Analogs of the Golgi complex in microsporidia: structure and avesicular mechanisms of function

Abstract

Microsporidia are obligatory intracellular parasites, most species of which live in the host cell cytosol. They synthesize and then transport secretory proteins from the endoplasmic reticulum to the plasma membrane for formation of the spore wall and the polar tube for cell invasion. However, microsporidia do not have a typical Golgi complex. Here, using quick-freezing cryosubstitution and chemical fixation, we demonstrate that the Golgi analogs of the microsporidia Paranosema (Antonospora) grylli and Paranosema locustae appear as 300-nm networks of thin (25- to 40-nm diameter), branching or varicose tubules that display histochemical features of a Golgi, but that do not have vesicles. Vesicles are not formed even if membrane fusion is inhibited. These tubular networks are connected to the endoplasmic reticulum, the plasma membrane and the forming polar tube, and are positive for Sec13, γCOP and analogs of giantin and GM130. The spore-wall and polar-tube proteins are transported from the endoplasmic reticulum to the target membranes through these tubular networks, within which they undergo concentration and glycosylation. We suggest that the intracellular transport of secreted proteins in microsporidia occurs by a progression mechanism that does not involve the participation of vesicles generated by coat proteins I and II.

Immunolocalization of an Alternative Respiratory Chain in Antonospora (Paranosema) locustae Spores: Mitosomes Retain Their Role in Microsporidial Energy Metabolism

“…The small amount of metabolic enzymes in the intracellular stages was not due to their leakage, degradation, or poor extraction. In the same samples of spores and merogonial plus early sporogonial stages, we have detected commensurable amounts of the Sec13 subunit of the COPII coat (3,8), two bands recognized by anti-Hsp70 Abs (present study), and SNARE protein syntaxin (our unpublished data). Thus, expression patterns of the enzymes of core carbon metabolism and other housekeeping proteins appear to be different in the life cycle of microsporidia.…”

Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites

“…Microsporidia are currently placed on an ancestral branch within the fungi, although this placement has only recently been worked out, due to the absence of clear morphological and physiological connections to other eukaryotes and the profound changes resulting from adaptations to an intracellular lifestyle (3)(4)(5)(6). The evolutionary history of microsporidia is marked by the loss of several eukaryotic features, such as mitochondria (7), a typical Golgi apparatus (8), a flagellum (3), and the evolutionary innovation of an infection apparatus, the polar tube. Microsporidia evolved distinctive genetic features, such as massive loss of genes, leading to the smallest known eukaryotic genomes (1).…”

Neogenesis and maturation of transient Golgi-like cisternae in a simple eukaryote

“…classical COPI vesicles). One scenario for the genesis of these connections is that they are formed from ESV membrane material analogous to mechanisms for Golgi ribbon formation (Trucco et al, 2004;Griffiths, 2000;Beznoussenko et al, 2007). Formation of such higher-order compartment structures in cells of mammals, plants and insects is thought to lead to more uniform distribution of processing enzymes.…”

“…In unicellular organisms, Golgi organization is less complex, ranging from unlinked stacks associated with ER exit sites in Pichia pastoris (Bevis et al, 2002;Rossanese et al, 1999) and several protozoa (Benchimol et al, 2001;Hager et al, 1999;Struck et al, 2008), to individual, functionally distinct Golgi cisternae without stacked organization in Saccharomyces cerevisiae (Rossanese et al, 1999). Microsporidia, intracellular fungal parasites of mammals, have highly reduced trafficking systems, and lack a conventional Golgi (Beznoussenko et al, 2007).…”