Ebola in great apes – current knowledge,possibilities for vaccination,and implications for conservation and human health

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Marburg virus infection detected in a common African bat

Marburg and Ebola viruses can cause large hemorrhagic fever (HF) outbreaks with high case fatality (80-90%) in human and great apes. Identification of the natural reservoir of these viruses is one of the most important topics in this field and a fundamental key to understanding their natural history. Despite the discovery of this virus family almost 40 years ago, the search for the natural reservoir of these lethal pathogens remains an enigma despite numerous ecological studies. Here, we report the discovery of Marburg virus in a common species of fruit bat (Rousettus aegyptiacus) in Gabon as shown by finding virus-specific RNA and IgG antibody in individual bats. These Marburg virus positive bats represent the first naturally infected non-primate animals identified. Furthermore, this is the first report of Marburg virus being present in this area of Africa, thus extending the known range of the virus. These data imply that more areas are at risk for MHF outbreaks than previously realized and correspond well with a recently published report in which three species of fruit bats were demonstrated to be likely reservoirs for Ebola virus.     

Does seed ingestion by bats enhance germination? A new meta‐analysis 15 years later

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The ecology of Ebola virus

Since Ebola virus was first identified more than 30 years ago, tremendous progress has been made in understanding the molecular biology and pathogenesis of this virus. However, the means by which Ebola virus is maintained and transmitted in nature remains unclear despite dedicated efforts to answer these questions. Recent work has provided new evidence that fruit bats might have a role as a reservoir species, but it is not clear whether other species are also involved or how transmission to humans or apes takes place. Two opposing hypotheses for Ebola emergence have surfaced; one of long-term local persistence in a cryptic and infrequently contacted reservoir, versus another of a more recent introduction of the virus and directional spread through susceptible populations. Nevertheless, with the increasing frequency of human filovirus outbreaks and the tremendous impact of infection on the already threatened great ape populations, there is an urgent need to better understand the ecology of Ebola virus in nature.     

Discovering the Brazilian bat fauna: a task for two centuries?

• 1 Brazil is the second most bat species‐rich country in the world, but the available information on the occurrence and distribution of bat species in Brazil is still heterogeneous and fragmented.
• 2 We review the occurrence and distribution of bat species in Brazil, analyse the spatial performance of inventories conducted to date and identify knowledge gaps. We also identify the main factors contributing to the recent increase in the knowledge of the Brazilian bat fauna, and make suggestions for maintaining this momentum into the near future.
• 3 We plotted record coordinates on a map, grouped them in 0.5 degrees of latitude × 0.5 degrees of longitude grid cells, and analysed records for each of the five terrestrial biomes in Brazil, and for the 1439 priority polygons for the conservation of Brazilian biodiversity.
• 4 We identified 5502 formal bat records in Brazil, indicating that less than 10% of the country is minimally surveyed, and that for nearly 60% of Brazil there is not a single record of bat species. Record coverage varies from 79% in the Atlantic Forest to 24% in Amazonia, but none of the Brazilian biomes is well surveyed for bats. Bat species have been recorded in only 15% of the priority areas for Brazilian biodiversity conservation.
• 5 If the current rate of recording bats in empty grid cells (10% every 4 years) was maintained, it would take 33 years for all cells to have a single record. If the current rate of recording ≥20 species in a grid cell (0.8% per year) was maintained, it would take 200 years for the bat fauna of Brazil to be minimally surveyed. Alarmingly, most of the data‐poor areas are at the expansion frontiers of the agro‐business, near the surrounding deforestation fronts.
• 6 We make recommendations for scientific research on bats in Brazil, to ensure the conservation of this ecologically important taxon.

     

Seasonal variation in food availability and relative importance of dietary items in the Gambian epauletted fruit bat (Epomophorus gambianus)

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Ebola and Marburg virus diseases in Africa: Increased risk of outbreaks in previously unaffected areas?

