Saprolegniaceae

Dictyuchus monosporus, from Lindau (1912).

Belongs within: Pseudofungi.

Water moulds
Published 12 November 2015
Salmonid infected with Saprolegnia, from the Scottish Government.

In the 1970s and 1980s, stocks of salmon and trout around the North Atlantic Ocean took a sizeable hit. Mature fish entering fresh water had their skin break out in lesions that eventually became covered in a slimy, cottony growth. With the lesions eventually eating into the underlying tissue, many fish died from these infections before they could spawn.

The disease became known as ulcerative dermal necrosis, and its underlying cause remains unknown. The cottony growth so often associated with the disease, however, was made up of a mould-like organism called Saprolegnia. Saprolegnia belongs to a family Saprolegniaceae in a group of organisms known as the Oomycetes, commonly referred to as ‘water moulds’. Most Saprolegniaceae function as saprobes, living off decaying organic matter. A few, however, can occasionally function as pathogens. In the case of the aforementioned necrosis outbreak, the Saprolegnia would have been a secondary infection that exacerbated the progress of the disease. Another genus, Aphanomycese, includes species that can cause root rot in vegetables such as peas or beets (Johnson et al. 2002).

Mature and developing oogonia of Saprolegnia, copyright George Barron.

In habit and lifestyle, water moulds resemble fungi, and were long classified as such. When they were first described in the 1700s, however, they were identified as algae due to similarities in their cell and spore morphology to freshwater algae such as Vaucheria. In recent decades, it has become clear that it was these original observers that were closer to the mark. Oomycetes are not directly related to the true fungi, but belong to a lineage known as the heterokonts or stramenopiles. Most heterokonts are microbial, but they also include algal forms such as the brown algae and (yes) Vaucheria. The heterokont affinities of water moulds become apparent during asexual reproduction when they produce motile zoospores bearing a pair of flagella (though many ‘water moulds’ are terrestrial rather than aquatic, these zoospores do require water to spread). As is typical of heterokonts, these two flagella differ in appearance: the anterior flagellum bears a series of lateral side-branches whereas the posterior flagellum in smooth. Other significant differences between oomycetes and true fungi are that oomycetes are diploid through the greater part of their life cycle (fungi are haploid), and their cell walls are composed not of chitin but of other compounds such as glucans and/or cellulose.

Drawing of zoospores of Saprolegnia, showing divergent flagella, from here.

Characteristic features of the Saprolegniaceae in particular include their possession of relatively broad hyphae, up to 150 µm in some cases (Dick 2001), that are not divided into cells by septae. Other distinguishing features relate to the production of reproductive cells. Most oomycetes are capable of both asexual and sexual reproduction, though one genus of Saprolegniaceae, Aplanopsis, is only known to reproduce sexually. In asexual reproduction, the motile zoospores are produced within a distinct zoosporangium (some other oomycetes do not separate the zoosporangium from the adjoining hypha until after zoospore formation). When first released, the zoospores move relatively little and soon transform into an immotile cyst. This cyst will eventually revert back into a zoospore, and it is at this stage that the greater part of dispersal happens. This secondary zoospore will then transform again into a cyst, from which will grow the mature hyphae.

Hyphae of an Achlya-like oomycete, with clusters of encysted zoospores at the ends of emptied zoosporangia, from here.

Sexual reproduction involves the production of distinct oogonia and antheridia, with the latter fertilising the former to produce oospores (some species can produce oospores parthenogenetically). These differ from zoospores in being aflagellate and immobile, with thick walls that make them more resistant to adverse conditions. Oospores of Saprolegniaceae contain oil globules that probably function as an energy store (like the endosperm of a plant seed). Depending on the species, the distribution of oil globules may vary between numerous small globules evenly distributed around the periphery of the centrally located cytoplasm (referred to as ‘centric’), or one large globule pushing the cytoplasm off to one side (‘eccentric’). An oospore may geminate into hyphae alone, or it may produce hyphae topped by zoosporangia.

