Fly iDNA suggests strict reliance of the causative agent of sylvatic anthrax on rainforest ecosystems

Abstract

Metabarcoding of invertebrate‐derived DNA (iDNA) is increasingly used to describe vertebrate diversity in terrestrial ecosystems. Fly iDNA has also shown potential as a tool for detecting pathogens. Combining these approaches makes fly iDNA a promising tool for understanding the ecology and distribution of novel pathogens or emerging infectious diseases. Here, we use fly iDNA to explore the geographic distribution of Bacillus cereus biovar anthracis (Bcbva) along a gradient from the forest within Taï National Park, Côte d'Ivoire, out to surrounding villages. We tested fly pools (N = 100 pools of 5 flies) collected in the forest (N = 25 pools), along the forest edge (N = 50 pools), and near surrounding villages (N = 25 pools) for Bcbva. Using the same iDNA, we sought to reconstruct fly and mammal communities with metabarcoding, with the aim of investigating potential links with Bcbva detection. We detected Bcbva in 5/100 fly pools and positivity varied significantly across the habitat types (forest = 4/25, edge = 1/50, village = 0/25). It was possible to culture Bcbva from all positive fly pools, confirming their positivity, while sequencing of their whole genomes revealed a considerable portion of known genomic diversity for this pathogen. iDNA generated data about the mammal and fly communities in these habitats, revealing the highest mammal diversity in the forest and considerable changes in fly community composition along the gradient. Bcbva host range estimates from fly iDNA were largely identical to the results of long‐term carcass monitoring efforts in the region. We show that fly iDNA can generate data on the geographic distribution and host range of a pathogen at kilometer scales, as well as reveal the pathogen's phylogenetic diversity. Our results highlight the power of fly iDNA for mammal biomonitoring and pathogen surveillance.

Genomic and Phylogenetic Analysis of Bacillus cereus Biovar anthracis Isolated from Archival Bone Samples Reveals Earlier Natural History of the Pathogen

“…SNP analysis of the virulence plasmids was unable to group strains isolated from the same animals, while chromosomal analysis grouped strains from the same individual primate closely. These primate strains were interspersed with strains isolated from flies (Calliphoridae) collected in traps, supporting the hypothesis that flies are active spreaders of Bcbva in the forest [12,[22][23][24].…”

Introduction to special issue: Advancing disease ecology through eDNA monitoring of infectious agents

“…Using molecular methods to survey parasites and pathogens from environmental samples has the potential to complement conventional methods and ameliorate some of the aforementioned challenges. Environmental DNA sequencing methods can improve our understanding of the spatiotemporal dynamics of pathogens and parasites across a diversity of systems by enabling more geographically widespread sampling (Jahan et al, 2023;Sieber et al, 2023;Young et al, 2023). The high frequency of surveillance with eDNA can lead to both the rapid update of genetic databases and increased effectiveness of conservation and management plans.…”

“…In addition to monitoring the distributions of pathogens across large aquatic systems, DNA sequencing has also been applied to monitor the pathogen and mammal diversity of Côte d'Ivoire. Jahan et al (2023) highlighted a major obstacle to using traditional camera trap methods to monitor wildlife diseases was that only animals with extremely visible disease symptoms were observed. Using DNA obtained from flies (Families: Calliphoridae and Sarcophagidae), an emerging form of anthrax caused by Bacillus cereus biovar anthracis (Bcbva) was tracked along a forest-to-village gradient in the Taï National Park.…”

“…Positive detections of Bcbva were associated with higher rates of fly and mammal diversity, which occurred in forested areas. By taking advantage of when nonvector animals come into contact with animals or their by-products, Jahan et al (2023) revealed new phylogenetic diversity of Bcbva and generated cooccurrence data on the rapidly changing geographic ranges of both host and pathogen. Young et al (2023) added an extra dimension to a large-scale metabarcoding project by assessing whether diet facilitated protozoan infection of the European turtle dove, Streptopelia turtur.…”

“…By taking advantage of when nonvector animals come into contact with animals or their by‐products, Jahan et al. (2023) revealed new phylogenetic diversity of Bcbva and generated co‐occurrence data on the rapidly changing geographic ranges of both host and pathogen.…”