Phylogenomic analysis supports Mycobacterium tuberculosis transmission between humans and elephants
Rajesh Man Rajbhandari1,2,3,4, Rajindra Napit4, Prajwol Manandhar4
1Departamento de Biologia, Faculdade de Ciencias da Universidade do Porto, Porto, Portugal.
Introduction:
Tuberculosis is an infectious disease caused by a group of acid-fast bacilli known as Mycobacterium tuberculosis complex (MTC), which has a major impact on humans. Transmission of MTC across the human-animal interface has been demonstrated by several studies. However, the reverse zoonotic transmission from humans to animals (zooanthroponosis) has often been neglected.
Methods:
In this study, we used Nanopore MinION and Illumina MiSeq approaches to sequence the whole genome of M. tuberculosis strains isolated from two deceased Asian elephants (Elephas maximus) and one human in Chitwan, Nepal. The evolutionary relationships and drug resistance capacity of these strains were assessed using the whole genome data generated by the stand-alone tool Tb-Profiler. Phylogenomic trees were also constructed using a non-synonymous SNP alignment of 2,596 bp, including 94 whole genome sequences representative of the previously described M. tuberculosis lineages from elephants worldwide (lineages 1 and 4) and from humans in Nepal (lineages 1, 2 and 3).
Results And Discussion:
The new genomes achieved an average coverage of 99.6%, with an average depth of 55.67x. These M. tuberculosis strains belong to lineage 1 (elephant DG), lineage 2 (elephant PK) and lineage 4 (human), and none of them were found to have drug-resistant variants. The elephant-derived isolates were evolutionarily closely related to human-derived isolates previously described in Nepal, both in lineages 1 and 2, providing additional support for zooanthroponosis or bidirectional transmission between humans and elephants. The human-derived isolate clustered together with other published human isolates from Argentina, Russia and the United Kingdom in the lineage 4 clade. This complex multi-pathogen, multi-host system is challenging and highlights the need for a One Health approach to tuberculosis prevention and control at human-animal interface, particularly in regions where human tuberculosis is highly endemic.
Insights
Reverse zoonotic transmission of tuberculosis (Mycobacterium tuberculosis complex) from humans to elephants was investigated. Elephant and human isolates were closely related, supporting human-to-elephant transmission and highlighting the need for a One Health approach.
Area of Science:
- Genomics
- Epidemiology
- One Health
Background:
- Tuberculosis, caused by Mycobacterium tuberculosis complex (MTC), impacts humans globally.
- Transmission of MTC between humans and animals is documented, but reverse zoonotic transmission (zooanthroponosis) is less understood.
- Asian elephants (Elephas maximus) are susceptible to MTC infections.
Purpose of the Study:
- To investigate the potential for zooanthroponosis of MTC in Nepal.
- To determine the evolutionary relationships and drug resistance profiles of MTC strains from elephants and humans.
- To assess the implications for tuberculosis control at the human-animal interface.
Main Methods:
- Whole genome sequencing of MTC strains from two Asian elephants and one human using Nanopore MinION and Illumina MiSeq.
- Phylogenomic analysis using non-synonymous single nucleotide polymorphism (SNP) alignment.
- Drug resistance variant analysis using Tb-Profiler.
Main Results:
- MTC strains belonged to lineage 1 (elephant DG), lineage 2 (elephant PK), and lineage 4 (human).
- No drug-resistant variants were detected in the sequenced MTC strains.
- Elephant-derived MTC isolates were evolutionarily closely related to human-derived isolates from Nepal (lineages 1 and 2), supporting zooanthroponosis.
- The human-derived MTC isolate clustered with international human isolates in lineage 4.
Conclusions:
- The findings provide evidence for zooanthroponosis or bidirectional transmission of MTC between humans and elephants in Nepal.
- The complex host-pathogen dynamics necessitate a One Health strategy for tuberculosis prevention and control.
- Integrated surveillance and control measures are crucial, especially in regions with high human tuberculosis prevalence.
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