Filoviral hemorrhagic fever (FHF) is caused by ebolaviruses and marburgviruses, which both belong to the family Filoviridae. Egyptian fruit bats (Rousettus aegyptiacus) are the most likely natural reservoir for marburgviruses and entry into caves and mines that they stay in has often been associated with outbreaks of MVD. On the other hand, the natural reservoir for ebola viruses remains elusive; however, handling of wild animal carcasses has been associated with some outbreaks of EVD. In the last two decades, there has been an increase in the incidence of FHF outbreaks in Africa, some being caused by a newly found virus and some occurring in previously unaffected areas such as Guinea, Liberia and Sierra Leone, in which the most recent EVD outbreak occurred in 2014. Indeed, the predicted geographic distribution of filoviruses and their potential reservoirs in Africa includes many countries in which FHF has not been reported. To minimize the risk of virus dissemination in previously unaffected areas, there is a need for increased investment in health infrastructure in African countries, policies to facilitate collaboration between health authorities from different countries, implementation of outbreak control measures by relevant multi‐disciplinary teams and education of the populations at risk.     

Molecular systematics and phylogeography of the tribe Myonycterini (Mammalia,Pteropodidae) inferred from mitochondrial and nuclear markers

The tribe Myonycterini comprises five fruit bat species of the family Pteropodidae, which are endemic to tropical Africa. Previous studies have produced conflicting results about their interspecific relationships.Here, we performed a comparative phylogeographic analysis based on 148 complete cytochrome b gene sequences from the three species distributed in West Africa and Central Africa (Myonycteris torquata, Lissonycteris angolensis and Megaloglossus woermanni). In addition, we investigated phylogenetic relationships within the tribe Myonycterini, using a matrix including 29 terminal taxa and 7235 nucleotide characters, corresponding to an alignment of two mitochondrial genes and seven nuclear introns. Our phylogenetic analyses confirmed that the genus Megaloglossus belongs to the tribe Myonycterini. Further, the genus Rousettus is paraphyletic, with R. lanosus, sometimes placed in the genus Stenonycteris, being the sister-group of the tribes Myonycterini and Epomophorini. Our phylogeographic results showed that populations of Myonycteris torquata and Megaloglossus woermanni from the Upper Guinea Forest are highly divergent from those of the Congo Basin Forest. Based on our molecular data, we recommended several taxonomic changes. First, Stenonycteris should be recognized as a separate genus from Rousettus and composed of S. lanosus. This genus should be elevated to a new tribe, Stenonycterini, within the subfamily Epomophorinae. This result shows that the evolution of lingual echolocation was more complicated than previously accepted. Second, the genus Lissonycteris is synonymised with Myonycteris. Third, the populations from West Africa formerly included in Myonycteris torquata and Megaloglossus woermanni are now placed in two distinct species, respectively, Myonycteris leptodon and Megaloglossus azagnyi sp. nov. Our molecular dating estimates show that the three phases of taxonomic diversification detected within the tribe Myonycterini can be related to three distinct decreases in tree cover vegetation, at 6.5–6, 2.7–2.5, and 1.8–1.6 Ma. Our results suggest that the high nucleotide distance between Ebolavirus Côte d’Ivoire and Ebolavirus Zaire can be correlated with the Plio/Pleistocene divergence between their putative reservoir host species, i.e., Myonycteris leptodon and Myonycteris torquata, respectively.     

The Glycoproteins of All Filovirus Species Use the Same Host Factors for Entry into Bat and Human Cells but Entry Efficiency Is Species Dependent

