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Geoghegan, J. L.

Publications and source records attributed to Geoghegan, J. L..

33 records · Page 2Linked to original sources

Host specificity shapes fish viromes across lakes on an isolated remote island

Fish viromes often provide insights into the origin and evolution of viruses affecting tetrapods, including those associated with significant human diseases. However, despite fish being the most diverse vertebrate group, their viruses are still understudied. We investigated the viromes of fish on Chatham Island (R[e]kohu), a geographically isolated island housing 9% of New Zealands threatened endemic fish species. Using metatranscriptomics, we analyzed samples from seven host species across 16 waterbodies. We identified 19 fish viruses, including 16 novel species, expanding families such as the Coronaviridae, Hantaviridae, Poxviridae, and the recently proposed Tosoviridae family. Surprisingly, virome composition was not influenced by ecological factors measured, and smelt (Retropinna retropinna) viromes were consistent across lakes despite differences in host life history, seawater influence, and community richness. Overall, fish viromes across R[e]kohu were highly diverse and revealed a long history of codivergence between host and virus despite their unique and geographically isolated ecosystem.

microbiology↗

Virome analysis of New Zealand's bats reveals cross-species viral transmission among the Coronaviridae

1.The lesser short-tailed bat (Mystacina tuberculata) and the long-tailed bat (Chalinolobus tuberculatus) are Aotearoa New Zealands only native extant terrestrial mammals and are believed to have migrated from Australia. Long-tailed bats arrived in New Zealand an estimated two million years ago and are closely related to other Australian bat species. Lesser short-tailed bats, in contrast, are the only extant species within the Mystacinidae and are estimated to have been living in isolation in New Zealand for the past 16-18 million years. Throughout this period of isolation, lesser short-tailed bats have become one of the most terrestrial bats in the world. Through a metatranscriptomic analysis of guano samples from eight locations across New Zealand we aimed to characterise the viromes of New Zealands bats and determine whether viruses have jumped between these species over the past two million years. High viral richness was observed among long-tailed bats with viruses spanning seven different viral families. In contrast, no bat-specific viruses were identified in lesser short-tailed bats. Both bat species harboured an abundance of likely dietary- and environmental-associated viruses. We also identified alphacoronaviruses in long-tailed bat guano that had previously been identified in lesser short-tailed bats, suggesting that these viruses had jumped the species barrier after long-tailed bats migrated to New Zealand. Of note, an alphacoronavirus species discovered here possessed a complete genome of only 22,416 nucleotides with entire deletions or truncations of several non-structural proteins, thereby representing what is possibly the shortest genome within the Coronaviridae identified to date. Overall, this study has revealed a diverse range of novel viruses harboured by New Zealands only native terrestrial mammals, in turn expanding our understanding of bat viral dynamics and evolution globally.

microbiology↗

A novel gyrovirus associated with a fatal respiratory disease in yellow-eyed penguin (Megadyptes antipodes) chicks

