Host Diversity and Responses to Bat-Associated Viruses

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Animal Viruses".

Deadline for manuscript submissions: closed (28 February 2023) | Viewed by 25931

Special Issue Editors

Departments of Pathology, Urology and Oncology, The Johns Hopkins Medical Institutions, Baltimore, MD, USA
EcoHealth Alliance, 520 Eighth Avenue, Suite 1200, New York, NY 10018-6507, USA
Interests: Nipah virus; coronavirus; bats; ebola virus; One Health
Arthropod-borne and Infectious Diseases Laboratory, Department of Microbiology, Immunology and Pathology, Colorado State University, Collins, CO, USA
Interests: rodent- and bat-borne viruses
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear colleagues,

This Special Issue focuses on host–virus relationships—specifically, issues of host-breadth or plasticity, pathogenicity, and transmissibility of bat-associated viruses. Examples could include co-evolution of virus and host receptors, host innate and adaptive immune responses to viral infection, viral incidence or prevalence studies, comparative experimental studies using animal models or cell lines, and potential for human–animal transmission, in either direction. This Special Issue will be limited to original research, literature reviews with novel insights, and hypothesis-based manuscripts.

Dr. Jonathan Epstein
Dr. Tony Schountz
Guest Editors

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Published Papers (9 papers)

