Hibernating Little Brown Myotis (Myotis lucifugus) Show Variable Immunological Responses to White-Nose Syndrome

Moore, Marianne; Reichard, Jonathan D.; Murtha, Timothy D.; Nabhan, Morgan L.; Pian, Rachel E.; Ferreira, Jennifer S.; Kunz, Thomas

doi:10.1371/journal.pone.0058976

Cited by 49 publications

(45 citation statements)

References 62 publications

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“…Although P. destructans exhibits rapid growth and causes disease in susceptible species under the same environmental conditions, the fungus exhibited extremely low activity on tolerant bats, becoming virtually undetectable after 77 days of hibernation. Microhabitat selection during hibernation may explain variable outcomes in tolerant bats (Moore et al., 2013; Zukal et al., 2016), but our results do not support the hypothesis that tolerance to WNS is caused in part by host microhabitat selection (Hayman et al., 2016). Instead, our data suggest that tolerance is an inherent (i.e., genetic) trait of some species, implying that tolerance could potentially evolve in species that are currently susceptible.…”

Section: Discussionmentioning

confidence: 99%

The other white‐nose syndrome transcriptome: Tolerant and susceptible hosts respond differently to the pathogen Pseudogymnoascus destructans

Davy

Donaldson

Willis

et al. 2017

Ecology and Evolution

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Mitigation of emerging infectious diseases that threaten global biodiversity requires an understanding of critical host and pathogen responses to infection. For multihost pathogens where pathogen virulence or host susceptibility is variable, host–pathogen interactions in tolerant species may identify potential avenues for adaptive evolution in recently exposed, susceptible hosts. For example, the fungus Pseudogymnoascus destructans causes white‐nose syndrome (WNS) in hibernating bats and is responsible for catastrophic declines in some species in North America, where it was recently introduced. Bats in Europe and Asia, where the pathogen is endemic, are only mildly affected. Different environmental conditions among Nearctic and Palearctic hibernacula have been proposed as an explanation for variable disease outcomes, but this hypothesis has not been experimentally tested. We report the first controlled, experimental investigation of response to P. destructans in a tolerant, European species of bat (the greater mouse‐eared bat, Myotis myotis). We compared body condition, disease outcomes and gene expression in control (sham‐exposed) and exposed M. myotis that hibernated under controlled environmental conditions following treatment. Tolerant M. myotis experienced extremely limited fungal growth and did not exhibit symptoms of WNS. However, we detected no differential expression of genes associated with immune response in exposed bats, indicating that immune response does not drive tolerance of P. destructans in late hibernation. Variable responses to P. destructans among bat species cannot be attributed solely to environmental or ecological factors. Instead, our results implicate coevolution with the pathogen, and highlight the dynamic nature of the “white‐nose syndrome transcriptome.” Interspecific variation in response to exposure by the host (and possibly pathogen) emphasizes the importance of context in studies of the bat‐WNS system, and robust characterization of genetic responses to exposure in various hosts and the pathogen should precede any attempts to use particular bat species as generalizable “model hosts.”

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Section: Discussionmentioning

confidence: 99%

The other white‐nose syndrome transcriptome: Tolerant and susceptible hosts respond differently to the pathogen Pseudogymnoascus destructans

Davy

Donaldson

Willis

et al. 2017

Ecology and Evolution

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“…2012; Moore et al. 2013) and absence (Meteyer et al. 2009) of an inflammatory immune response to Pd during winter (see also the discussion in Brook and Dobson 2015).…”

Section: Discussionmentioning

confidence: 99%

Antibodies to Pseudogymnoascus destructans are not sufficient for protection against white‐nose syndrome

