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Costa, V. A.

Publications and source records attributed to Costa, V. A..

9 recordsLinked to original sources

A new lineage of Ranavirus micropterus1 infects ornamental wrasses from the Great Barrier Reef and causes severe disease in captivity

The Great Barrier Reef (GBR) supports remarkable vertebrate diversity but is among the most fragile ecosystems globally, and diseases affecting reef fishes remain poorly understood. We employed traditional veterinary diagnostic techniques and metatranscriptomics to investigate a disease outbreak with 100% mortality in captive wrasses (Macropharyngodon choati) from the GBR. Histopathology revealed multifocal necrosis of renal tubules, and cytopathic effect was observed in bluegill fry cell lines. A novel ranavirus isolate, Macropharyngodon choati ranavirus (McRV), was identified at exceptionally high transcript abundance across different host tissues, alongside strong expression of host genes linked to cellular stress and immune function. Phylogenetic analysis placed McRV in a distinct clade of wrasse ranaviruses, clustering with a virus previously identified on the GBR, suggesting that wild wrasses serve as natural hosts. These data emphasise the need for enhanced pathogen monitoring in marine wildlife increasingly threatened by anthropogenic change.

microbiology↗

Limited transmission of microbial species among coral reef fishes from the Great Barrier Reef, Australia

Reef fishes account for one-third of all extant marine fishes and exhibit enormous biodiversity within a highly interactive ecosystem. Yet relatively little is known about the diversity and evolution of microbial species (bacteria, viruses, and eukaryotes) associated with reef fish, even though this may provide valuable insights into the factors that shape microbial communities within vertebrate hosts as well as the extent and pattern of cross-species transmission. Through metatranscriptomic sequencing we characterised the viruses, bacteria, and single-celled eukaryotes from 128 reef fish species inhabiting Lizard Island and Orpheus Island on the Great Barrier Reef, Australia. We assessed whether microbial communities differed between islands that are separated by approximately 450 kilometres, and to what extent viruses were able to emerge in new hosts. Notably, despite strong ecological interactions in the reef environment, and the presence of the same families and subfamilies of viruses and bacteria on both islands, there was minimal evidence for the cross-species transmission of individual microorganisms among fish species. An exception was the high prevalence of the bacterial pathogen Photobacterium damselae among apparently healthy cardinalfishes from both islands, indicating that these fish species are natural reservoirs within the reef system. Overall, these data suggest that reef fishes have microbial-host associations that arose prior to the formation of the Great Barrier Reef, leading to strong host barriers to cross-species microbial transmission even within a highly interactive and species-rich environment.

microbiology↗

Mapping glycoprotein structure reveals defining events in the evolution of the Flaviviridae

Viral glycoproteins drive membrane fusion in enveloped viruses and determine host range, tissue tropism and pathogenesis. Despite their importance, there is a fragmentary understanding of glycoproteins within the Flaviviridae; for many species the glycoproteins have not yet been identified, for others, such as the hepaciviruses, the molecular mechanisms of membrane fusion remain uncharacterised. Here, we combine comprehensive phylogenetic analyses with systematic protein structure prediction to survey glycoproteins across the entire Flaviviridae. We discover class-II fusion systems, homologous to the orthoflavivirus E glycoprotein, in most species, including highly-divergent jingmenviruses and large genome flaviviruses. However, the E1E2 glycoproteins of the hepaci-, pegi- and pestiviruses are structurally distinct, may represent a novel class of fusion mechanism, and are strictly associated with infection of vertebrate hosts. By mapping glycoprotein distribution onto the underlying phylogeny we reveal a complex history of evolutionary events that have shaped the diverse virology and ecology of the Flaviviridae.

microbiology↗

Host adaptive radiation is associated with rapid virus diversification and cross-species transmission in African cichlid fishes

Adaptive radiations are generated through a complex interplay of biotic and abiotic factors. Although adaptive radiations have been widely studied in the context of animal and plant evolution, little is known about how they impact the evolution of the viruses that infect these hosts, which in turn may provide insights into the drivers of disease emergence. We examined how the rapid adaptive radiation of the African cichlid fishes of Lake Tanganyika over the last 10 million years has shaped the diversity and evolution of the viruses they carry. Through metatranscriptomic analysis we identified 121 vertebrate-associated viruses among various tissue types that fell into 13 RNA and 4 DNA virus groups. Host-switching was commonplace, particularly within the Astroviridae, Metahepadnavirus, Nackednavirus, Picornaviridae, and Hepacivirus groups, occurring more frequently than in other fish communities. A time-calibrated phylogeny revealed that hepacivirus evolution was not constant throughout the cichlid radiation, but accelerated 2-3 million years ago, coinciding with a period of rapid cichlid diversification and niche packing in Lake Tanganyika, thereby providing more closely related hosts for viral infection. These data show that African cichlids contain a complex interacting pool of virus diversity, likely reflecting their close genetic relationships that lowers the barriers to cross-species virus transmission.

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↗

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↗

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↗

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↗