Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2020 Dec 1:11:580719.
doi: 10.3389/fmicb.2020.580719. eCollection 2020.

Metabolic Contributions of an Alphaproteobacterial Endosymbiont in the Apicomplexan Cardiosporidium cionae

Elizabeth Sage Hunter  1 , Christopher Paight  2 , Christopher E Lane  1
Affiliations

Metabolic Contributions of an Alphaproteobacterial Endosymbiont in the Apicomplexan Cardiosporidium cionae

Elizabeth Sage Hunter et al. Front Microbiol. .

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.

Keywords: alphaproteobacteria host-associated bacteria; apicomplexa; bacterial endosymbiont; mutualism; parasite – host interactions; parasitism.

PubMed Disclaimer

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
System overview of Cardiosporidium cionae and Nephromyces showing tunicate host (A,F), area of localization (B,G), filamentous life stage (C,H), oocyst life stage (D,I), and vertically transferred fluorescent in situ hybridization (FISH) labeled bacterial endosymbionts within the oocysts (E,J). Scale bars are approximations due to resizing of images. FISH was carried out according to the method in Paight et al. (2020).
FIGURE 2
FIGURE 2
Metabolism of Cardiosporidium cionae. Solid colors indicate genomic protein homologs, dots show where homologs were only found in the transcriptome data, and bold pathways represent bacterial endosymbiont contributions. This figure corresponds to the genome and transcriptome information in Supplementary Table 2.
FIGURE 3
FIGURE 3
Apicoplast phylogeny created using a modified dataset provided by Muñoz-Gómez et al. (2019a), showing the monophyly of C. cionae and Nephromyces. The complete, circularized C. cionae apicoplast recovered from the genomic dataset, and Nephromyces apicoplast sp. 654, are shown in blue. The resolved topology differs from Muñoz-Gómez et al. (2019a) because of the exclusion of gregarines from our dataset, which includes Nephromycida (blue), Piroplasmida (red), Coccidia (green), and apicomonads (yellow) as the outgroup. Statistical support was estimated using aLRT (1,000) and ultrafast bootstrap (1,000) (Nguyen et al., 2015) and these values are shown in this order on the nodes.
FIGURE 4
FIGURE 4
Size, contig distribution, coding density, and annotations of major functional categories of genes in the α-proteobacteria endosymbiont genome.
FIGURE 5
FIGURE 5
Alphaproteobacteria phylogeny created with GToTree pipeline (117 concatenated genes) including all sequenced alphaproteobacteria published on NCBI and both the C. cionae and Nephromycesα-endosymbionts (in red). Bootstrap support is shown as a decimal value on the nodes.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Abrahamsen M. S., Templeton T. J., Enomoto S., Abrahante J. E., Zhu G., Lancto C. A., et al. (2004). Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304 441–445. 10.1126/science.1094786 - DOI - PubMed
    1. Alarcón M. E., Jara-F A., Briones R. C., Dubey A. K., Slamovits C. H. (2017). Gregarine infection accelerates larval development of the cat flea Ctenocephalides Felis (Bouché). Parasitology 144 419–425. 10.1017/S0031182016002122 - DOI - PubMed
    1. Babraham Bioinformatics (n.d.). FastQC A Quality Control Tool for High Throughput Sequence Data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (accessed November 30, 2019).
    1. Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Kulikov A. S., et al. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19 455–477. 10.1089/cmb.2012.0021 - DOI - PMC - PubMed
    1. Blume M., Seeber F. (2018). Metabolic interactions between Toxoplasma Gondii and its host. F1000Res. 7:1719. 10.12688/f1000research.16021.1 - DOI - PMC - PubMed

LinkOut - more resources