Temporal patterns of vampire bat rabies and host connectivity in Belize

Becker, Daniel J.; Broos, Alice; Bergner, Laura M.; Meza, Diana K.; Simmons, Nancy B.; Fenton, M. Brock; Altizer, Sonia; Streicker, Daniel G.

doi:10.1111/tbed.13754

Cited by 16 publications

(16 citation statements)

References 76 publications

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“…As part of an ongoing longitudinal study (Becker et al, 2020b), we sampled vampire bats in April 2019 in the Lamanai Archeological Reserve, northern Belize. This same population was sampled in 2015 for our earlier proteomic analysis (Neely et al, 2020).…”

Section: Methodsmentioning

confidence: 99%

Serum proteomics identifies immune pathways and candidate biomarkers of coronavirus infection in wild vampire bats

Becker

Lei

Janech

et al. 2022

Preprint

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The apparent ability of bats to harbor many virulent viruses without showing disease is likely driven by distinct immune responses that coevolved with mammalian flight and the exceptional longevity of this order. Yet our understanding of the immune mechanisms of viral tolerance is restricted to a small number of bat-virus relationships and remains poor for coronaviruses (CoVs), despite their relevance to human health. Proteomics holds particular promise for illuminating the immune factors involved in bat responses to infection, because it can accommodate especially low sample volumes (e.g., sera) and thus can be applied to both large and small bat species as well as in longitudinal studies where lethal sampling is necessarily limited. Further, as the serum proteome includes proteins secreted from not only blood cells but also proximal organs, it provides a more general characterization of immune proteins. Here, we expand our recent work on the serum proteome of wild vampire bats (Desmodus rotundus) to better understand CoV pathogenesis. Across 19 bats sampled in 2019 in northern Belize with available sera, we detected CoVs in oral or rectal swabs from four individuals (21.1% positivity). Phylogenetic analyses identified all vampire bat sequences as novel α-CoVs most closely related to known human CoVs. Across 586 identified serum proteins, we found no strong differences in protein composition nor abundance between uninfected and infected bats. However, receiver operating characteristic curve analyses identified seven to 32 candidate biomarkers of CoV infection, including AHSG, C4A, F12, GPI, DSG2, GSTO1, and RNH1. Enrichment analyses using these protein classifiers identified downregulation of complement, regulation of proteolysis, immune effector processes, and humoral immunity in CoV-infected bats alongside upregulation of neutrophil immunity, overall granulocyte activation, myeloid cell responses, and glutathione processes. Such results denote a mostly cellular immune response of vampire bats to CoV infection and identify putative biomarkers that could provide new insights into CoV pathogenesis in wild and experimental populations. More broadly, applying a similar proteomic approach across diverse bat species and to distinct life history stages in target species could improve our understanding of the immune mechanisms by which wild bats tolerate viruses.

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Section: Methodsmentioning

confidence: 99%

Serum proteomics identifies immune pathways and candidate biomarkers of coronavirus infection in wild vampire bats

Becker

Lei

Janech

et al. 2022

Preprint

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“…These land-use changes have fragmented previously intact forest and have provided vampire bats with an abundant prey in the form of livestock . In recent years (2016 onward), rabies outbreaks in domestic animals have increased across Belize and in Orange Walk District, and virus isolates from livestock have been characterized as vampire bat-associated variants . Although we are unaware of other viral detection efforts in vampire bats in Belize, this species has tested positive elsewhere in Central and South America for adenoviruses, coronaviruses, flaviviruses, hantaviruses, herpesviruses, and paramyxoviruses, as well as for antibodies against henipavirus-like viruses. ,− …”

Section: Methodsmentioning

confidence: 99%

Surveying the Vampire Bat (Desmodus rotundus) Serum Proteome: A Resource for Identifying Immunological Proteins and Detecting Pathogens

et al. 2021

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Bats are increasingly studied as model systems for longevity and as natural hosts for some virulent viruses. Yet the ability to characterize immune mechanisms of viral tolerance and to quantify infection dynamics in wild bats is often limited by small sample volumes and few species-specific reagents. Here, we demonstrate how proteomics can overcome these limitations by using data-independent acquisition-based shotgun proteomics to survey the serum proteome of 17 vampire bats (Desmodus rotundus) from Belize. Using just 2 μL of sample and relatively short separations of undepleted serum digests, we identified 361 proteins across 5 orders of magnitude. Levels of immunological proteins in vampire bat serum were then compared to human plasma via published databases. Of particular interest were antiviral and antibacterial components, circulating 20S proteasome complex and proteins involved in redox activity. Lastly, we used known virus proteomes to putatively identify Rh186 from Macacine herpesvirus 3 and ORF1a from Middle East respiratory syndrome-related coronavirus, indicating that mass spectrometry-based techniques show promise for pathogen detection. Overall, these results can be used to design targeted mass-spectrometry assays to quantify immunological markers and detect pathogens. More broadly, our findings also highlight the application of proteomics in advancing wildlife immunology and pathogen surveillance.

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“…During April and May in 2017 and 2018, we sampled 160 bats from 26 species in the Orange Walk District of Belize (Herrera et al, 2018;Becker et al, 2020aBecker et al, , 2021. Bats were captured using mist nets (monitored continuously from approximately 19:00 h to 22:00 h) and harp traps (monitored every half-hour from 18:00 h to 22:00 h and then at 05:00 h the following morning); all individuals were identified to species based on morphology (Reid, 1997).…”

Section: Materials and Methods Bat Samplingmentioning

confidence: 99%

Body size affects immune cell proportions in birds and non-volant mammals, but not bats

Ruhs

Becker

Oakey

et al. 2021

Journal of Experimental Biology

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Powered flight has evolved several times in vertebrates and constrains morphology and physiology in ways that likely have shaped how organisms cope with infections. Some of these constraints likely have impacts on aspects of immunology, such that larger fliers might prioritize risk reduction and safety. Addressing how the evolution of flight may have driven relationships between body size and immunity could be particularly informative for understanding the propensity of some taxa to harbor many virulent and sometimes zoonotic pathogens without showing clinical disease. Here, we used a comparative framework to quantify scaling relationships between body mass and the proportions of two types of white blood cells--lymphocytes, and granulocytes (neutr-/heterophils)--across 63 bat species, 400 bird species, and 251 non-volant mammal species. By using phylogenetically-informed statistical models on field-collected data from wild Neotropical bats and from captive bats, non-volant mammals and birds, we show that lymphocyte and neutrophil proportions do not vary systematically with body mass among bats. In contrast, larger birds and non-volant mammals have disproportionately higher granulocyte proportions than expected for their body size. Our inability to distinguish bat lymphocyte scaling from birds and bat granulocyte scaling from all other taxa suggest there may be other ecological explanations (i.e. not flight-related) for the cell proportion scaling patterns. Future comparative studies of wild bats, birds, and non-volant mammals of similar body mass should aim to further differentiate evolutionary effects and other aspects of life history on immune defense and its role in tolerance of (zoonotic) infections.

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Temporal patterns of vampire bat rabies and host connectivity in Belize

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 16 publications

References 76 publications

Serum proteomics identifies immune pathways and candidate biomarkers of coronavirus infection in wild vampire bats

Serum proteomics identifies immune pathways and candidate biomarkers of coronavirus infection in wild vampire bats

Surveying the Vampire Bat (Desmodus rotundus) Serum Proteome: A Resource for Identifying Immunological Proteins and Detecting Pathogens

Body size affects immune cell proportions in birds and non-volant mammals, but not bats

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