Johnson

Reeder

Lilley

et al. 2015

Ecology and Evolution

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White-nose syndrome (WNS) is a fungal disease caused by Pseudogymnoascus destructans (Pd) that affects bats during hibernation. Although millions of bats have died from WNS in North America, mass mortality has not been observed among European bats infected by the fungus, leading to the suggestion that bats in Europe are immune. We tested the hypothesis that an antibody-mediated immune response can provide protection against WNS by quantifying antibodies reactive to Pd in blood samples from seven species of free-ranging bats in North America and two free-ranging species in Europe. We also quantified antibodies in blood samples from little brown myotis (Myotis lucifugus) that were part of a captive colony that we injected with live Pd spores mixed with adjuvant, as well as individuals surviving a captive Pd infection trial. Seroprevalence of antibodies against Pd, as well as antibody titers, was greater among little brown myotis than among four other species of cave-hibernating bats in North America, including species with markedly lower WNS mortality rates. Among little brown myotis, the greatest titers occurred in populations occupying regions with longer histories of WNS, where bats lacked secondary symptoms of WNS. We detected antibodies cross-reactive with Pd among little brown myotis naïve to the fungus. We observed high titers among captive little brown myotis injected with Pd. We did not detect antibodies against Pd in Pd-infected European bats during winter, and titers during the active season were lower than among little brown myotis. These results show that antibody-mediated immunity cannot explain survival of European bats infected with Pd and that little brown myotis respond differently to Pd than species with higher WNS survival rates. Although it appears that some species of bats in North America may be developing resistance to WNS, an antibody-mediated immune response does not provide an explanation for these remnant populations.

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“…This antibody was generated using www.nature.com/scientificreports www.nature.com/scientificreports/ sera from ERBs, as well as sera from nine other bat species comprising four chiropteran families (manufacturer product datasheet). While this antibody has been confirmed to react with sera from these 10 chiropteran species and has been used with success to detect IgG antibodies in sera from >27 bat species comprising seven chiropteran families [48][49][50][51][52][53][54][55][56][57] , it is possible that its reactivity with IgG antibodies from divergent bat species might diminish. If this is the case, the concentration of secondary antibody may need to be optimized prior to testing a new species of bat or an alternative secondary antibody may need to be used.…”

Section: Filovirus Antigen Lysate Cutoffmentioning

confidence: 99%

Comparative analysis of serologic cross-reactivity using convalescent sera from filovirus-experimentally infected fruit bats

Schuh

Amman

Sealy

et al. 2019

Sci Rep

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With the exception of Reston and Bombali viruses, the marburgviruses and ebolaviruses (family Filoviridae ) cause outbreaks of viral hemorrhagic fever in sub-Saharan Africa. The Egyptian rousette bat (ERB) is a natural reservoir host for the marburgviruses and evidence suggests that bats are also natural reservoirs for the ebolaviruses. Although the search for the natural reservoirs of the ebolaviruses has largely involved serosurveillance of the bat population, there are no validated serological assays to screen bat sera for ebolavirus-specific IgG antibodies. Here, we generate filovirus-specific antisera by prime-boost immunization of groups of captive ERBs with all seven known culturable filoviruses. After validating a system of filovirus-specific indirect ELISAs utilizing infectious-based virus antigens for detection of virus-specific IgG antibodies from bat sera, we assess the level of serological cross-reactivity between the virus-specific antisera and heterologous filovirus antigens. This data is then used to generate a filovirus antibody fingerprint that can predict which of the filovirus species in the system is most antigenically similar to the species responsible for past infection. Our filovirus IgG indirect ELISA system will be a critical tool for identifying bat species with high ebolavirus seroprevalence rates to target for longitudinal studies aimed at establishing natural reservoir host-ebolavirus relationships.

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Hibernating Little Brown Myotis (Myotis lucifugus) Show Variable Immunological Responses to White-Nose Syndrome

Cited by 49 publications

References 62 publications

The other white‐nose syndrome transcriptome: Tolerant and susceptible hosts respond differently to the pathogen Pseudogymnoascus destructans

The other white‐nose syndrome transcriptome: Tolerant and susceptible hosts respond differently to the pathogen Pseudogymnoascus destructans

Antibodies to Pseudogymnoascus destructans are not sufficient for protection against white‐nose syndrome

Comparative analysis of serologic cross-reactivity using convalescent sera from filovirus-experimentally infected fruit bats

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