Novel Trypanosomatid-Bacterium Association: Evolution of Endosymbiosis in Action

Abstract

We describe a novel symbiotic association between a kinetoplastid protist, Novymonas esmeraldas gen. nov., sp. nov., and an intracytoplasmic bacterium, “Candidatus Pandoraea novymonadis” sp. nov., discovered as a result of a broad-scale survey of insect trypanosomatid biodiversity in Ecuador. We characterize this association by describing the morphology of both organisms, as well as their interactions, and by establishing their phylogenetic affinities. Importantly, neither partner is closely related to other known organisms previously implicated in eukaryote-bacterial symbiosis. This symbiotic association seems to be relatively recent, as the host does not exert a stringent control over the number of bacteria harbored in its cytoplasm. We argue that this unique relationship may represent a suitable model for studying the initial stages of establishment of endosymbiosis between a single-cellular eukaryote and a prokaryote. Based on phylogenetic analyses, Novymonas could be considered a proxy for the insect-only ancestor of the dixenous genus Leishmania and shed light on the origin of the two-host life cycle within the subfamily Leishmaniinae.

Isolation of Novel Trypanosomatid, Zelonia australiensis sp. nov. (Kinetoplastida: Trypanosomatidae) Provides Support for a Gondwanan Origin of Dixenous Parasitism in the Leishmaniinae

“…Indeed, a Neotropical origin is supported by the evidence available, though the appearance of Leishmania probably occurred much earlier than the Neotropical hypothesis initially proposed (Fig 8) [3, 56]. The Neotropical origins theory is also supported by the limited range of the Paraleishmania which are restricted to the New World, and are basal to all Euleishmania [3, 6, 16] (Figs 7 and 8). The Multiple Origins hypothesis suggests the Euleishmania and Paraleishmania evolved on Gondwana prior to the opening of the Atlantic Ocean.…”

“…The parasite shows a high degree of pleomorphism in culture. This has been reported for other trypanosomatids, and limits the use of morphology for classification of these organisms [16, 101]. …”

“…costaricensis and Z . australiensis are presumably monoxenous trypanosomatids basal to all dixenous Leishmaniinae (Fig 6) [4, 16], and probably represent the nearest ancestors of a parasite that transitioned from a monoxenous to a dixenous life cycle [87]. The rigorous growth of Z .…”

“…seymouri also possesses an alternate hematophagous host [98]. While they are still considered monoxenous, and are continually grouped in basal clades to Leishmania [16, 17, 99] (Figs 6, 7 and 8), it is plausible that certain monoxenous Leishmaniinae are ancestors of transitional forms that did not complete the switch to a dixenous life cycle. Indeed, monoxenous trypanosomatids occasionally explore the dixenous niche based on multiple reports of infections involving animals and humans [98].…”

Development of a toolbox to dissect host-endosymbiont interactions and protein trafficking in the trypanosomatid Angomonas deanei

“…Whereas most trypanosomatids are nutritionally fastidious and have a strict requirement for heme and several amino acids, members of the Strigomonadinae can grow in defined media lacking heme and containing a reduced number of amino acids because many metabolites can be synthesized by the endosymbiont and delivered to the host [21–23]. Besides members of the Strigomonadinae, there is a single trypanosomatid species ( Novymonas esmeraldas ) that is known to have acquired bacterial endosymbionts independently [24]. …”