Ebola and marburgviruses, members of the family Filoviridae, can cause severe hemorrhagic fever in humans. The ongoing Ebola virus (EBOV) disease epidemic in Western Africa claimed more than 11,300 lives and was associated with secondary cases outside Africa, demonstrating that filoviruses pose a global health threat. Bats constitute an important natural reservoir of filoviruses, including viruses of the recently identified Cuevavirus genus within the Filoviridae family. However, the interactions of filoviruses with bat cells are incompletely understood. Here, we investigated whether filoviruses employ different strategies to enter human and bat cells. For this, we examined host cell entry driven by glycoproteins (GP) from all filovirus species into cell lines of human and fruit bat origin. We show that all GPs were able to mediate entry into human and most fruit bat cell lines with roughly comparable efficiency. In contrast, the efficiency of entry into the cell line EidNi/41 derived from a straw-colored fruit bat varied markedly between the GPs of different filovirus species. Furthermore, inhibition studies demonstrated that filoviruses employ the same host cell factors for entry into human, non-human primate and fruit bat cell lines, including cysteine proteases, two pore channels and NPC1 (Niemann-Pick C1 molecule). Finally, processing of GP by furin and the presence of the mucin-like domain in GP were dispensable for entry into both human and bat cell lines. Collectively, these results show that filoviruses rely on the same host cell factors for entry into human and fruit bat cells, although the efficiency of the usage of these factors might differ between filovirus species.     

Zoonotic risk factors associated with seroprevalence of Ebola virus GP antibodies in the absence of diagnosed Ebola virus disease in the Democratic Republic of Congo

BackgroundEbola virus (EBOV) is a zoonotic filovirus spread through exposure to infected bodily fluids of a human or animal. Though EBOV is capable of causing severe disease, referred to as Ebola Virus Disease (EVD), individuals who have never been diagnosed with confirmed, probable or suspected EVD can have detectable EBOV antigen-specific antibodies in their blood. This study aims to identify risk factors associated with detectable antibody levels in the absence of an EVD diagnosis.MethodologyData was collected from September 2015 to August 2017 from 1,366 consenting individuals across four study sites in the DRC (Boende, Kabondo-Dianda, Kikwit, and Yambuku). Seroreactivity was determined to EBOV GP IgG using Zaire Ebola Virus Glycoprotein (EBOV GP antigen) ELISA kits (Alpha Diagnostic International, Inc.) in Kinshasa, DRC; any result above 4.7 units/mL was considered seroreactive. Among the respondents, 113 (8.3%) were considered seroreactive. Several zoonotic exposures were associated with EBOV seroreactivity after controlling for age, sex, healthcare worker status, location, and history of contact with an EVD case, namely: ever having contact with bats, ever having contact with rodents, and ever eating non-human primate meat. Contact with monkeys or non-human primates was not associated with seroreactivity.ConclusionsThis analysis suggests that some zoonotic exposures that have been linked to EVD outbreaks can also be associated with EBOV GP seroreactivity in the absence of diagnosed EVD. Future investigations should seek to clarify the relationships between zoonotic exposures, seroreactivity, asymptomatic infection, and EVD.     

Intrinsic and extrinsic factors affecting dietary specialization in Neotropical frugivorous bats

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Analysis of Cathepsin and Furin Proteolytic Enzymes Involved in Viral Fusion Protein Activation in Cells of the Bat Reservoir Host

Bats of different species play a major role in the emergence and transmission of highly pathogenic viruses including Ebola virus, SARS-like coronavirus and the henipaviruses. These viruses require proteolytic activation of surface envelope glycoproteins needed for entry, and cellular cathepsins have been shown to be involved in proteolysis of glycoproteins from these distinct virus families. Very little is currently known about the available proteases in bats. To determine whether the utilization of cathepsins by bat-borne viruses is related to the nature of proteases in their natural hosts, we examined proteolytic processing of several viral fusion proteins in cells derived from two fruit bat species, Pteropus alecto and Rousettus aegyptiacus. Our work shows that fruit bat cells have homologs of cathepsin and furin proteases capable of cleaving and activating both the cathepsin-dependent Hendra virus F and the furin-dependent parainfluenza virus 5 F proteins. Sequence analysis comparing Pteropus alecto furin and cathepsin L to proteases from other mammalian species showed a high degree of conservation; however significant amino acid variation occurs at the C-terminus of Pteropus alecto furin. Further analysis of furin-like proteases from fruit bats revealed that these proteases are catalytically active and resemble other mammalian furins in their response to a potent furin inhibitor. However, kinetic analysis suggests that differences may exist in the cellular localization of furin between different species. Collectively, these results indicate that the unusual role of cathepsin proteases in the life cycle of bat-borne viruses is not due to the lack of active furin-like proteases in these natural reservoir species; however, differences may exist between furin proteases present in fruit bats compared to furins in other mammalian species, and these differences may impact protease usage for viral glycoprotein processing.     

