiology, and treatment outcomes.

evolutionary biology↗

A 39.8kb flavi-like virus uses a novel strategy for overcoming the RNA virus error threshold

It is commonly held that there is a fundamental relationship between genome size and error rate, manifest as a notional "error threshold" that sets an upper limit on genome sizes. The genome sizes of RNA viruses, which have intrinsically high mutation rates due to a lack of mechanisms for error correction, must therefore be small to avoid accumulating an excessive number of deleterious mutations that will ultimately lead to population extinction. The proposed exceptions to this evolutionary rule are RNA viruses from the order Nidovirales (such as coronaviruses) that encode an error correcting exonuclease, enabling them to reach genome lengths greater than 40kb. The recent discovery of large genome flavi-like viruses (Flaviviridae), which comprise genomes up to 27kb in length yet seemingly do not encode exonuclease domains, has led to the proposal that a proofreading mechanism is required to facilitate the expansion of RNA virus genomes above 30kb. Herein, we describe a 39.8kb flavi-like virus identified in a Haliclona sponge metatranscriptome that does not encode an exonuclease. Structural analysis revealed that this virus may have instead captured bacterial domains associated with nucleic acid metabolism that have not been previously found in RNA viruses. Phylogenetic analysis placed this virus as a divergent pesti-like lineage, such that we have provisionally termed it Maximus pesti-like virus. This virus represents the first instance of a flavi-like virus achieving a genome size comparable to that of the Nidovirales and demonstrates that RNA viruses have evolved multiple solutions to overcome the error threshold.

evolutionary biology↗

Evidence for an aquatic origin of influenza virus and the order Articulavirales

The emergence of novel disease-causing viruses in mammals is part of the long evolutionary history of viruses. Tracing these evolutionary histories contextualises virus spill over events and may help to elucidate how and why they occur. We used a combination of total RNA sequencing and transcriptome data mining to extend the diversity and evolutionary history of the order Articulavirales, which includes the influenza viruses. From this, we identified the first instance of Articulavirales in the Cnidaria (including corals), constituting a novel and divergent family that we tentatively named the Cnidenomoviridae. This may be the basal group within the Articulavirales. We also extended the known evolutionary history of the influenza virus lineage by identifying a highly divergent, sturgeon-associated influenza virus. This suggests that fish were among the first hosts of influenza viruses. Finally, we substantially expanded the known diversity of quaranjaviruses and proposed that this genus be reclassified as a family (the Quaranjaviridae). We find evidence that vertebrate infecting Quaranjaviridae may have initially evolved in crustaceans before spilling into terrestrial Chelicerata (i.e., ticks). Together, our findings indicate that the Articulavirales has evolved over at least 600 million years, first emerging in aquatic animals. Importantly, the evolution of this order was not shaped by strict virus-host codivergence, but rather by multiple aquatic-terrestrial transitions and substantial host jumps, some of which are still observable today.

evolutionary biology↗

Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians

The Flaviviridae are a family of positive-sense RNA viruses that include well-documented agents of human disease. Despite their importance and ubiquity, the time-scale of flaviviral evolution is uncertain. An ancient origin, spanning time-scales of millions of years, is supported by their presence in both vertebrates and invertebrates and the identification of a flavivirus-derived endogenous viral element in the peach blossom jellyfish genome (Craspedacusta Sowerby, phylum Cnidaria), implying that the flaviviruses arose early in the evolution of the Metazoa. To date, however, no exogenous flavivirus sequences have been identified in these hosts. To help resolve the antiquity of the Flavivirdae we mined publicly available transcriptome data across the Metazoa. From this, we expanded the diversity within the family through the identification of 32 novel viral sequences, and extended the host range of the pestiviruses to include amphibians, reptiles, and ray-finned fish. Through cophylogenetic analysis we found cross-species transmission to be the predominate macroevolutionary event across the non-vectored flaviviral genera (median, 68%), including a cross-species transmission event between bats and rodents, although long-term virus-host co-divergence was still a regular occurrence (median, 23%). Notably, we discovered flavivirus-like sequences in basal metazoan species, including the first associated with Cnidaria. This sequence formed a basal lineage to the genus Flavivirus and was closer to arthropod and crustacean flaviviruses than those in the tamanavirus group that include a variety of invertebrate and vertebrate viruses. Combined, these data attest an ancient origin of the flaviviruses, close to the emergence of the metazoans 750-800 million years ago.

microbiology↗