The inner membrane complex (IMC) of apicomplexan parasites contains a network of intermediate filament-like proteins. The 14 alveolin domain-containing IMC proteins in Toxoplasma gondii fall into different groups defined by their distinct spatiotemporal dynamics during the internal budding process of tachyzoites. Here, we analyzed representatives of different IMC protein groups across all stages of the Toxoplasma life cycle and during Sarcocystis neurona asexual development. We found that across asexually dividing Toxoplasma stages, IMC7 is present exclusively in the mother’s cytoskeleton, whereas IMC1 and IMC3 are both present in mother and daughter cytoskeletons (IMC3 is strongly enriched in daughter buds). In developing macro- and microgametocytes, IMC1 and -3 are absent, whereas IMC7 is lost in early microgametocytes but retained in macrogametocytes until late in their development. We found no roles for IMC proteins during meiosis and sporoblast formation. However, we observed that IMC1 and IMC3, but not IMC7, are present in sporozoites. Although the spatiotemporal pattern of IMC15 and IMC3 suggests orthologous functions in Sarcocystis, IMC7 may have functionally diverged in Sarcocystis merozoites. To functionally characterize IMC proteins, we knocked out IMC7, -12, -14, and -15 in Toxoplasma. IMC14 and -15 appear to be involved in switching between endodyogeny and endopolygeny. In addition, IMC7, -12, and -14, which are all recruited to the cytoskeleton outside cytokinesis, are critical for the structural integrity of extracellular tachyzoites. Altogether, stage- and development-specific roles for IMC proteins can be discerned, suggesting different niches for each IMC protein across the entire life cycle.
Digital Object Identifier (DOI)
This work was supported by NIH grants, USDA NIFA grant 2009-65109-05918 to D.K.H., grant AI110638 to J.S., and grant AI081924 to M.-J.G.
Supplemental material for this article may be found at https://doi.org/10.1128/ mSphere.00409-17.
Dubey, Rashmi; Harrison, Brooke; Dangoudoubiyam, Sriveny; Bandini, Giulia; Cheng, Katherine; Kosber, Aziz; Agop-Nersesian, Carolina; Howe, Daniel K.; Samuelson, John; Ferguson, David J. P.; and Gubbels, Marc-Jan, "Differential Roles for Inner Membrane Complex Proteins Across Toxoplasma gondii and Sarcocystis neurona Development" (2017). Gluck Equine Research Center Faculty Publications. 15.
FIG S2, TIF file, 2.3 MB.tif (2388 kB)
FIG S3, TIF file, 2.5 MB.tif (2588 kB)
FIG S4, PDF file, 0.1 MB.pdf (59 kB)
FIG S5, TIF file, 2.3 MB.tif (2396 kB)
FIG S6, TIF file, 0.9 MB.tif (969 kB)
FIG S7, TIF file, 2.4 MB.tif (2502 kB)
FIG S8, TIF file, 1.4 MB.tif (1509 kB)
FIG S9, TIF file, 0.3 MB.tif (269 kB)
TABLE S1, PDF file, 0.1 MB.pdf (60 kB)