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Ultrastructure of Early Stages of Rozella Allomycis (Cryptomycota) Infection of Its Host, Allomyces Macrogynus (Blastocladiomycota)

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Ultrastructure of Early Stages of Rozella Allomycis (Cryptomycota) Infection of Its Host, Allomyces Macrogynus (Blastocladiomycota) Fungal Biology 123 (2019) 109e116 Contents lists available at ScienceDirect Fungal Biology journal homepage: www.elsevier.com/locate/funbio Ultrastructure of early stages of Rozella allomycis (Cryptomycota) infection of its host, Allomyces macrogynus (Blastocladiomycota) * Martha J. Powell, Peter M. Letcher Department of Biological Sciences, The University of Alabama, Tuscaloosa, Alabama 35487, USA article info abstract Article history: This study reconstructs early stages of Rozella allomycis endoparasitic infection of its host, Allomyces Received 15 August 2018 macrogynus. Young thalli of A. macrogynus were inoculated with suspensions of R. allomycis zoospores Received in revised form and allowed to develop for 120 h. Infected thalli at intervals were fixed for electron microscopy and 28 September 2018 observed. Zoospores were attracted to host thalli, encysted on their surfaces, and penetrated their walls Accepted 13 November 2018 with an infection tube. The parasite cyst discharged its protoplast through an infection tube, which Available online 22 November 2018 invaginated the host plasma membrane. The host plasma membrane then surrounded the parasite Corresponding Editor: Pieter van West protoplast and formed a compartment confining it inside host cytoplasm. The earliest host-parasite interface within host cytoplasm consisted of two membranes, the outer layer the host plasma mem- Keywords: brane and the inner layer the parasite plasma membrane. At first a wide space separated the two Development membranes and no material was observed within this space. Later, as the endoparasite thallus expanded Interface within the compartment, the two membranes became closely appressed. As the endoparasite thallus Mitochondria continued to enlarge, the interface developed into three membrane layers. Thus, host plasma membrane Parasitism surrounded the parasite protoplast initially without the parasite having to pierce the host plasma Plasmodium membrane for entry. Significantly, host-derived membrane was at the interface throughout Zoospores development. © 2018 British Mycological Society. Published by Elsevier Ltd. All rights reserved. 1. Introduction endoparasites, the algal parasite Aphelida and the animal parasite Microsporidia (Letcher et al., 2013, 2015; Karpov et al., 2013, 2014b). The objective of our research is to determine the mode of infec- These three groups have been named the Opisthosporidia (Karpov tion of the obligate endoparasite, Rozella allomycis, into its blastoclad et al., 2014a), but their consistent phylogenetic placement in a host, Allomyces. Although ultrastructural studies demonstrate that monophyletic lineage is controversial (Bass et al., 2018; Tedersoo the unwalled parasite thallus is located within host cytoplasm (Held, et al., 2018). It is however clear that they are related. As a clade sis- 1973a; Powell et al., 2017), how it gains entry into the host is un- ter of free-living nucleariids and Chytridiomycota, this lineage is known. Rozella parasitizes chytrids, oomycetes, and green algae and widely viewed as an early-diverging branch of fungi (Berbee et al., was once classified within the Chytridiomycota because of its pro- 2017; James et al., 2013; Tedersoo et al., 2018), and as such can duction of posteriorly uniflagellate zoospores (Barr, 1980; Sparrow, reveal adaptations in the evolution of fungi. The three groups have in 1960). Molecular analyses have revealed that phylogenetically common a stage in which chitin-containing walls are produced, but Rozella lies outside the Chytridiomycota (James et al., 2006)andis they are diverse in other ways. Rozella and aphelids reproduce with now classified in the phylum Cryptomycota (Karpov et al., 2014a). In posteriorly uniflagellate zoospores, whereas Microsporidia reproduce molecular phylogenetic studies, R. allomycis places together with with a walled spore containing a specialized structure for infection, other Rozella species (James et al., 2006; Letcher et al., 2017a, b)and the polar filament. In addition Rozella and aphelids are phagotrophic commonly within a clade with two other groups of plasmodial whereas Microsporidia are osmotrophic. Of particular interest in reconstructing the evolutionary diver- gence of these groups from free-living nucleariids (Berbee et al., * Corresponding author. 1332 SEC, Box 870344, 300 Hackberry Lane, Tuscaloosa, 2017) is understanding the evolution of nutritional modes. Key to Alabama 35487, USA. Fax: þ1 205 348 1786. understanding nutrition of obligate endoparasites is understanding E-mail addresses: [email protected] (M.J. Powell), [email protected] how the parasite gains entry into host cells without damaging and (P.M. Letcher). https://doi.org/10.1016/j.funbio.2018.11.009 1878-6146/© 2018 British Mycological Society. Published by Elsevier Ltd. All rights reserved. 