Yellow-eyed penguins (Megadyptes antipodes), or hoiho in te reo M[a]ori, are predicted to become extinct on mainland Aotearoa New Zealand in the next few decades, with infectious disease a significant contributor to their decline. A recent disease phenomenon termed respiratory distress syndrome (RDS) causing lung pathology has been identified in very young chicks. To date, no causative pathogens for RDS have been identified. In 2020 and 2021, the number of chick deaths from suspected RDS increased four- and five-fold, respectively, with a mortality rate of >90%. Here, we aimed to identify possible pathogens responsible for RDS disease impacting yelloweyed penguins. Total RNA was extracted from tissue samples collected during post-mortem of 43 chicks and subject to metatranscriptomic sequencing. From these data we identified a novel and highly abundant gyrovirus in 80% of tissue samples. This virus exhibited only 41% amino acid identity within VP1 to its closest relative, Gyrovirus 8, discovered in a diseased seabird. No other exogenous viral transcripts, nor pathogenic bacterial, protozoal and fungal organisms, were identified in these tissues. Due to the high relative abundance of viral reads, it is likely that this novel gyrovirus is associated with RDS in yellow-eyed penguin chicks. Author SummaryNew Zealands population of yellow-eyed penguins, also called hoiho, are predicted to become extinct in the next 20-30 years, with disease a major factor contributing to their decline. A new disease, causing fluid and bleeding into the lungs, was initially identified in 2019 in very young chicks. It was characterised as causing respiratory distress with a mortality of >90% usually within the first week of life. To date, no causative pathogens of the disease have been identified. We aimed to identify possible pathogens responsible for respiratory disease in these penguin chicks. A metatranscriptomic survey of dead chicks identified a novel and highly abundant gyrovirus present in diseased tissue, with closely related viruses causing disease in other avian hosts. It is, therefore, highly likely that this novel gyrovirus is associated with respiratory disease in these chicks. This finding offers the potential to increase the success of disease management in the critically endangered yellow-eyed penguin and possibly other at-risk penguin species. The potential to lessen mortality and slow the decline of the species is essential in protecting the biodiversity of New Zealands fauna and flora.

microbiology↗

Faecal virome of the Australian grey-headed flying fox from urban/suburban environments contains novel coronaviruses, retroviruses and sapoviruses

Bats are important reservoirs for viruses of public health and veterinary concern. Virus studies in Australian bats usually target the families Paramyxoviridae, Coronaviridae and Rhabdoviridae, with little known about their overall virome composition. We used metatranscriptomic sequencing to characterise the faecal virome of grey-headed flying foxes from three colonies in urban/suburban locations from two Australian states. We identified viruses from three mammalian-infecting (Coronaviridae, Caliciviridae, Retroviridae) and one possible mammalian-infecting (Birnaviridae) family. Of particular interest were a novel bat betacoronavirus (subgenus Nobecovirus) and a novel bat sapovirus (Caliciviridae), the first identified in Australian bats, as well as a potentially exogenous retrovirus. The novel betacoronavirus was detected in two sampling locations 1,375 km apart and falls in a viral lineage likely with a long association with bats. This study highlights the utility of unbiased sequencing of faecal samples for identifying novel viruses and revealing broad-scale patterns of virus ecology and evolution.

microbiology↗

Cloacal virome of an ancient host lineage - the tuatara (Sphenodon punctatus) - reveals abundant and diverse diet-related viruses

1.Tuatara (Sphenodon punctatus) are one of the most phylogenetically isolated species and provide a unique host system to study virus evolution. While the tuatara genome, sequenced in 2020, revealed many endogenous viral elements, we know little of the exogenous viruses that infect tuatara. We performed a metatranscriptomics study of tuatara cloaca samples from a wild population on Takapourewa (Stephens Island), Aotearoa New Zealand. From these data we identified 49 potentially novel viral species that spanned 20 RNA viral families and/or orders, the vast majority (48) of which were likely dietary related. Notably, using a protein structure homology search, we identified a highly divergent novel virus within the Picornaviridae which may directly infect tuatara. Additionally, two endogenous tuatara adintoviruses were characterised that exhibited long-term viral-host co-divergence. Overall, our results indicate that the tuatara cloacal virome is highly diverse likely due a large number of dietary related viruses.

microbiology↗

Limited Cross-Species Virus Transmission in a Spatially Restricted Coral Reef Fish Community

