Termitidae comprises ∼80% of all termite species 1 that play dominant decomposer roles in tropical ecosystems 2, 3. Two major events during termite evolution were the loss of cellulolytic gut ...protozoans in the ancestor of Termitidae and the subsequent gain in the termitid subfamily Macrotermitinae of fungal symbionts cultivated externally in “combs” constructed within the nest 4, 5. How these symbiotic transitions occurred remains unresolved. Phylogenetic analyses of mitochondrial data previously suggested that Macrotermitinae is the earliest branching termitid lineage, followed soon after by Sphaerotermitinae 6, which cultivates bacterial symbionts on combs inside its nests 7. This has led to the hypothesis that comb building was an important evolutionary step in the loss of gut protozoa in ancestral termitids 8. We sequenced genomes and transcriptomes of 55 termite species and reconstructed phylogenetic trees from up to 4,065 orthologous genes of 68 species. We found strong support for a novel sister-group relationship between the bacterial comb-building Sphaerotermitinae and fungus comb-building Macrotermitinae. This key finding indicates that comb building is a derived trait within Termitidae and that the creation of a comb-like “external rumen” involving bacteria or fungi may not have driven the loss of protozoa from ancestral termitids, as previously hypothesized. Instead, associations with gut prokaryotic symbionts, combined with dietary shifts from wood to other plant-based substrates, may have played a more important role in this symbiotic transition. Our phylogenetic tree provides a platform for future studies of comparative termite evolution and the evolution of symbiosis in this taxon.
•A phylogenetic tree of termites is reconstructed using 4,065 orthologous genes•Fungiculture in Macrotermitinae postdates the loss of gut protists•Sphaerotermes and Macrotermitinae descended from a common comb-building ancestor•Gut protists were probably replaced by gut bacteria in the ancestor of Termitidae
Bucek et al. use transcriptomic data to reconstruct a phylogenetic tree of termites. Their tree sheds light on the relationships among termite families and subfamilies, and it provides a timeline of the evolution of termites with their digestive symbionts.
Understanding the microbiome of ticks in Australia is of considerable interest given the ongoing debate over whether Lyme disease and its causative agent, the bacterium
, are present in Australia. ...The diversity of bacteria infecting Australian ticks has been studied using both culture- and metagenomics-based techniques. However, little is known about the virome of Australian ticks, including whether this includes viruses with the potential to infect mammals. We used a meta-transcriptomics approach to reveal the diversity and evolution of viruses from Australian ticks collected from two locations on the central east coast of Australia, including metropolitan Sydney. From this we identified 19 novel RNA viruses belonging to 12 families, as well as 1 previously described RNA virus. The majority of these viruses were related to arthropod-associated viruses, suggesting that they do not utilize mammalian hosts. However, two novel viruses discovered in ticks feeding on bandicoot marsupials clustered closely within the mammal-associated hepacivirus and pestivirus groups (family
). Another bandicoot tick yielded a novel coltivirus (family
), a group of largely tick-associated viruses containing the known human pathogen Colorado tick fever virus and its relative, Eyach virus. Importantly, our transcriptomic data provided no evidence for the presence of
in any tick sample, providing further evidence against the presence of Lyme disease in Australia. In sum, this study reveals that Australian ticks harbor a diverse virome, including some viruses that merit additional screening in the context of emerging infectious disease.
Each year a growing number of individuals along the east coast of Australia experience debilitating disease following tick bites. As there is no evidence for the presence of the causative agent of Lyme disease,
, in Australian ticks, the etiological basis of this disease syndrome remains controversial. To characterize the viruses associated with Australian ticks, particularly those that might be associated with mammalian infection, we performed unbiased RNA sequencing on 146 ticks collected across two locations along the coast of New South Wales, Australia. This revealed 19 novel RNA viruses from a diverse set of families. Notably, three of these viruses clustered with known mammalian viruses, including a novel coltivirus that was related to the human pathogen Colorado tick fever virus.
Insects comprise the largest proportion of animals on earth and are frequently implicated in the transmission of vector-borne diseases. However, considerable attention has been paid to the ...phytophagous and hematophagous insects, with results that provide insufficient and biased information about the viruses in insects. Here, we have delivered compelling evidence for the exceptional abundance and genetic diversity of RNA viruses in a wide range of insects. Novel viruses were found to cover major categories of RNA viruses, and many formed novel clusters divergent from the previously described taxa, dramatically broadening the range of known RNA viruses in insects. These newly characterized RNA viruses exhibited high levels of genomic plasticity in genome size, open reading frame (ORF) number, intergenic structure, and gene rearrangement and segmentation. This work provides comprehensive insight into the origin, spread, and evolution of RNA viruses. Of course, a large-scale virome project involving more organisms would provide more-detailed information about the virus infections in insects.