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Research

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14 pages, 3049 KiB  
Article
Genomic Comparisons of Alphacoronaviruses and Betacoronaviruses from Korean Bats
by Van Thi Lo, Sun Woo Yoon, Yong Gun Choi, Dae Gwin Jeong and Hye Kwon Kim
Viruses 2022, 14(7), 1389; https://0-doi-org.brum.beds.ac.uk/10.3390/v14071389 - 25 Jun 2022
Viewed by 1818
Abstract
Coronaviruses are well known as a diverse family of viruses that affect a wide range of hosts. Since the outbreak of severe acute respiratory syndrome, a variety of bat-associated coronaviruses have been identified in many countries. However, they do not represent all the [...] Read more.
Coronaviruses are well known as a diverse family of viruses that affect a wide range of hosts. Since the outbreak of severe acute respiratory syndrome, a variety of bat-associated coronaviruses have been identified in many countries. However, they do not represent all the specific geographic locations of their hosts. In this study, full-length genomes representing newly identified bat coronaviruses in South Korea were obtained using an RNA sequencing approach. The analysis, based on genome structure, conserved replicase domains, spike gene, and nucleocapsid genes revealed that bat Alphacoronaviruses are from three different viral species. Among them, the newly identified B20-97 strain may represent a new putative species, closely related to PEDV. In addition, the newly-identified MERS-related coronavirus exhibited shared genomic nucleotide identities of less than 76.4% with other Merbecoviruses. Recombination analysis and multiple alignments of spike and RBD amino acid sequences suggested that this strain underwent recombination events and could possibly use hDPP4 molecules as its receptor. The bat SARS-related CoV B20-50 is unlikely to be able to use hACE2 as its receptor and lack of an open reading frame in ORF8 gene region. Our results illustrate the diversity of coronaviruses in Korean bats and their evolutionary relationships. The evolution of the bat coronaviruses related ORF8 accessory gene is also discussed. Full article
(This article belongs to the Special Issue Host Diversity and Responses to Bat-Associated Viruses)
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17 pages, 5894 KiB  
Article
Histopathologic and Immunohistochemical Evaluation of Induced Lesions, Tissue Tropism and Host Responses following Experimental Infection of Egyptian Rousette Bats (Rousettus aegyptiacus) with the Zoonotic Paramyxovirus, Sosuga Virus
by Shannon G. M. Kirejczyk, Brian R. Amman, Amy J. Schuh, Tara K. Sealy, César G. Albariño, Jian Zhang, Corrie C. Brown and Jonathan S. Towner
Viruses 2022, 14(6), 1278; https://0-doi-org.brum.beds.ac.uk/10.3390/v14061278 - 12 Jun 2022
Cited by 4 | Viewed by 1955
Abstract
Ecological and experimental infection studies have identified Egyptian rousette bats (ERBs; Rousettus aegyptiacus: family Pteropodidae) as a reservoir host for the zoonotic rubula-like paramyxovirus Sosuga virus (SOSV). A serial sacrifice study of colony-bred ERBs inoculated with wild-type, recombinant SOSV identified small intestines [...] Read more.
Ecological and experimental infection studies have identified Egyptian rousette bats (ERBs; Rousettus aegyptiacus: family Pteropodidae) as a reservoir host for the zoonotic rubula-like paramyxovirus Sosuga virus (SOSV). A serial sacrifice study of colony-bred ERBs inoculated with wild-type, recombinant SOSV identified small intestines and salivary gland as major sites of viral replication. In the current study, archived formalin-fixed paraffin-embedded (FFPE) tissues from the serial sacrifice study were analyzed in depth—histologically and immunohistochemically, for SOSV, mononuclear phagocytes and T cells. Histopathologic lesion scores increased over time and viral antigen persisted in a subset of tissues, indicating ongoing host responses and underscoring the possibility of chronic infection. Despite the presence of SOSV NP antigen and villus ulcerations in the small intestines, there were only mild increases in mononuclear phagocytes and T cells, a host response aligned with disease tolerance. In contrast, there was a statistically significant, robust and targeted mononuclear phagocyte cell responses in the salivary glands at 21 DPI, where viral antigen was sparse. These findings may have broader implications for chiropteran–paramyxovirus interactions, as bats are hypothesized to be the ancestral hosts of this diverse virus family and for ERB immunology in general, as this species is also the reservoir host for the marburgviruses Marburg virus (MARV) and Ravn virus (RAVV) (family Filoviridae). Full article
(This article belongs to the Special Issue Host Diversity and Responses to Bat-Associated Viruses)
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13 pages, 2073 KiB  
Article
Evolution of TRIM5 and TRIM22 in Bats Reveals a Complex Duplication Process
by Alexandre P. Fernandes, Ana Águeda-Pinto, Ana Pinheiro, Hugo Rebelo and Pedro J. Esteves
Viruses 2022, 14(2), 345; https://0-doi-org.brum.beds.ac.uk/10.3390/v14020345 - 08 Feb 2022
Cited by 6 | Viewed by 2075
Abstract
The innate immunological response in mammals involves a diverse and complex network of many proteins. Over the last years, the tripartite motif-containing protein 5 (TRIM5) and 22 (TRIM22) have shown promise as restriction factors of a plethora of viruses that infect primates. Although [...] Read more.
The innate immunological response in mammals involves a diverse and complex network of many proteins. Over the last years, the tripartite motif-containing protein 5 (TRIM5) and 22 (TRIM22) have shown promise as restriction factors of a plethora of viruses that infect primates. Although there have been studies describing the evolution of these proteins in a wide range of mammals, no prior studies of the TRIM6/34/5/22 gene cluster have been performed in the Chiroptera order. Here, we provide a detailed analysis of the evolution of this gene cluster in several bat genomes. Examination of different yangochiroptera and yinpterochiroptera bat species revealed a dynamic history of gene expansion occurring in TRIM5 and TRIM22 genes. Multiple copies of TRIM5 were found in the genomes of several bats, demonstrating a very low degree of conservation in the synteny of this gene among species of the Chiroptera order. Our findings also reveal that TRIM22 is often found duplicated in yangochiroptera bat species, an evolutionary phenomenon not yet observed in any other lineages of mammals. In total, we identified 31 TRIM5 and 19 TRIM22 amino acids to be evolving under positive selection, with most of the residues being placed in the PRYSPRY domain, known to be responsible for binding to the viral capsid during restriction in the primate orthologous TRIM proteins. Altogether, our results help to shed light on the distinctive role of bats in nature as reservoirs of viruses, many of which have become threatening zoonotic diseases through virus spillover in the last decades. Full article