The Great Barrier Reef (GBR) - the largest coral reef ecosystem in the world - supports over 1200 fish species with some of the highest population densities and diversities seen in vertebrates, offering a high potential for virus transmission among species. As such, the GBR represents an exceptional natural ecosystem to determine the impact of host community diversity on virus evolution and emergence. In recent decades the GBR has also experienced significant threats of extinction, making it one of the most vulnerable ecosystems on the planet. However, our understanding of virus diversity and connectivity in tropical reef fishes remains poor. Here, we employed metatranscriptomic sequencing to reveal the viromes of 61 reef fish species. This identified a total of 132 viruses, 38 of which were vertebrate-associated and therefore likely infecting the fish, including a novel isolate of Santee-cooper ranavirus (Iridoviridae). Notably, we found little evidence for virus transmission between fish species living within a very restricted geographical space - a 100 m2 coral reef ecosystem - suggesting that there might be important host genetic barriers to successful cross-species transmission despite regular exposure. We also identified differences in virome composition between reef fish families, such that cryptobenthic reef fishes - characterized by small body sizes and short life-spans - exhibited greater virome richness compared to large reef fishes. This study suggests that there are important barriers to cross-species transmission, and that successful emergence in a reef fish community likely requires active host adaptation, even among closely related host species.

microbiology↗

Transcriptome Mining Reveals a Spectrum of RNA Viruses in Primitive Plants

Current knowledge of plant viruses stems largely from those affecting economically important plants. Yet, plant species in cultivation represent a small and bias subset of the plant kingdom. Here, we describe virus diversity and abundance from a survey of 1079 transcriptomes from species across the breadth of the plant kingdom (Archaeplastida) by analysing open-source data from the One Thousand Plant Transcriptomes Initiative (1KP). We identified 104 potentially novel viruses, of which 40% comprised single-stranded positive-sense RNA viruses across eight orders, including members of the Hepelivirales, Tymovirales, Cryppavirales, Martellivirales and Picornavirales. One-third of the newly described viruses comprised double-stranded RNA viruses from the orders Durnavirales and Ghabrivirales. The remaining were negative-sense RNA viruses from the Rhabdoviridae, Aspiviridae, Yueviridae, Phenuiviridae and the newly proposed Viridisbunyaviridae. Our analysis considerably expands the known host range of 13 virus families to include lower plants (e.g., Benyviridae and Secoviridae) and four virus families to include algae hosts (e.g., Tymoviridae and Chrysoviridae). The discovery of the first 30 kDa movement protein in a non-vascular plant, suggests that the acquisition of plant virus movement proteins occurred prior to the emergence of the plant vascular system. More broadly, however, a co-phylogeny analysis revealed that the evolutionary history of these families is largely driven by cross-species transmission events. Together, these data highlight that numerous RNA virus families are associated with older evolutionary plant lineages than previously thought and that the scarcity of RNA viruses found in lower plants to date likely reflects a lack of investigation rather than their absence. ImportanceOur knowledge of plant viruses is mainly limited to those infecting economically important host species. In particular, we know little about those viruses infecting primitive plant lineages such as the ferns, lycophytes, bryophytes and charophytes. To expand this understanding, we conducted a broad-scale viral survey of species across the breadth of the plant kingdom. We find that primitive plants harbour a wide diversity of RNA viruses including some that are sufficiently divergent to comprise a new virus family. The primitive plant virome we reveal offers key insights into the evolutionary history of core plant virus gene modules and genome segments. More broadly, this work emphasises that the scarcity of viruses found in these species to date likely reflects the absence of research in this area.

microbiology↗

Slippery when wet: cross-species transmission of divergent coronaviruses in bony and jawless fish and the evolutionary history of the Coronaviridae