ABSTRACT
Increasing data indicate that insects serve as major reservoirs and vectors of viruses, which account for the continuously increasing ecological burden and infectious disease outbreaks. Uncovering the hidden diversity of viruses in insects will further the understanding of the ecological and evolutionary perspectives in the emergence of insect-associated virus diseases. In this study, we queried transcriptome sequencing (RNA-Seq) data from more than 600 species across 32 insect orders dwelling in different ecological habitats and recovered more than 1,213 RNA viruses that were recapitulated in 40 families, 2 unclassified genera, and many unspecified viral groups. These novel viruses included the well-known insect-associated viruses within
Flaviviridae
,
Picornavirales
,
Bunyavirales
,
Mononegavirales
,
Nidovirales
,
Reoviridae
, and
Negevirus
. More appeared to form novel clusters within previously described taxa or could be resolved as paraphyletic, including the first astrovirus identified in insects, in which many were sufficiently divergent to warrant the establishment of new virus genera or families. Additionally, some viruses were closely related to the recognized plant-, fungus-, and vertebrate-specific species, implying the importance of relationships between insect behavior and virus spread. Comparative genome analyses also revealed high genomic variability with respect to the flexible gene pool and genome architecture of these newly described viruses, including the evidence for genome reshuffling first discovered in
Dicistroviridae
. The data reflecting the genetically and ecologically diverse viral populations in insects greatly expand our understanding of RNA viruses in nature and highlight that the biodiversity of RNA viruses remains largely unexplored.
IMPORTANCE
Insects comprise the largest proportion of animals on earth and are frequently implicated in the transmission of vector-borne diseases. However, considerable attention has been paid to the phytophagous and hematophagous insects, with results that provide insufficient and biased information about the viruses in insects. Here, we have delivered compelling evidence for the exceptional abundance and genetic diversity of RNA viruses in a wide range of insects. Novel viruses were found to cover major categories of RNA viruses, and many formed novel clusters divergent from the previously described taxa, dramatically broadening the range of known RNA viruses in insects. These newly characterized RNA viruses exhibited high levels of genomic plasticity in genome size, open reading frame (ORF) number, intergenic structure, and gene rearrangement and segmentation. This work provides comprehensive insight into the origin, spread, and evolution of RNA viruses. Of course, a large-scale virome project involving more organisms would provide more-detailed information about the virus infections in insects.
Viruses use the cellular machinery of their hosts for replication. It has therefore been proposed that the nucleotide and dinucleotide compositions of viruses should match those of their host ...species. If this is upheld, it may then be possible to use dinucleotide composition to predict the true host species of viruses sampled in metagenomic surveys. However, it is also clear that different taxonomic groups of viruses tend to have distinctive patterns of dinucleotide composition that may be independent of host species. To determine the relative strength of the effect of host versus virus family in shaping dinucleotide composition, we performed a comparative analysis of 20 RNA virus families from 15 host groupings, spanning two animal phyla and more than 900 virus species. In particular, we determined the odds ratios for the 16 possible dinucleotides and performed a discriminant analysis to evaluate the capability of virus dinucleotide composition to predict the correct virus family or host taxon from which it was isolated. Notably, while 81% of the data analyzed here were predicted to the correct virus family, only 62% of these data were predicted to their correct subphylum/class host and a mere 32% to their correct mammalian order. Similarly, dinucleotide composition has a weak predictive power for different hosts within individual virus families. We therefore conclude that dinucleotide composition is generally uniform within a virus family but less well reflects that of its host species. This has obvious implications for attempts to accurately predict host species from virus genome sequences alone.
Determining the processes that shape virus genomes is central to understanding virus evolution and emergence. One question of particular importance is why nucleotide and dinucleotide frequencies differ so markedly between viruses. In particular, it is currently unclear whether host species or virus family has the biggest impact on dinucleotide frequencies and whether dinucleotide composition can be used to accurately predict host species. Using a comparative analysis, we show that dinucleotide composition has a strong phylogenetic association across different RNA virus families, such that dinucleotide composition can predict the family from which a virus sequence has been isolated. Conversely, dinucleotide composition has a poorer predictive power for the different host species within a virus family and across different virus families, indicating that the host has a relatively small impact on the dinucleotide composition of a virus genome.
