Abstract
Apicomplexa is a diverse protistan phylum composed almost exclusively of metazoan-infecting parasites, including the causative agents of malaria, cryptosporidiosis, and toxoplasmosis. A single apicomplexan genus, Nephromyces, was described in 2010 as a mutualist partner to its tunicate host. Here we present genomic and transcriptomic data from the parasitic sister species to this mutualist, Cardiosporidium cionae, and its associated bacterial endosymbiont. Cardiosporidium cionae and Nephromyces both infect tunicate hosts, localize to similar organs within these hosts, and maintain bacterial endosymbionts. Though many other protists are known to harbor bacterial endosymbionts, these associations are completely unknown in Apicomplexa outside of the Nephromycidae clade. Our data indicate that a vertically transmitted α-proteobacteria has been retained in each lineage since Nephromyces and Cardiosporidium diverged. This α-proteobacterial endosymbiont has highly reduced metabolic capabilities, but contributes the essential amino acid lysine, and essential cofactor lipoic acid to C. cionae. This partnership likely reduces resource competition with the tunicate host. However, our data indicate that the contribution of the single α-proteobacterial endosymbiont in C. cionae is minimal compared to the three taxa of endosymbionts present in the Nephromyces system, and is a potential explanation for the virulence disparity between these lineages.
Highlights
Apicomplexa includes a multitude of highly virulent pathogenic organisms, such as Plasmodium falciparum, Cryptosporidium parvum, and Toxoplasma gondii, the causative agents of malaria, cryptosporidiosis, and toxoplasmosis, respectively
As part of a larger investigation of the Nephromycidae, here we focus on characterizing the role of the bacterial endosymbiont reported in C. cionae (Ciancio et al, 2008)
The remaining contigs that were classified by CAT were either unclassified or identified as contamination from a variety of marine organisms, bacteria and other protists
Summary
Apicomplexa includes a multitude of highly virulent pathogenic organisms, such as Plasmodium falciparum, Cryptosporidium parvum, and Toxoplasma gondii, the causative agents of malaria, cryptosporidiosis, and toxoplasmosis, respectively. Despite the high pathogenicity and parasitic adaptations of many members, questions have emerged over whether Apicomplexa is an entirely parasitic group Though this sentiment has long been mentioned in publications (Roos, 2005; Morrison, 2009; Gubbels and Duraisingh, 2012; Woo et al, 2015; Votýpka et al, 2016; McFadden and Yeh, 2017; Mathur et al, 2018), the current evidence suggests that the interactions between apicomplexans and their hosts are far more varied than previously recognized. Bacterial endosymbionts are frequently sequestered to specific structures or tissues, but in protists they must reside directly in the cytoplasm, making these associations far more intimate (Nowack and Melkonian, 2010) Though these interactions appear beneficial, endosymbiosis is rooted in conflict (Keeling and McCutcheon, 2017; McCutcheon et al, 2019). The maintenance of bacterial endosymbionts could be reducing host dependency and resource competition by providing novel biosynthetic pathways, thereby reducing virulence in this unique lineage
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