The Nidovirales comprise a genetically diverse group of positive-sense single-stranded RNA virus families that infect a range of invertebrate and vertebrate hosts. Recent metagenomic studies have identified nido-like virus sequences, particularly those related to the Coronaviridae, in a range of aquatic hosts including fish, amphibians and reptiles. We sought to identify additional members of the Coronaviridae in both bony and jawless fish through a combination of total RNA sequencing (meta-transcriptomics) and data mining of published RNA sequencing data, and from this reveal more of the long-term patterns and processes of coronavirus evolution. Accordingly, we identified a number of divergent viruses that fell within the Letovirinae subfamily of the Coronaviridae, including those in a jawless fish - the pouched lamprey. By mining fish transcriptome data we identified additional virus transcripts matching these viruses in bony fish from both marine and freshwater environments. These new viruses retained sequence conservation in the RNA-dependant RNA polymerase across the Coronaviridae, but formed a distinct and diverse phylogenetic group. Although there are broad-scale topological similarities between the phylogenies of the major groups of coronaviruses and their vertebrate hosts, the evolutionary relationships of viruses within the Letovirinae does not mirror that of their hosts. For example, the coronavirus found in the pouched lamprey fell within the phylogenetic diversity of bony fish letoviruses, indicative of past host switching events. Hence, despite possessing a phylogenetic history that likely spans the entire history of the vertebrates, coronavirus evolution has been characterised by relatively frequent cross-species transmission, particularly in hosts that reside in aquatic habitats.

microbiology↗

Metagenomic sequencing reveals a lack of virus exchange between native and invasive freshwater fish across the Murray-Darling Basin, Australia

Biological invasions are among the biggest threats to freshwater biodiversity. This is increasingly relevant in the Murray-Darling Basin, Australia, particularly since the introduction of the common carp (Cyprinus carpio). This invasive species now occupies up to 90% of fish biomass, with hugely detrimental impacts on native fauna and flora. To address the ongoing impacts of carp, cyprinid herpesvirus 3 (CyHV-3) has been proposed as a potentially effective biological control. Crucially, however, it is unknown whether CyHV-3 and other cyprinid herpesviruses already exist in the Murray-Darling. Further, little is known about those viruses that naturally occur in wild freshwater fauna, and the frequency with which these viruses jump species boundaries. To document the evolution and diversity of freshwater fish viromes and better understand the ecological context to the proposed introduction of CyHV-3, we performed a meta-transcriptomic viral survey of invasive and native fish across the Murray-Darling Basin, covering over 2,200 km of the river system. Across a total of 36 RNA libraries representing 10 species, we failed to detect CyHV-3 nor any closely related viruses. Rather, meta-transcriptomic analysis identified 18 vertebrate-associated viruses that could be assigned to the Arenaviridae, Astroviridae, Bornaviridae, Caliciviridae, Coronaviridae, Chuviridae, Flaviviridae, Hantaviridae, Hepeviridae, Paramyxoviridae, Picornaviridae, Poxviridae, Reoviridae and Rhabdoviridae families, and a further 27 that were deemed to be associated with non-vertebrate hosts. Notably, we revealed a marked lack of viruses that are shared among invasive and native fishes sampled here, suggesting that there is little virus transmission from common carp to native fish species. Overall, this study provides the first data on the viruses naturally circulating in a major river system and supports the notion that fish harbour a large diversity of viruses with often deep evolutionary histories. Author SummaryThe ongoing invasion of the common carp in the Murray-Darling Basin, Australia, has wreaked havoc on native freshwater ecosystems. This has stimulated research into the possible biological control of invasive carp through the deliberate release of the virus cyprinid herpesvirus 3 (CyHV-3). However, little is known on the diversity of viruses that naturally circulate in wild freshwater fauna, whether these viruses are transmitted between invasive and native species, nor if CyHV-3 or other cyprinid herpesviruses are already present in the basin. To address these fundamental questions we employed meta-transcriptomic next-generation sequencing to characterise the total assemblage of viruses (i.e. the viromes) in three invasive and seven native fish species cohabiting at 10 sites across 2,200 km of the river system. From this analysis we identified 18 vertebrate-associated viruses across 14 viral families, yet a marked lack of virus transmission between invasive and native species. Importantly, no CyHV-3 was detected. This study shows that freshwater fish harbour a high diversity and abundance of viruses, that viruses have likely been associated with fish for millennia, and that there is likely little direct virus transmission between introduced and native species.

microbiology↗

A novel rubi-like virus in the Pacific electric ray (Tetronarce californica) reveals the complex evolutionary history of the Matonaviridae