Mapping Risk of Nipah Virus Transmission from Bats to Humans in Thailand

Nipah virus (NiV) is a zoonotic virus that can pose a serious threat to human and livestock health. Old-world fruit bats (Pteropus spp.) are the natural reservoir hosts for NiV, and Pteropus lylei, Lyle’s flying fox, is an important host of NiV in mainland Southeast Asia. NiV can be transmitted from bats to humans directly via bat-contaminated foods (i.e., date palm sap or fruit) or indirectly via livestock or other intermediate animal hosts. Here we construct risk maps for NiV spillover and transmission by combining ecological niche models for the P. lylei bat reservoir with other spatial data related to direct or indirect NiV transmission (livestock density, foodborne sources including fruit production, and human population). We predict the current and future (2050 and 2070) distribution of P. lylei across Thailand, Cambodia, and Vietnam. Our best-fit model predicted that central and western regions of Thailand and small areas in Cambodia are currently the most suitable habitats for P. lylei. However, due to climate change, the species range is predicted to expand to include lower northern, northeastern, eastern, and upper southern Thailand and almost all of Cambodia and lower southern Vietnam. This expansion will create additional risk areas for human infection from P. lylei in Thailand. Our combined predictive risk maps showed that central Thailand, inhabited by 2.3 million people, is considered highly suitable for the zoonotic transmission of NiV from P. lylei. These current and future NiV transmission risk maps can be used to prioritize sites for active virus surveillance and developing awareness and prevention programs to reduce the risk of NiV spillover and spread in Thailand.

     

Isolation of Genetically Diverse Marburg Viruses from Egyptian Fruit Bats

In July and September 2007, miners working in Kitaka Cave, Uganda, were diagnosed with Marburg hemorrhagic fever. The likely source of infection in the cave was Egyptian fruit bats (Rousettus aegyptiacus) based on detection of Marburg virus RNA in 31/611 (5.1%) bats, virus-specific antibody in bat sera, and isolation of genetically diverse virus from bat tissues. The virus isolates were collected nine months apart, demonstrating long-term virus circulation. The bat colony was estimated to be over 100,000 animals using mark and re-capture methods, predicting the presence of over 5,000 virus-infected bats. The genetically diverse virus genome sequences from bats and miners closely matched. These data indicate common Egyptian fruit bats can represent a major natural reservoir and source of Marburg virus with potential for spillover into humans.     

Multiple mortality events in bats: a global review

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Natural selection in the evolution of SARS-CoV-2 in bats created a generalist virus and highly capable human pathogen

Virus host shifts are generally associated with novel adaptations to exploit the cells of the new host species optimally. Surprisingly, Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) has apparently required little to no significant adaptation to humans since the start of the Coronavirus Disease 2019 (COVID-19) pandemic and to October 2020. Here we assess the types of natural selection taking place in Sarbecoviruses in horseshoe bats versus the early SARS-CoV-2 evolution in humans. While there is moderate evidence of diversifying positive selection in SARS-CoV-2 in humans, it is limited to the early phase of the pandemic, and purifying selection is much weaker in SARS-CoV-2 than in related bat Sarbecoviruses. In contrast, our analysis detects evidence for significant positive episodic diversifying selection acting at the base of the bat virus lineage SARS-CoV-2 emerged from, accompanied by an adaptive depletion in CpG composition presumed to be linked to the action of antiviral mechanisms in these ancestral bat hosts. The closest bat virus to SARS-CoV-2, RmYN02 (sharing an ancestor about 1976), is a recombinant with a structure that includes differential CpG content in Spike; clear evidence of coinfection and evolution in bats without involvement of other species. While an undiscovered “facilitating” intermediate species cannot be discounted, collectively, our results support the progenitor of SARS-CoV-2 being capable of efficient human–human transmission as a consequence of its adaptive evolutionary history in bats, not humans, which created a relatively generalist virus.

