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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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Disentangling interactions among mercury, immunity and infection in a Neotropical bat community
Abstract Contaminants such as mercury are pervasive and can have immunosuppressive effects on wildlife. Impaired immunity could be important for forecasting pathogen spillover, as many land‐use changes that generate mercury contamination also bring wildlife into close contact with humans and domestic animals. However, the interactions among contaminants, immunity and infection are difficult to study in natural systems, and empirical tests of possible directional relationships remain rare.We capitalized on extreme mercury variation in a diverse bat community in Belize to test association among contaminants, immunity and infection. By comparing a previous dataset of bats sampled in 2014 with new data from 2017, representing a period of rapid agricultural land conversion, we first confirmed bat species more reliant on aquatic prey had higher fur mercury. Bats in the agricultural habitat also had higher mercury in recent years. We then tested covariation between mercury and cellular immunity and determined if such relationships mediated associations between mercury and bacterial pathogens. As bat ecology can dictate exposure to mercury and pathogens, we also assessed species‐specific patterns in mercury–infection relationships.Across the bat community, individuals with higher mercury had fewer neutrophils but not lymphocytes, suggesting stronger associations with innate immunity. However, the odds of infection for haemoplasmas andBartonellaspp. were generally lowest in bats with high mercury, and relationships between mercury and immunity did not mediate infection patterns. Mercury also showed species‐ and clade‐specific relationships with infection, being associated with especially low odds for haemoplasmas inPteronotus mesoamericanusandDermanura phaeotis. ForBartonellaspp., mercury was associated with particularly low odds of infection in the genusPteronotusbut high odds in the subfamily Stenodermatinae.Synthesis and application. Lower general infection risk in bats with high mercury despite weaker innate defense suggests contaminant‐driven loss of pathogen habitat (i.e. anemia) or vector mortality as possible causes. Greater attention to these potential pathways could help disentangle relationships among contaminants, immunity and infection in anthropogenic habitats and help forecast disease risks. Our results also suggest that contaminants may increase infection risk in some taxa but not others, emphasizing the importance of considering surveillance and management at different phylogenetic scales.
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- Award ID(s):
- 1716698
- PAR ID:
- 10452801
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Journal of Applied Ecology
- Volume:
- 58
- Issue:
- 4
- ISSN:
- 0021-8901
- Page Range / eLocation ID:
- p. 879-889
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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