(This article belongs to the Special Issue Host Diversity and Responses to Bat-Associated Viruses)
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11 pages, 1271 KiB  
Article
Alphavirus Identification in Neotropical Bats
by Lucía Moreira Marrero, Germán Botto Nuñez, Sandra Frabasile and Adriana Delfraro
Viruses 2022, 14(2), 269; https://0-doi-org.brum.beds.ac.uk/10.3390/v14020269 - 28 Jan 2022
Cited by 1 | Viewed by 2952
Abstract
Alphaviruses (Togaviridae) are arthropod-borne viruses responsible for several emerging diseases, maintained in nature through transmission between hematophagous arthropod vectors and susceptible vertebrate hosts. Although bats harbor many species of viruses, their role as reservoir hosts in emergent zoonoses has been verified [...] Read more.
Alphaviruses (Togaviridae) are arthropod-borne viruses responsible for several emerging diseases, maintained in nature through transmission between hematophagous arthropod vectors and susceptible vertebrate hosts. Although bats harbor many species of viruses, their role as reservoir hosts in emergent zoonoses has been verified only in a few cases. With bats being the second most diverse order of mammals, their implication in arbovirus infections needs to be elucidated. Reports on arbovirus infections in bats are scarce, especially in South American indigenous species. In this work, we report the genomic detection and identification of two different alphaviruses in oral swabs from bats captured in Northern Uruguay. Phylogenetic analysis identified Río Negro virus (RNV) in two different species: Tadarida brasiliensis (n = 6) and Myotis spp. (n = 1) and eastern equine encephalitis virus (EEEV) in Myotis spp. (n = 2). Previous studies of our group identified RNV and EEEV in mosquitoes and horse serology, suggesting that they may be circulating in enzootic cycles in our country. Our findings reveal that bats can be infected by these arboviruses and that chiropterans could participate in the viral natural cycle as virus amplifiers or dead-end hosts. Further studies are warranted to elucidate the role of these mammals in the biological cycle of these alphaviruses in Uruguay. Full article
(This article belongs to the Special Issue Host Diversity and Responses to Bat-Associated Viruses)
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12 pages, 633 KiB  
Article
Serological Positivity against Selected Flaviviruses and Alphaviruses in Free-Ranging Bats and Birds from Costa Rica Evidence Exposure to Arboviruses Seldom Reported Locally in Humans
by Daniel Felipe Barrantes Murillo, Marta Piche-Ovares, José Carlos Gamboa-Solano, Luis Mario Romero, Claudio Soto-Garita, Alejandro Alfaro-Alarcón and Eugenia Corrales-Aguilar
Viruses 2022, 14(1), 93; https://0-doi-org.brum.beds.ac.uk/10.3390/v14010093 - 06 Jan 2022
Cited by 4 | Viewed by 2152
Abstract
Arboviruses have two ecological transmission cycles: sylvatic and urban. For some, the sylvatic cycle has not been thoroughly described in America. To study the role of wildlife in a putative sylvatic cycle, we sampled free-ranging bats and birds in two arbovirus endemic locations [...] Read more.
Arboviruses have two ecological transmission cycles: sylvatic and urban. For some, the sylvatic cycle has not been thoroughly described in America. To study the role of wildlife in a putative sylvatic cycle, we sampled free-ranging bats and birds in two arbovirus endemic locations and analyzed them using molecular, serological, and histological methods. No current infection was detected, and no significant arbovirus-associated histological changes were observed. Neutralizing antibodies were detected against selected arboviruses. In bats, positivity in 34.95% for DENV-1, 16.26% for DENV-2, 5.69% for DENV-3, 4.87% for DENV-4, 2.43% for WNV, 4.87% for SLEV, 0.81% for YFV, 7.31% for EEEV, and 0.81% for VEEV was found. Antibodies against ZIKV were not detected. In birds, PRNT results were positive against WNV in 0.80%, SLEV in 5.64%, EEEV in 8.4%, and VEEV in 5.63%. An additional retrospective PRNT analysis was performed using bat samples from three additional DENV endemic sites resulting in a 3.27% prevalence for WNV and 1.63% for SLEV. Interestingly, one sample resulted unequivocally WNV positive confirmed by serum titration. These results suggest that free-ranging bats and birds are exposed to not currently reported hyperendemic-human infecting Flavivirus and Alphavirus; however, their role as reservoirs or hosts is still undetermined. Full article
(This article belongs to the Special Issue Host Diversity and Responses to Bat-Associated Viruses)
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19 pages, 2344 KiB  
Article
Tolerance and Persistence of Ebola Virus in Primary Cells from Mops condylurus, a Potential Ebola Virus Reservoir
by Marcel Bokelmann, Uwe Vogel, Franka Debeljak, Ariane Düx, Silke Riesle-Sbarbaro, Angelika Lander, Annette Wahlbrink, Nicole Kromarek, Stuart Neil, Emmanuel Couacy-Hymann, Joseph Prescott and Andreas Kurth
Viruses 2021, 13(11), 2186; https://0-doi-org.brum.beds.ac.uk/10.3390/v13112186 - 29 Oct 2021
Cited by 6 | Viewed by 2661
Abstract
Although there have been documented Ebola virus disease outbreaks for more than 40 years, the natural reservoir host has not been identified. Recent studies provide evidence that the Angolan free-tailed bat (Mops condylurus), an insectivorous microbat, is a possible ebolavirus reservoir. [...] Read more.
Although there have been documented Ebola virus disease outbreaks for more than 40 years, the natural reservoir host has not been identified. Recent studies provide evidence that the Angolan free-tailed bat (Mops condylurus), an insectivorous microbat, is a possible ebolavirus reservoir. To investigate the potential role of this bat species in the ecology of ebolaviruses, replication, tolerance, and persistence of Ebola virus (EBOV) were investigated in 10 different primary bat cell isolates from M. condylurus. Varying EBOV replication kinetics corresponded to the expression levels of the integral membrane protein NPC1. All primary cells were highly tolerant to EBOV infection without cytopathic effects. The observed persistent EBOV infection for 150 days in lung primary cells, without resultant selective pressure leading to virus mutation, indicate the intrinsic ability of EBOV to persist in this bat species. These results provide further evidence for this bat species to be a likely reservoir of ebolaviruses. Full article
(This article belongs to the Special Issue Host Diversity and Responses to Bat-Associated Viruses)
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Review

