Abstract
Bacterial endosymbiosis has been instrumental in eukaryotic evolution, and includes both mutualistic, dependent and parasitic associations. Here we characterize an intracellular bacterium inhabiting the flagellated protist Bodo saltans (Kinetoplastida). We present a complete bacterial genome comprising a 1.39 Mb circular chromosome with 40.6% GC content. Fluorescent in situ hybridisation confirms that the endosymbiont is located adjacent to the nuclear membrane, and a detailed model of its intracellular niche is generated using serial block-face scanning electron microscopy. Phylogenomic analysis shows that the endosymbiont belongs to the Holosporales, most closely related to other α-proteobacterial endosymbionts of ciliates and amoebae. Comparative genomics indicates that it has a limited metabolism and is nutritionally host-dependent. However, the endosymbiont genome does encode diverse symbiont-specific secretory proteins, including a type VI secretion system and three separate toxin-antitoxin systems. We show that these systems are actively transcribed and hypothesize they represent a mechanism by which B. saltans becomes addicted to its endosymbiont. Consistent with this idea, attempts to cure Bodo of endosymbionts led to rapid and uniform cell death. This study adds kinetoplastid flagellates to ciliates and amoebae as hosts of Paracaedibacter-like bacteria, suggesting that these antagonistic endosymbioses became established very early in Eukaryotic evolution.
Highlights
Eukaryotes commonly live in intimate associations with microbes [1]
Analysis of prokaryotic rRNA reads identified four bacterial taxa; Klebsiella, Cupriavidus, Delftia, and an unknown bacterium with greatest sequence identity (98.6%) to uncultured bacterial sequences belonging to Family Paracaedibacteraceae, followed by Paracaedibacter (86.9%)
Given the symbiotic association of Family Paracaedibacteraceae with other protists and low sequence identity of this taxon with any defined genus, we propose that it represents the endosymbiont and hereafter refer to it as Candidatus Bodocaedibacter vickermanii (Cbv) sp. nov
Summary
Eukaryotes commonly live in intimate associations with microbes [1]. For microeukaryotes, intracellular microbes live as endosymbionts passing to progeny cells following fission [2], whereas endosymbionts of multicellular species live within host tissues and pass to progeny during reproduction, commonly inside eggs [3]. The defensive Burkholderia symbiont of the fungus Rhizopus is required for completion of the host’s sexual phase [10], a system mirroring the requirement of Asobara tabida wasps for one of their Wolbachia symbionts to complete oogenesis [11] In these cases, coadaptation over deep evolutionary time to the presence of the symbiont means that the host fails when the symbiont is removed, irrespective of any benefit the symbiont might confer. Three parasitic lineages, Novymonas, Phytomonas and the Strigomonadinae, are known to contain a β-proteobacterial symbionts [16,17,18,19] These symbionts are mutualistic, cooperating in various metabolic pathways that provide essential amino acids and vitamins to the host [20,21,22]. We tested whether Bodo was dependent on its symbiont, potentially driven by these toxin-antitoxin systems, showing that antibiotic treatment results in rapid death of B. saltans, consistent with an addiction hypothesis
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