DESCRIPTION OF THE PHYLUM OOMYCOTA (WINTER 1879)

EUKARYA> CHROMALVEOLATA> HETEROKONTAE> OOMYCOTA

Oomycota (o-o-mi-KO-ta) is derived from two Greek roots that mean egg (oario -ωάριο) and fungus (mykes -μύκης). The reference is to the fungus-like habit of the organism and its typical oogamous sexual reproduction. Winter defined the class, Oomycetes, we gave it the proper ending for a phylum of a fungus-like organism. In addition, the description of this group is broader than the original Oomycetes. This description includes hyphochytrids and several heterokont taxa with close associations with the Oomycetes.

INTRODUCTION TO THE OOMYCOTA The water molds are among the most economically important organisms in the heterokonts. Although some like Saprolegnia (Figure 1) are used for the commercial production of acetone and other small organics, most are important because of the damage that they do to agriculture. The most notable outcome of economic importance was the great potato famine of Ireland (1845-1850) caused by Phytophthora (Figure 2). The famine began in September of 1845 with the leaves of potato plants appearing blackened. Soon, however, the feeding filaments (hyphae) had coursed through the plants, which turned to stinking, nauseous masses of slime. The spores released by the plants infected in the initial assault spread over the island of Ireland, and the crop of potatoes, the principle food crop, failed. The potato blight persisted through the next four years, a time called The great Hunger during which as many as 5 million may have died from starvation. Other members of the oomycotes cause the familiar downy mildew of Lilac. The life cycles of the Oomycota generally are eucarpic, but some may be holocarpic. Details of the life histories can best be seen in Figure 3, Life Cycle of Saprolegnia. Note that there is an asexual cycle (Figure 3-A-H) and a sexual cycle (Figure 3-I-O). In the asexual cycle, the organism produces specialized sporangia (Figure 3-B) from which emerge zoospores with typical heterokont flagella (an anterior tinsel flagellum and a recurrent whiplash flagellum; see Figure 3-C). Notably, they have two types of zoospores (text with tooltip) A zoospore is an asexual spore that is motile. Zoo- (pronoumced zo-o) is a prefix that means moving. which may be produced in succession: a primary zoospore (Figure 3-C) with both flagella originating at the anterior end and a secondary zoospore (Figure 3-F) with the two flagella originating laterally. Zoospores then germinate to produce a body with cellulose and glucan walls (Figure 3-H and -A). The filaments are siphonaceous filaments (called hyphae), coarse, and non-septate. Nuclear division is closed, with a persistent nucleolus and an intranuclear spindle (text with tooltip) An intranuclear spindle elaborates within the nuclear membrane of an organism with closed mitosis. with poles near pairs of centrioles oriented at 180o to each other. In the vegetative state, they are diploid organisms with gametic meiosis. Sexual reproduction begins with the apposition of two hyphae that are cut off by septa (text with tooltip) A septum (septa, pl.) is a crosswall. It can be the crosswall in a filament, or the mesentary in a cnidarian. at their tips (Figure 3-J-K). Figure 3-L illustrates the migration of nuclei through channels from one (differentiated as an antheridium) to the other (differentiated as an oogonium). Following fertilization, the zygote develops into a thick-walled (chitinous) oospore (Figure 3-M-N). The oospores are resting stages that germinate by the production of a diploid vegetative filament (Figure 3-O).

FIGURE 1. Oogonia of Saprolegnia. Image from http://www.botany.utoronto.ca/ResearchLabs/MallochLab/Malloch/Moulds/Classification.html	FIGURE 2. Labeled photomicrograph of Phytophthora. Image from http://www.inspection.gc.ca/english/plaveg/pestrava/phyram/images/fig17.jpg

FIGURE 3. Life Cycle of Saprolegnia. A-H is the asexual cycle and I-O is the sexual cycle. See the text for a detailed explanation of the stages. Image taken from Bold et al. (1987)

THE HYPHOCHYTRIDS Hyphochytridium (Figure 4) is in a group that is reduced in form and resembles a chytrid, but only superficially so. These organisms range from parasitic to saprobic and can be found in freshwater or marine environments. Like Saprolegnia, these tend to be diploid with a haploid phase that is reduced or restricted to the gametes. They tend to be holocarpic and have walls of chitin and sometimes also cellulose. In the asexual cycle, zoospores have only a single anterior tinsel flagellum and a barren basal body (text with tooltip) A basal body (kinetosome) is called barren if it is never associated with a flagellum. , formed within an inoperculate sporangium or in a plasmodial (text with tooltip) A plasmodium is a multinucleate cell formed by nuclear divisions without cytokinesis. mass released from a zoosporangium. During mitosis the nucleus is perforated at the poles with centrioles in orthogonal pairs. During the sexual cycle gametes are motile and similar (isogametes or anisogametes). As in Figure 3, the hyphochytrids make both sexual and asexual resting spores. However, upon germination, both spores release zoospores.