110 M.J. Powell, P.M. Letcher / Fungal Biology 123 (2019) 109e116 killing the host at the onset of infection. An ultrastructural devel- Zoospores of R. allomycis mixed with young host thalli were opmental study of R. allomycis in its blastoclad host, Allomyces attracted to the host and clustered around the host (Fig.1A). At 2.5 h anomalous, demonstrated that the parasite enters the host cyto- after inoculation, parasite zoospores encysted and attached to the plasm and totally phagocytizes the host from within the host host thalli (Fig. 1B). Although attachment to the rhizoids could cytoplasm (Powell et al., 2017). How the parasite gains entry occur (Fig. 1C), the hyphal portion of the 24hr-old host thallus was directly into the host cytoplasm is not known. In another endo- most densely infected (Fig. 1B). By 4.0 h after inoculation, small parasite of Allomyces, the blastoclad Catenaria allomycis, the para- protoplasts of the parasite were visible in the host cytoplasm site's thallus is totally immersed within host cytoplasm (Powell, (Fig. 1C). At 24 h after inoculation, cultures consisted of a range of 1982; Sykes and Porter, 1980). Unlike the thallus of R. allomycis, developmental stages because infection continued. From this stage the thallus of C. allomycis appears to be walled at the earliest stage multiple infections could be observed within a single host thallus within the host (Sykes and Porter, 1980), even from the round-cell (Fig. 1D). stage (Powell, 1982). Sykes and Porter (1980) concluded that during penetration into the host and entry into the host cytoplasm, the 3.2. Electron microscopy parasite ruptured the host plasma membrane, but did not imme- diately kill the host cell. 3.2.1. Parasite infection of the host The purpose of this study is to reconstruct the early infection Parasite zoospores contacted the host wall, rounded-up and process of R. allomycis in its host Allomyces macrogynus. Held (1974) produced a cyst wall (Fig. 2A). The cyst then produced an appres- demonstrated that Rozella was a biotrophic obligate endoparasite sorium, which attached to the host wall (Fig. 2A, B). A large vacuole because Rozella was not capable of infecting dead host hyphae. (the posterior vacuole) appeared in the cyst (Fig. 2B). The host cell Consequently, the host-parasite interface is critical because this is wall changed in density (Fig. 2B) as an infection tube extended from the site of molecular and nutritional exchange necessary for an appressorium and penetrated through the host wall (Fig. 2C, D). maintaining the relationship between an obligate endoparasite and The infection tube was peg-like at first (Fig. 2C). As the infection its living host required for the parasite's survival. Mode of entry into tube grew, it invaginated the host plasma membrane, which a relationship with the host cytoplasm is important because if the thickened at the area of contact. Granular material appeared be- obligate parasite damages the host plasma membrane during the tween the host and parasite at this stage (Fig. 2C). The infection initial entry process, it could cause immediate death of the host cell tube continued to elongate into the host, pushing the host plasma and the inability of the parasite to continue development. membrane inward as the parasite discharged its protoplast through an opening in the infection tube (Fig. 2D). The infection tube wall 2. Materials and methods was thickened in the region it penetrated into the host cytoplasm (Fig. 2D). The cyst vacuole appeared to expand during this process 2.1. Culture (Fig. 2D) until the parasite protoplast was discharged, leaving only remnants of its cytoplasm in the cyst (Fig. 2E). The empty cysts R. allomycis (UM690) parasitic in A. macrogynus was obtained (Fig. 2A, E) eventually collapsed (Fig. 2A). from Gerald Benny (University of Florida) who obtained it from the culture collection of R. K. Benjamin (Rancho Santa Ana Botanic Gar- 3.2.2. Early host compartmentalization of parasite dens, California). Single-membered cultures of A. macrogynus and At 3.5 h after inoculation, parasite spherical protoplasts lay in dual-membered cultures of A. macrogynus infected with R. allomycis compartments within the host cytoplasm and near the host cell were maintained at 24 C on 1/8 strength Emerson YPSS agar (Difco wall (Fig. 2A, F). The host-parasite interface at this stage was two 273910) with a thin layer of water coating the agar surface. layered with a wide space between the two membranes (Figs. 2DeF; 3AeC), the outer membrane layer being derived from 2.2. Microscopy the host plasma membrane and the inner layer being the parasite plasma membrane. The space between the two membranes was On day 11 after inoculation of nutrient agar plates with the dual devoid of visible contents (Figs. 2F; 3A, C). There was variability in culture, R. allomycis zoospores were numerous and easily distin- the width of space between the two membranes at the host- guished from the larger host spores. Twenty-four hr old thalli of parasite interface within a compartment (Fig. 2F). The lumen A. macrogynus were inoculated with suspensions of R. allomycis could be wide in one area of the compartment while the parasite zoospores and allowed to infect host hyphae and develop for 120 h. might be adjacent to the host membrane in another region of the Infected hyphae were observed with a Nikon Eclipse E200 light compartment (Fig.
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