Rubella virus (RuV) is the causative agent of rubella ("German measles") and remains a global health concern. Until recently, RuV was the only known member of the genus Rubivirus and the only virus species classified within the Matonaviridae family of positive-sense RNA viruses. Other matonaviruses, including two new rubella-like viruses, Rustrela virus and Ruhugu virus, have been identified in several mammalian species, along with more divergent viruses in fish and reptiles. To screen for the presence of additional novel rubella-like viruses we mined published transcriptome data using genome sequences from Rubella, Rustrela, and Ruhugu viruses as baits. From this, we identified a novel rubella-like virus in a transcriptome of Tetronarce californica (Pacific electric ray) that is more closely related to mammalian Rustrela virus than to the divergent fish matonavirus and indicative of a complex pattern of cross-species virus transmission. Analysis of host reads confirmed that the sample analysed was indeed from a Pacific electric ray, and two other viruses identified in this animal, from the Arenaviridae and Reoviridae, grouped with other fish viruses. These findings indicate that the evolutionary history of the Matonaviridae is more complex than previously thought and highlights the vast number of viruses still to be discovered.

microbiology↗

Meta-transcriptomic identification of divergent Amnoonviridae in fish

Tilapia lake virus (TiLV) has caused mass mortalities in farmed and wild tilapia with serious economic and ecological consequences. Until recently, this virus was the sole member of the Amnoonviridae, a family within the order Articulavirales comprising segmented negative-sense RNA viruses. We sought to identify additional viruses within the Amnoonviridae through total RNA sequencing (meta-transcriptomics) and data mining of published transcriptomes. Accordingly, we sampled marine fish species from both Australia and China and discovered two new viruses within the Amnoonviridae, tentatively called Flavolineata virus and Piscibus virus, respectively. In addition, by mining vertebrate transcriptome data we identified nine additional virus transcripts matching to multiple genomic segments of TiLV in both marine and freshwater fish. These new viruses retained sequence conservation with the distantly related Orthomyxoviridae in the RdRp subunit PB1, but formed a distinct and diverse phylogenetic group. These data suggest that the Amnoonviridae have a broad host range within fish and that greater animal sampling will identify additional divergent members of the Articulavirales.

microbiology↗

Divergent influenza-like viruses of amphibians and fish support an ancient evolutionary association

Influenza viruses (family Orthomyxoviridae) infect a variety of vertebrates, including birds, humans, and other mammals. Recent metatranscriptomic studies have uncovered divergent influenza viruses in amphibians, fish and jawless vertebrates, suggesting that these viruses may be widely distributed. We sought to identify additional vertebrate influenza-like viruses through the analysis of publicly available RNA sequencing data. Accordingly, by data mining, we identified the complete coding segments of five divergent vertebrate influenza-like viruses. Three fell as sister lineages to influenza B virus: salamander influenza-like virus in Mexican walking fish (Ambystoma mexicanum) and plateau tiger salamander (Ambystoma velasci), siamese algae-eater influenza-like virus in siamese algae-eater fish (Gyrinocheilus aymonieri) and chum salmon influenza-like virus in chum salmon (Oncorhynchus keta). Similarly, we identified two influenza-like viruses of amphibians that fell as sister lineages to influenza D virus: cane toad influenza-like virus and the ornate chorus frog influenza-like virus, in the cane toad (Rhinella marina) and ornate chorus frog (Microhyla fissipes), respectively. Despite their divergent phylogenetic positions, these viruses retained segment conservation and splicing consistent with transcriptional regulation in influenza B and influenza D viruses, and were detected in respiratory tissues. These data suggest that influenza viruses have been associated with vertebrates for their entire evolutionary history.

microbiology↗

How accurately can we assess zoonotic risk?