FIGURE 4. Hyphochytridium grown from a spore in 24 hrs from an infected pollen grain. Image from http://www.bsu.edu/classes/ruch/msa/barr.html

SYSTEMATICS OF THE OOMYCOTA Note that the Hyphochytrids (Pr-25 and Pr-21) and Oomycetes (Pr-27 and Pr-20) are treated as separate phyla by Margulis and Schwartz (1988 and 1998, respectively), Dick (1990) and Fuller (1990). Indeed, Fuller (1990) explores the reasons for lumping or separating them and concludes that the similarities in lysine synthesis and mitochondria cannot counterbalance differences in cell wall chemistry, mitosis, centrioles and rRNA. Perhaps, such differences do not really occur. Patterson (1999) places them together in the Stramenopiles (Heterokonts). Indeed, the tree of Sogin and Patterson (Tree of Life Project) has the two groups closely linked on the same clade within the heterokonts. Barr and Desaulniers (1989) further suggest that the similarities in their flagellar structures warrant their association. I have followed their lead and lumped both groups into a single phylum, Oomycota. Beakes (1989) reports that the oomycetes have ultrastructural and biochemical affinities with the brown algae and eustigs as well as obvious (but perhaps misleading) morphological similarities with the xanthophyte, Vaucheria. Dick (1990) agrees that the siphonaceous form in the Oomycota is not only convergent with that of the Xanthophyta but highly advanced within the Oomycota. Still, they have obvious ties to other members of the heterokonts. Most of the recent molecular phylogenetic analyses (e.g. Andersen 2004; Brown and Sorhannus 2010; Figure 5) show the Oomycota as the sister to the photosynthetic heterokonts. Basal taxa in the clade that includes the Oomycota are Pirsonia (Figure 6) and Developayella (Figure 7). A examination of these taxa, because they occur near the point at which a heterotrophic motile heterokont entered into secondary endosymbiosis to become photosynthetic, is great interest. Pirsonia is similar to taxa in the Oomycota in that it is fungus-like in its life history and ecology. Figure 6 shows the margin of a heavily infected centric diatom with the liberation of propagules from the parasite. Curiously, the motile cells that they produce have two flagella, each of which has flagellar hairs. The anterior flagellum has the typical heterokont tripartite tubular hairs, but the posteriorly-directed flagellum has simple flagellar hairs. Although Kuhn et al. (2004) show Pirsonia as sister to the Oomycota, Yubuki et al. (2010) have Pirsonia emerging as sister to Oomycota + Ochrophyta (Photosynthetic Heterokonts). Developayella (Figure 7) is a free-living gliding flagellate with a ventral feeding groove. It does seem to be able to attach to the substrate by long strands of cytoplasm, which is reminiscent of the amoeboid silicoflagellates. Though the form of the cell would suggest that they should occupy a more basal position in the Oomycota clade, actual analyses have produced variable results. Andersen (2004) and Riisberg et al. (2009) have Developayella emerge as basal or sister to the Oomycota. However, Developayella appears within the Oomycota (Grant et al. 2009; Yubuki et al. 2010), as sister to the Ochrophytes (Kostka et al. 2004), and within the heterotrophic heterokonts, but not associated with the Oomycota (Kostka et al. 2007).

FIGURE 5. A cladogram of the Oomycota sensu latu (taxa in shaded box) within the heterotrophic taxa of the heterokonts (taxa in bold). This is a consensus of many analyses including Andersen (2004), Riisberg et al. (2009), and Brown and Sorhannus (2010).

FIGURE 6. Photomicrograph of Pirsonia infecting a centric diatom. It is beginning to release propagules from the infected cell. Image from: Kuhn et al. (2004), Figure 2.	FIGURE 7. Drawing of Developayella, a free-living biflagellate that is sister to the Oomycota and close to the ancestor of the heterokont that underwent the secondary endosymbiosis to produce the photosynthetic heterokonts. Image from: Tong (1995).

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By Jack R. Holt. Last revised: 02/19/2013