In the 19th century, there were several major cholera pandemics in the Indian subcontinent, Europe, and North America. The causes of these outbreaks and the genomic strain identities remain a ...mystery. We used targeted high-throughput sequencing to reconstruct the Vibrio cholerae genome from the preserved intestine of a victim of the 1849 cholera outbreak in Philadelphia, part of the second cholera pandemic. This O1 biotype strain has 95 to 97% similarity with the classical O395 genome, differing by 203 single-nucleotide polymorphisms (SNPs), lacking three genomic islands, and probably having one or more tandem cholera toxin prophage (CTX) arrays, which potentially affected its virulence. This result highlights archived medical remains as a potential resource for investigations into the genomic origins of past pandemics.
Aquatic birds harbor diverse influenza A viruses and are a major viral reservoir in nature. The recent discovery of influenza viruses of a new H17N10 subtype in Central American fruit bats suggests ...that other New World species may similarly carry divergent influenza viruses. Using consensus degenerate RT-PCR, we identified a novel influenza A virus, designated as H18N11, in a flat-faced fruit bat (Artibeus planirostris) from Peru. Serologic studies with the recombinant H18 protein indicated that several Peruvian bat species were infected by this virus. Phylogenetic analyses demonstrate that, in some gene segments, New World bats harbor more influenza virus genetic diversity than all other mammalian and avian species combined, indicative of a long-standing host-virus association. Structural and functional analyses of the hemagglutinin and neuraminidase indicate that sialic acid is not a ligand for virus attachment nor a substrate for release, suggesting a unique mode of influenza A virus attachment and activation of membrane fusion for entry into host cells. Taken together, these findings indicate that bats constitute a potentially important and likely ancient reservoir for a diverse pool of influenza viruses.
Wolbachia is an endosymbiotic bacterium that can block viral infections in arthropods, generating interest in its potential to control the spread of mosquito-borne disease. Drosophila melanogaster is ...model organism for Wolbachia infection, and the wMel strain of Wolbachia can improve host survival following viral infection. However, it is unclear whether wMel induces anti-viral blocking against the broader native virome of D.melanogaster, or whether the major effect of Wolbachia is a reduction in viral abundance rather than viral clearance. We examined the effect of Wolbachia on viral abundance by comparing the total transcriptome of wMel-positive and wMel-negative D. melanogaster populations sampled from six locations in Australia. In addition, we examined the impact of wMel on individual flies by obtaining transcriptome data from 20 wMelpositive and 20 wMel-negative D. melanogaster from the location (Melbourne) with highest density of wMel. These data revealed high viral abundance in both Wolbachia-positive and -negative populations and individuals. Notably, none of the viral species identified, representing RNA viruses from at least nine families/floating genera, showed evidence of protection by wMel. Although the viral loads of picorna-like viruses are reduced by wMel under experimental conditions, we observed no such effect here. These data show that D. melanogaster can harbour abundant RNA viruses regardless of its Wolbachia status and imply that the interaction between Wolbachia and viruses in nature is more complex than simple blocking.
Viruses of the family Flaviviridae are important pathogens of humans and other animals and are currently classified into four genera. To better understand their diversity, evolutionary history, and ...genomic flexibility, we used transcriptome sequencing (RNA-seq) to search for the viruses related to the Flaviviridae in a range of potential invertebrate and vertebrate hosts. Accordingly, we recovered the full genomes of five segmented jingmenviruses and 12 distant relatives of the known Flaviviridae ("flavi-like" viruses) from a range of arthropod species. Although these viruses are highly divergent, they share a similar genomic plan and common ancestry with the Flaviviridae in the NS3 and NS5 regions. Remarkably, although these viruses fill in major gaps in the phylogenetic diversity of the Flaviviridae, genomic comparisons reveal important changes in genome structure, genome size, and replication/gene regulation strategy during evolutionary history. In addition, the wide diversity of flavi-like viruses found in invertebrates, as well as their deep phylogenetic positions, suggests that they may represent the ancestral forms from which the vertebrate-infecting viruses evolved. For the vertebrate viruses, we expanded the previously mammal-only pegivirus-hepacivirus group to include a virus from the graceful catshark (Proscyllium habereri), which in turn implies that these viruses possess a larger host range than is currently known. In sum, our data show that the Flaviviridae infect a far wider range of hosts and exhibit greater diversity in genome structure than previously anticipated.
