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AbstractSummit disease, in which infected hosts seek heights (gravitropism), first noted in modern times by nineteenth-century naturalists, has been shown to be induced by disparate pathogens ranging from viruses to fungi. Infection results in dramatic changes in normal activity patterns, and such parasite manipulation of host behaviors suggests a strong selection for convergent outcomes albeit evolved via widely divergent mechanisms. The two best-studied examples involve a subset of viral and fungal pathogens of insects that induce “summiting” in infected hosts. Summiting presumably functions as a means for increasing the dispersal of the pathogen, thus significantly increasing fitness. Here, we review current advances in our understanding of viral- and fungal-induced summit disease and the host behavioral manipulation involved. Viral genes implicated in this process include a host hormone-targeting ecdysteroid UDP-glucosyltransferase (apparently essential for mediating summit disease induced by some viruses but not all) and a protein tyrosine phosphatase, with light dependance implicated. For summit disease-causing fungi, though much remains obscure, targeting of molting, circadian rhythms, sleep, and responses to light patterns appear involved. Targeting of host neuronal pathways by summit-inducing fungi also appears to involve the production of effector molecules and secondary metabolites that affect host muscular, immune, and/or neurological processes. It is hypothesized that host brain structures, particularly Mushroom Bodies (no relation to the fungus itself), important for olfactory association learning and control of locomotor activity, are critical targets for mediating summiting during infection. This phenomenon expands the diversity of microbial pathogen-interactions and host dynamics. Key points•Summit disease or height seeking (gravitropism) results from viral and fungal pathogens manipulating insect host behaviors presumably to increase pathogen dispersal.•Insect baculoviruses and select fungal pathogens exhibit convergent evolution in host behavioral manipulation but use disparate molecular mechanisms.•Targets for affecting host behavior include manipulation of host hormones, feeding, locomotion, and immune, circadian, and neurological pathways.
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Serum proteomics reveals a tolerant immune phenotype across multiple pathogen taxa in wild vampire bats
Bats carry many zoonotic pathogens without showing pronounced pathology, with a few exceptions. The underlying immune tolerance mechanisms in bats remain poorly understood, although information-rich omics tools hold promise for identifying a wide range of immune markers and their relationship with infection. To evaluate the generality of immune responses to infection, we assessed the differences and similarities in serum proteomes of wild vampire bats (Desmodus rotundus) across infection status with five taxonomically distinct pathogens: bacteria (Bartonellaspp., hemoplasmas), protozoa (Trypanosoma cruzi), and DNA (herpesviruses) and RNA (alphacoronaviruses) viruses. From 19 bats sampled in 2019 in Belize, we evaluated the up- and downregulated immune responses of infected versus uninfected individuals for each pathogen. Using a high-quality genome annotation for vampire bats, we identified 586 serum proteins but found no evidence for differential abundance nor differences in composition between infected and uninfected bats. However, using receiver operating characteristic curves, we identified four to 48 candidate biomarkers of infection depending on the pathogen, including seven overlapping biomarkers (DSG2, PCBP1, MGAM, APOA4, DPEP1, GOT1, and IGFALS). Enrichment analysis of these proteins revealed that our viral pathogens, but not the bacteria or protozoa studied, were associated with upregulation of extracellular and cytoplasmatic secretory vesicles (indicative of viral replication) and downregulation of complement activation and coagulation cascades. Additionally, herpesvirus infection elicited a downregulation of leukocyte-mediated immunity and defense response but an upregulation of an inflammatory and humoral immune response. In contrast to our two viral infections, we found downregulation of lipid and cholesterol homeostasis and metabolism withBartonellaspp. infection, of platelet-dense and secretory granules with hemoplasma infection, and of blood coagulation pathways withT. cruziinfection. Despite the small sample size, our results suggest that vampire bats have a similar suite of immune mechanisms for viruses distinct from responses to the other pathogen taxa, and we identify potential biomarkers that can expand our understanding of pathogenesis of these infections in bats. By applying a proteomic approach to a multi-pathogen system in wild animals, our study provides a distinct framework that could be expanded across bat species to increase our understanding of how bats tolerate pathogens.
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- Award ID(s):
- 2213854
- PAR ID:
- 10509821
- Publisher / Repository:
- Frontiers
- Date Published:
- Journal Name:
- Frontiers in Immunology
- Volume:
- 14
- ISSN:
- 1664-3224
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fimmu.2023.1281732
