Metabolic Contributions of an Alphaproteobacterial Endosymbiont in the Apicomplexan Cardiosporidium cionae

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.

Peptidylarginine Deiminase (PAD) and Post-Translational Protein Deimination—Novel Insights into Alveolata Metabolism, Epigenetic Regulation and Host–Pathogen Interactions

“…Likewise of interest is that while all apicomplexans are considered parasitic and some are highly pathogenic, much wider roles for their function in host interactions have been suggested, including commensalism and mutualism [76]. Given the conserved status of PAD/ADI throughout phylogeny, the roles for the deimination regulation of the pathways involved in host-pathogen interaction and the coevolution of Alveolata may therefore be of considerable interest, particularly in the light of the various pathways identified here for deimination, which are linked to a wide range of metabolic processes, transcription and gene regulation.…”

NAD(P) transhydrogenase isoform distribution provides insight into apicomplexan evolution

“…genus Cardiosporidium ) relationships. Species of Nephromycida are unusual in that they accommodate and rely on bacterial endosymbionts ( Hunter et al, 2020 ; Paight et al, 2022 ). At least two distinct βα-type NTH-encoding genes are present in the assembled genome of Cardiosporidium cionae species isolated from the hemolymph of the tunicate Ciona intestinalis ( Hunter et al, 2020 ) ( Table S2 ).…”

“…Species of Nephromycida are unusual in that they accommodate and rely on bacterial endosymbionts ( Hunter et al, 2020 ; Paight et al, 2022 ). At least two distinct βα-type NTH-encoding genes are present in the assembled genome of Cardiosporidium cionae species isolated from the hemolymph of the tunicate Ciona intestinalis ( Hunter et al, 2020 ) ( Table S2 ). In addition, we identified at least three distinct βα-type NTH-encoding genes from the metagenome of Nephromyces species isolated from the renal sac of the tunicate Molgula occidentalis ( Munoz-Gomez et al, 2019 ) ( Table S2 ).…”

Amino Acid Metabolism in Apicomplexan Parasites

“…It likely indicates the need for de novo synthesis of these amino acids during encystation and calls for future work to identify the missing enzymes and their importance during latency or a different developmental stage. Fascinatingly and unique to a few apicomplexans, Cardiosporidium cionae appears to have maintained a bacterial endosymbiont that contains the pathway for de novo lysine biosynthesis [88]. It provides only two key metabolites: lysine and lipoic acid, a mechanism that cleverly reduces host dependency and potential virulence, making the extracellular life of C. cionae possible [88].…”

“…Fascinatingly and unique to a few apicomplexans, Cardiosporidium cionae appears to have maintained a bacterial endosymbiont that contains the pathway for de novo lysine biosynthesis [88]. It provides only two key metabolites: lysine and lipoic acid, a mechanism that cleverly reduces host dependency and potential virulence, making the extracellular life of C. cionae possible [88].…”