The family Flaviviridae of RNA viruses contains several notorious human pathogens, including dengue virus, West Nile virus, and hepatitis C virus. To date, however, our understanding of the biodiversity and evolution of the Flaviviridae has largely been directed toward vertebrate hosts and their blood-feeding arthropod vectors. Therefore, we investigated an expanded group of potential arthropod and vertebrate host species that have generally been ignored by surveillance programs. Remarkably, these species contained diverse flaviviruses and related viruses that are characterized by major changes in genome size and genome structure, such that these traits are more flexible than previously thought. More generally, these data suggest that arthropods may be the ultimate reservoir of the Flaviviridae and related viruses, harboring considerable genetic and phenotypic diversity. In sum, this study revises the traditional view on the evolutionary history, host range, and genomic structures of a major group of RNA viruses.
The Tasmanian devil is an endangered carnivorous marsupial threatened by devil facial tumor disease (DFTD). While research on DFTD has been extensive, little is known about viruses in devils and ...whether any are of potential conservation relevance for this endangered species. Using both metagenomics based on virion enrichment and sequence-independent amplification (virion-enriched metagenomics) and metatranscriptomics based on bulk RNA sequencing, we characterized and compared the fecal viromes of captive and wild devils. A total of 54 fecal samples collected from two captive and four wild populations were processed for virome characterization using both approaches. In total, 24 novel marsupial-related viruses, comprising a sapelovirus, astroviruses, rotaviruses, picobirnaviruses, parvoviruses, papillomaviruses, polyomaviruses, and a gammaherpesvirus, were identified, as well as known mammalian pathogens such as rabbit hemorrhagic disease virus 2. Captive devils showed significantly lower viral diversity than wild devils. Comparison of the two virus discovery approaches revealed substantial differences in the number and types of viruses detected, with metatranscriptomics better suited for RNA viruses and virion-enriched metagenomics largely identifying more DNA viruses. Thus, the viral communities revealed by virion-enriched metagenomics and metatranscriptomics were not interchangeable and neither approach was able to detect all viruses present. An integrated approach using both virion-enriched metagenomics and metatranscriptomics constitutes a powerful tool for obtaining a complete overview of both the taxonomic and functional profiles of viral communities within a sample.
The Tasmanian devil is an iconic Australian marsupial that has suffered an 80% population decline due to a contagious cancer, devil facial tumor disease, along with other threats. Until now, viral discovery in this species has been confined to one gammaherpesvirus (dasyurid herpesvirus 2 DaHV-2), for which captivity was identified as a significant risk factor. Our discovery of 24 novel marsupial-associated RNA and DNA viruses, and that viral diversity is lower in captive than in wild devils, has greatly expanded our knowledge of gut-associated viruses in devils and provides important baseline information that will contribute to the conservation and captive management of this endangered species. Our results also revealed that a combination of virion-enriched metagenomics and metatranscriptomics may be a more comprehensive approach for virome characterization than either method alone. Our results thus provide a springboard for continuous improvements in the way we study complex viral communities.
distinct lineage of influenza A virus from bats Tong, Suxiang; Li, Yan; Rivailler, Pierre ...
Proceedings of the National Academy of Sciences,
03/2012, Letnik:
109, Številka:
11
Journal Article
Recenzirano
Odprti dostop
Influenza A virus reservoirs in animals have provided novel genetic elements leading to the emergence of global pandemics in humans. Most influenza A viruses circulate in waterfowl, but those that ...infect mammalian hosts are thought to pose the greatest risk for zoonotic spread to humans and the generation of pandemic or panzootic viruses. We have identified an influenza A virus from little yellow-shouldered bats captured at two locations in Guatemala. It is significantly divergent from known influenza A viruses. The HA of the bat virus was estimated to have diverged at roughly the same time as the known subtypes of HA and was designated as H17. The neuraminidase (NA) gene is highly divergent from all known influenza NAs, and the internal genes from the bat virus diverged from those of known influenza A viruses before the estimated divergence of the known influenza A internal gene lineages. Attempts to propagate this virus in cell cultures and chicken embryos were unsuccessful, suggesting distinct requirements compared with known influenza viruses. Despite its divergence from known influenza A viruses, the bat virus is compatible for genetic exchange with human influenza viruses in human cells, suggesting the potential capability for reassortment and contributions to new pandemic or panzootic influenza A viruses.
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