The authors have withdrawn their manuscript as a website associated with a zoonotic risk prediction tool mentioned here was not public. Therefore, the authors do not wish this work to be cited as reference for the project. If you have any questions, please contact the corresponding author

microbiology↗

Red fox viromes across an urban-rural gradient

The Red fox (Vulpes vulpes) has established large populations in Australias urban and rural areas since its introduction following European settlement. Foxes cryptic and highly adaptable nature allows them to invade cities and live among humans while remaining largely unnoticed. Urban living and access to anthropogenic food resources also influences fox ecology. Urban foxes grow larger, live at higher densities and are more social than their rural counterparts. These ecological changes in urban red foxes are likely to impact the pathogens that they harbour, and foxes could pose a disease risk to humans and other species that share these urban spaces. To assess this possibility, we used a meta-transcriptomic approach to characterise the viromes of urban and rural foxes across the Greater Sydney region in Australia. Urban and rural foxes differed significantly in virome composition, with rural foxes harbouring a greater abundance of viruses compared to their urban counterparts. In contrast, urban fox viromes comprised a greater diversity of viruses compared to rural foxes. We identified nine potentially novel vertebrate-associated viruses in both urban and rural foxes, some of which are related to viruses associated with disease in domestic species and humans. These included members of the Astroviridae, Picobirnaviridae, Hepeviridae and Picornaviridae as well as rabbit haemorrhagic disease virus-2 (RHDV2). This study sheds light on the viruses carried by urban and rural foxes and emphasises the need for greater genomic surveillance of foxes and other invasive species at the human-wildlife interface. ImportanceUrbanisation of wild environments is increasing as human populations continue to expand. Remnant pockets of natural environments and other green spaces in urban landscapes provide invasive wildlife such as red foxes with refuges within urban areas, where they thrive on the food resources provisioned by humans. Close contact between humans, domestic species and foxes likely increases the risk of novel pathogen emergence. Indeed, the vast majority of emerging infectious diseases in humans originate in wild animals. Here, we explored potential differences in viromes between urban fox invaders and their rural counterparts. Viromes of foxes and their ectoparasites comprise a diversity of viruses including those from the Astroviridae, Picobirnaviridae, Hepeviridae, Caliciviridae and Picornaviridae. Microbial surveillance in foxes and other urban wildlife is vital for monitoring viral emergence and for the prevention of infectious diseases.

microbiology↗

Host evolutionary history and ecology shape virome composition in fishes

Revealing the determinants of virome composition is central to placing disease emergence in a broader evolutionary context. Fish are the most species-rich group of vertebrates and so provide an ideal model system to study the factors that shape virome compositions and their evolution. We characterised the viromes of 19 wild-caught species of marine fish using total RNA sequencing (meta-transcriptomics) combined with analyses of sequence and protein structural homology to identify divergent viruses that often evade characterisation. From this, we identified 25 new vertebrate-associated viruses and a further 22 viruses likely associated with fish diet or their microbiomes. The vertebrate-associated viruses identified here included the first fish virus in the Matonaviridae (single-strand, negative-sense RNA virus). Other viruses fell within the Astroviridae, Picornaviridae, Arenaviridae, Reoviridae, Hepadnaviridae, Paramyxoviridae, Rhabdoviridae, Hantaviridae, Filoviridae and Flaviviridae and were sometimes phylogenetically distinct from known fish viruses. We also show how key metrics of virome composition - viral richness, abundance and diversity - can be analysed along with host ecological and biological factors as a means to understand virus ecology. Accordingly, these data suggest that that the vertebrate-associated viromes of the fish sampled here are predominantly shaped by the phylogenetic history (i.e. taxonomic order) of their hosts, along with several biological factors including water temperature, habitat depth, community diversity and swimming behaviour. No such correlations were found for viruses associated with porifera, molluscs, arthropods, fungi and algae, that are unlikely to replicate in fish hosts. Overall, these data indicate that fish harbour particularly large and complex viromes and the vast majority of fish viromes are undescribed.

microbiology↗