Comparative genomics reveals Cyclospora cayetanensis possesses coccidia-like metabolism and invasion components but unique surface antigens

Abstract

BackgroundCyclospora cayetanensis is an apicomplexan that causes diarrhea in humans. The investigation of foodborne outbreaks of cyclosporiasis has been hampered by a lack of genetic data and poor understanding of pathogen biology. In this study we sequenced the genome of C. cayetanensis and inferred its metabolism and invasion components based on comparative genomic analysis.ResultsThe genome organization, metabolic capabilities and potential invasion mechanism of C. cayetanensis are very similar to those of Eimeria tenella. Propanoyl-CoA degradation, GPI anchor biosynthesis, and N-glycosylation are some apparent metabolic differences between C. cayetanensis and E. tenella. Unlike Eimeria spp., there are no active LTR-retrotransposons identified in C. cayetanensis. The similar repertoire of host cell invasion-related proteins possessed by all coccidia suggests that C. cayetanensis has an invasion process similar to the one in T. gondii and E. tenella. However, the significant reduction in the number of identifiable rhoptry protein kinases, phosphatases and serine protease inhibitors indicates that monoxenous coccidia, especially C. cayetanensis, have limited capabilities or use a different system to regulate host cell nuclear activities. C. cayetanensis does not possess any cluster of genes encoding the TA4-type SAG surface antigens seen in E. tenella, and may use a different family of surface antigens in initial host cell interactions.ConclusionsOur findings indicate that C. cayetanensis possesses coccidia-like metabolism and invasion components but unique surface antigens. Amino acid metabolism and post-translation modifications of proteins are some major differences between C. cayetanensis and other apicomplexans. The whole genome sequence data of C. cayetanensis improve our understanding of the biology and evolution of this major foodborne pathogen and facilitate the development of intervention measures and advanced diagnostic tools.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2632-3) contains supplementary material, which is available to authorized users.

Cyclospora cayetanensis

“…andToxoplasma gondii. The dominant surface antigens observed in other coccidian are not present or significantly diminished (Liu et al, 2016). Nevertheless, these results need to be validated.…”

“…The conserved sequence nature of rRNA and HSP70 genes and intra-isolate variations among different copies of ITS-1 and ITS-2 had made the development of genotyping tools for the parasite difficult (Adam et al, 2000;Olivier et al, 2001;Riner et al, 2010;Zhou et al, 2011;Sulaiman et al, 2013Sulaiman et al, , 2014. The recent availability of whole mitochondrial and apicoplast genome sequences (Tang et al, 2015;Qvarnstrom et al, 2015;Cinar et al, 2015) and whole genome sequencing (Liu et al, 2016) beyond rRNA and heat shock protein genes could facilitate development of genotyping tools for investigations of Cyclospora outbreaks. Recently, whole-genome sequence data from C. cayetanensis protozoa enabled the development of a MLST genotyping tool for characterizing isolates.…”

Transmembrane solute transport in the apicomplexan parasite Plasmodium

“…Even so, the apparent lack of transporters in Plasmodium parasites suggests there is little functional redundancy and reinforces their potential therapeutic possibilities [11]. Though not studied in as much detail in other apicomplexan parasites (see for example [12]), Toxoplasma has a greater number of transporters than Plasmodium (including within transporter classes), suggesting far more redundancy and thus fewer targeting opportunities. Interestingly, Cryptosporidium and Babesia parasites may have reduced numbers of transporters and/or transporter classes compared with Plasmodium (in this case targeting opportunities could be increased due to less functional redundancy and/or decreased due to druggable transport classes not being present).…”

Molecular typing of Cyclospora cayetanensis in produce and clinical samples using targeted enrichment of complete mitochondrial genomes and next-generation sequencing

“…Progress on the development of molecular epidemiologic tools to link cases with sources of infection has been hindered by the limited DNA sequence information. With the recent advances in sequencing technologies such as nextgeneration sequencing (NGS) and availability of efficient genome assembly programs, whole genome assemblies, complete mitochondrial and apicoplast genomes of C. cayetanensis have become available [11][12][13][14][15][16][17][18]. NGS is the preferred technology for generation of high-throughput high-resolution data in streamlined fashion for clinical diagnostics, forensic science, and public health research.…”