Blood transcriptomes reveal novel parasitic zoonoses circulating in Madagascar's lemurs

Abstract

Zoonotic diseases are a looming threat to global populations, and nearly 75% of emerging infectious diseases can spread among wildlife, domestic animals and humans. A 'One World, One Health' perspective offers us an ideal framework for understanding and potentially mitigating the spread of zoonoses, and the island of Madagascar serves as a natural laboratory for conducting these studies. Rapid habitat degradation and climate change on the island are contributing to more frequent contact among humans, livestock and wildlife, increasing the potential for pathogen spillover events. Given Madagascar's long geographical isolation, coupled with recent and repeated introduction of agricultural and invasive species, it is likely that a number of circulating pathogens remain uncharacterized in lemur populations. Thus, it is imperative that new approaches be implemented for de novo pathogen discovery. To this end, we used non-targeted deep sequencing of blood transcriptomes from two species of critically endangered wild lemurs (Indri indri and Propithecus diadema) to characterize blood-borne pathogens. Our results show several undescribed vector-borne parasites circulating within lemurs, some of which may cause disease in wildlife, livestock and humans. We anticipate that advanced methods for de novo identification of unknown pathogens will have broad utility for characterizing other complex disease transmission systems.

Keywords: disease surveillance; metagenomics; next-generation; one health; wildlife; zoonotic.

Figure 1.

Map of Madagascar showing sampling localities for three Indri indri and three P. diadema screened for vector-borne pathogens. Grey shading in the country map identifies the Toamasina Province. Inset shows blue (I. indri) and red (P. diadema) sampling localities. Yellow shading defines the approximate boundary of the Ambatovy Minerals nickel mine site, an area where ongoing lemur health evaluations are being conducted by C.V.W., R.E.J., and J.R. Grey shading within inset identifies the extent of transitional and undisturbed primary forest.

Figure 2.

ML phylogenies of tick-borne parasites (Babesia (a), Borrelia (b) and Candidatus Neoehrlichia (c)) discovered through blood transcriptome sequencing. Taxa in bold were identified in I. indri and P. diadema (table 1; figure 1). Black circles identify statistically supported nodes (>75% bootstrap support). Asterisk indicates that similar genetic strains were found in multiple lemur individuals.