Mycobacterium leprae genomes from naturally infected nonhuman primates.

Tanvi P Honap,Koichi Suzuki,Anne C Stone,Michelle L Sauther,Ross P Tarara,Genevieve Housman,Luz-Andrea Pfister,Michael S Rosenberg,Frank P Cuozzo,Sarah Mills,Pamela L C Small

doi:10.1371/journal.pntd.0006190

Abstract

Leprosy is caused by the bacterial pathogens Mycobacterium leprae and Mycobacterium lepromatosis. Apart from humans, animals such as nine-banded armadillos in the Americas and red squirrels in the British Isles are naturally infected with M. leprae. Natural leprosy has also been reported in certain nonhuman primates, but it is not known whether these occurrences are due to incidental infections by human M. leprae strains or by M. leprae strains specific to nonhuman primates. In this study, complete M. leprae genomes from three naturally infected nonhuman primates (a chimpanzee from Sierra Leone, a sooty mangabey from West Africa, and a cynomolgus macaque from The Philippines) were sequenced. Phylogenetic analyses showed that the cynomolgus macaque M. leprae strain is most closely related to a human M. leprae strain from New Caledonia, whereas the chimpanzee and sooty mangabey M. leprae strains belong to a human M. leprae lineage commonly found in West Africa. Additionally, samples from ring-tailed lemurs from the Bezà Mahafaly Special Reserve, Madagascar, and chimpanzees from Ngogo, Kibale National Park, Uganda, were screened using quantitative PCR assays, to assess the prevalence of M. leprae in wild nonhuman primates. However, these samples did not show evidence of M. leprae infection. Overall, this study adds genomic data for nonhuman primate M. leprae strains to the existing M. leprae literature and finds that this pathogen can be transmitted from humans to nonhuman primates as well as between nonhuman primate species. While the prevalence of natural leprosy in nonhuman primates is likely low, nevertheless, future studies should continue to explore the prevalence of leprosy-causing pathogens in the wild.

Highlights

Leprosy has afflicted mankind for many millennia and remains a highly prevalent disease in economically underprivileged countries
Our results suggest that M. leprae strains can be transmitted from humans to nonhuman primates as well as between nonhuman primate species, and other primates might serve as a host for M. leprae in the wild
We assessed whether wild ring-tailed lemurs from Madagascar and chimpanzees from Uganda showed presence of M. leprae infection. These populations tested negative for M. leprae infection, further research on the prevalence of M. leprae in other wild nonhuman primate populations, especially in leprosy-endemic regions, is warranted

Summary

Introduction

Leprosy has afflicted mankind for many millennia and remains a highly prevalent disease in economically underprivileged countries. The disease has been almost eradicated from developed countries; approximately 250,000 new leprosy cases occur each year worldwide [1]. The majority of these cases occur in tropical and subtropical countries including India, Brazil, and the Central African Republic, thereby making leprosy a Neglected Tropical Disease [1]. Depending on the host immune response, the infection can progress to either the tuberculoid (paucibacillary) or lepromatous (multibacillary) form of leprosy. Tuberculoid leprosy is characterized by the presence of one or a few hypopigmented patches with loss of sensation and thickened peripheral nerves, whereas lepromatous leprosy results in systemic lesions which may become infiltrated with fluids [2]. The pathogen has a long incubation period that averages three to five years and can extend up to thirty years, which hampers early detection of infection

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