A study of the natural origins of SARS-CoV-2 reveals very little adaptive evolution occurring since it emerged in humans, but strong evolutionary signals in the bat virus lineage from which SARS-CoV-2 arose. Evolution in bats involved lineage-specific depletion of CpG nucleotides (linked to host anti-viral molecules), and clear evidence of recombination across these lineages, supporting bat host species’ influence on the ancestral viruses.     

COVID-19, media coverage of bats and related Web searches: a turning point for bat conservation?

1. SARS-CoV-2, the virus that caused the COVID-19 pandemic, is genomically similar to a SARS-like beta-coronavirus found in Asian rhinolophid bats. This evolutionary relationship impressed the global media, which then emphasised bats as key actors in the spillover that resulted in the pandemic. In this study, we highlight changes in the traditional and new media coverage of bats and in Internet search volumes that occurred since the beginning of the COVID-19 pandemic in 2020.
2. We analysed Google and Wikipedia searches for bats and coronaviruses in 21 countries and eight languages, as well as television broadcasts in the USA, some of which have global coverage, between January 2016 and December 2020. In January 2020, the amount of television news about bats boomed, and news associated with the term ‘bat’ shifted to COVID-19-related topics. A nearly identical pattern was observed in Google searches during 2020 at the global scale. The daily time series of television coverage and Internet search volumes on bats and coronavirus in the USA covaried in the first quarter of 2020, in line with the existence of a media bubble. Time-series analysis revealed that both the Google Trends index and visits to Wikipedia pages about bats boomed in early 2020, despite the fact that this time of year is usually characterised by low search volumes.
3. Media coverage emphasised, correctly or not, the role of bats in the COVID-19 pandemic and amplified public interest in bats worldwide. The public image of these mammals, in many cases threatened and important ecosystem service providers, was seriously compromised. We therefore recommend that policymakers and journalists prioritise scientifically accurate communication campaigns about bats, which would help counteract the surge in bat persecution, and leverage interest towards positive human–bat interactions.

     

Pteropus lylei primarily forages in residential areas in Kandal,Cambodia

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The Distribution of Henipaviruses in Southeast Asia and Australasia: Is Wallace’s Line a Barrier to Nipah Virus?

Nipah virus (NiV) (Genus Henipavirus) is a recently emerged zoonotic virus that causes severe disease in humans and has been found in bats of the genus Pteropus. Whilst NiV has not been detected in Australia, evidence for NiV-infection has been found in pteropid bats in some of Australia’s closest neighbours. The aim of this study was to determine the occurrence of henipaviruses in fruit bat (Family Pteropodidae) populations to the north of Australia. In particular we tested the hypothesis that Nipah virus is restricted to west of Wallace’s Line. Fruit bats from Australia, Papua New Guinea, East Timor and Indonesia were tested for the presence of antibodies to Hendra virus (HeV) and Nipah virus, and tested for the presence of HeV, NiV or henipavirus RNA by PCR. Evidence was found for the presence of Nipah virus in both Pteropus vampyrus and Rousettus amplexicaudatus populations from East Timor. Serology and PCR also suggested the presence of a henipavirus that was neither HeV nor NiV in Pteropus alecto and Acerodon celebensis. The results demonstrate the presence of NiV in the fruit bat populations on the eastern side of Wallace’s Line and within 500 km of Australia. They indicate the presence of non-NiV, non-HeV henipaviruses in fruit bat populations of Sulawesi and Sumba and possibly in Papua New Guinea. It appears that NiV is present where P. vampyrus occurs, such as in the fruit bat populations of Timor, but where this bat species is absent other henipaviruses may be present, as on Sulawesi and Sumba. Evidence was obtained for the presence henipaviruses in the non-Pteropid species R. amplexicaudatus and in A. celebensis. The findings of this work fill some gaps in knowledge in geographical and species distribution of henipaviruses in Australasia which will contribute to planning of risk management and surveillance activities.