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11 pages, 760 KiB  
Review
Different but Not Unique: Deciphering the Immunity of the Jamaican Fruit Bat by Studying Its Viriome
by Quinnlan David, Tony Schountz, Martin Schwemmle and Kevin Ciminski
Viruses 2022, 14(2), 238; https://0-doi-org.brum.beds.ac.uk/10.3390/v14020238 - 25 Jan 2022
Cited by 3 | Viewed by 3177
Abstract
A specialized and fine-tuned immune response of bats upon infection with viruses is believed to provide the basis for a “friendly” coexistence with these pathogens, which are often lethal for humans and other mammals. First insights into the immunity of bats suggest that [...] Read more.
A specialized and fine-tuned immune response of bats upon infection with viruses is believed to provide the basis for a “friendly” coexistence with these pathogens, which are often lethal for humans and other mammals. First insights into the immunity of bats suggest that bats have evolved to possess their own strategies to cope with viral infections. Yet, the molecular details for this innocuous coexistence remain poorly described and bat infection models are the key to unveiling these secrets. In Jamaican fruit bats (Artibeus jamaicensis), a New World bat species, infection experiments with its (putative) natural viral pathogens Tacaribe virus (TCRV), rabies virus (RABV), and the bat influenza A virus (IAV) H18N11, have contributed to an accurate, though still incomplete, representation of the bat-imposed immunity. Surprisingly, though many aspects of their innate and adaptive immune responses differ from that of the human immune response, such as a contraction of the IFN locus and reduction in the number of immunoglobulin subclasses, variations could also be observed between Jamaican fruit bats and other bat species. Full article
(This article belongs to the Special Issue Host Diversity and Responses to Bat-Associated Viruses)
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13 pages, 611 KiB  
Review
Exploring the Role of Innate Lymphocytes in the Immune System of Bats and Virus-Host Interactions
by Wan Rong Sia, Yichao Zheng, Fei Han, Shiwei Chen, Shaohua Ma, Lin-Fa Wang and Edwin Leeansyah
Viruses 2022, 14(1), 150; https://0-doi-org.brum.beds.ac.uk/10.3390/v14010150 - 14 Jan 2022
Cited by 8 | Viewed by 5908
Abstract
Bats are reservoirs of a large number of viruses of global public health significance, including the ancestral virus for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and the causative agent of coronavirus disease 2019 (COVID-19). Although bats are natural carriers of multiple pathogenic [...] Read more.
Bats are reservoirs of a large number of viruses of global public health significance, including the ancestral virus for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and the causative agent of coronavirus disease 2019 (COVID-19). Although bats are natural carriers of multiple pathogenic viruses, they rarely display signs of disease. Recent insights suggest that bats have a more balanced host defense and tolerance system to viral infections that may be linked to the evolutionary adaptation to powered flight. Therefore, a deeper understanding of bat immune system may provide intervention strategies to prevent zoonotic disease transmission and to identify new therapeutic targets. Similar to other eutherian mammals, bats have both innate and adaptive immune systems that have evolved to detect and respond to invading pathogens. Bridging these two systems are innate lymphocytes, which are highly abundant within circulation and barrier tissues. These cells share the characteristics of both innate and adaptive immune cells and are poised to mount rapid effector responses. They are ideally suited as the first line of defense against early stages of viral infections. Here, we will focus on the current knowledge of innate lymphocytes in bats, their function, and their potential role in host–pathogen interactions. Moreover, given that studies into bat immune systems are often hindered by a lack of bat-specific research tools, we will discuss strategies that may aid future research in bat immunity, including the potential use of organoid models to delineate the interplay between innate lymphocytes, bat viruses, and host tolerance. Full article
(This article belongs to the Special Issue Host Diversity and Responses to Bat-Associated Viruses)
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Other

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8 pages, 1722 KiB  
Brief Report
Evolution of CCR5 and CCR2 Genes in Bats Showed Multiple Independent Gene Conversion Events
by Alexandre P. Fernandes, Ana Águeda-Pinto, Ana Pinheiro, Hugo Rebelo and Pedro J. Esteves
Viruses 2022, 14(2), 169; https://0-doi-org.brum.beds.ac.uk/10.3390/v14020169 - 18 Jan 2022
Viewed by 1550
Abstract
Chemokine receptors are an important determinant for the infectiousness of different pathogens, which are able to target the host cells by binding to the extracellular domains of these proteins. This is the mechanism of infection of HIV-1, among other concerning human diseases. Over [...] Read more.
Chemokine receptors are an important determinant for the infectiousness of different pathogens, which are able to target the host cells by binding to the extracellular domains of these proteins. This is the mechanism of infection of HIV-1, among other concerning human diseases. Over the past years, it has been shown that two chemokine receptors, CCR2 and CCR5, have been shaped by events of gene conversion in different mammalian lineages, which has been linked to a possible selective advantage against pathogens. Here, by taking advantage of available bat genomes, we present the first insight of CCR2 and CCR5 evolution within the Chiroptera order. In total, four independent events of recombination between CCR2 and CCR5 were detected: two in a single species, Miniopterus natalensis; one in two species from the Rhinolophoidea superfamily; and one in four species from the Pteropodidae family. The regions affected by the gene conversions were generally extensive and always encompassed extracellular domains. Overall, we demonstrate that CCR2 and CCR5 have been subject to extensive gene conversion in multiple species of bats. Considering that bats are known to be large reservoirs of virus in nature, these results might indicate that chimeric CCR2-CCR5 genes might grant some bat species a selective advantage against viruses that rely in the extracellular portions of either CCR2 or CCR5 as gateways into the cell. Full article
(This article belongs to the Special Issue Host Diversity and Responses to Bat-Associated Viruses)
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