Oogonium of Saprolegnia, with associated antheridium, copyright George Barron.

The genera of Saprolegniaceae have been primarily distinguished by features of the zoosporangia, such as the manner of release of the zoospores. In some genera, the initial zoospores may have already progressed to encystment or the secondary zoospore stage by the time they fully emerge. In genera such as Achlya, the spores are released from a single terminal opening and form a clump at the end of the emptied sporangium. In others such as Saprolegnia, they disperse individually as soon as they escape. And in genera such as Dictyuchus, the zoosporangium wall opens in multiple places and the spores are all sent out by their own distinct orifice. However, more recent phylogenetic studies have cast doubt on the integrity of some of these genera: the Achlya type of zoospore dispersal, for instance, is probably basal for the Saprolegniaceae as a whole and this genus is polyphyletic.

Systematics of Saprolegniaceae
Saprolegniaceae
|--Protoachlya Coker 1923KC01
|--Couchia Martin 1981KC01
|--Calyptralegnia Coker 1927KC01
|--Aplanes de Bary 1888KC01
|--Archilegnia Apinis 1935KC01
|--Brevilegnia Coker & Couch 1927KC01
|--Geolegnia Coker 1925KC01
|--Hamidia Chaudhuri 1942 (n. d.)KC01
|--Hydatinophagus Valkanov 1931KC01
|--Isoachlya Kauffman 1921KC01
|--Jaraia Němec 1912 (n. d.)KC01
|--Scoliolegnia Dick 1969KC01
|--Sommerstorffia Arnautov 1923KC01
|--Thraustotheca Humphrey 1893BP99
| `--*T. clavata (de Bary) Humphrey 1893 [=Dictyuchus clavatus de Bary ex Busgen 1882]BP99
|--Pythiopsis de Bary 1888KC01
| `--P. cymosaMNI02
|--Aplanopsis Höhnk 1952KC01
| |--A. spinosaVBD99
| `--A. terrestrisMNI02
|--Achlya Nees 1823 [=Hydronema Carus ex Rchb. 1828, Pringsheimina Kuntze 1891]KC01
| |--A. ambisexualisOC09
| |--A. bisexualisC-SC06
| |--A. debaryanaBP99
| `--A. klebsianaSM03
|--Saprolegnia Nees 1823 [incl. Cladolegnia Johannes 1955, Diplanes Leitg. 1868]KC01
| |--S. asterophoraHM88
| |--S. declinaLE18
| |--S. feraxC-SC06
| |--S. monoicaKC01
| `--S. parasiticaPHK96
`--Dictyuchus Leitgeb 1868BP99
|--*D. monosporus Leitgeb 1869-1870 [incl. D. anomalus Nagai 1931, D. carpophorus, D. magnusii, D. sterile]BP99
|--D. achlyoides Coker 1927BP99
|--D. lucknowensis Rai & Misra 1978BP99
|--D. missouriensis Couch 1931BP99
| |--D. m. var. missouriensisBP99
| `--D. m. var. moruzii Toma 1970BP99
|--D. pisci Khulbe & Sati 1983BP99
|--D. polysporusBP99
|--D. pseudachlyoides Beneke 1948BP99
|--D. pseudodictyon Coker & Braxton ex Couch 1931BP99
`--D. variabilis [=Brevilegnia variabilis]BP99

*Type species of generic name indicated

References

[BP99] Blackwell, W. H., & M. J. Powell. 1999. Taxonomic summary and reconsideration of the genetic concept of Dictyuchus. Mycotaxon 73: 247–256.

[C-SC06] Cavalier-Smith, T., & E. E.-Y. Chao. 2006. Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). Journal of Molecular Evolution 62: 388–420.

Dick, M. W. 2001. Straminipilous Fungi: Systematics of the Peronosporomycetes including accounts of the marine straminipilous protists, the plasmodiophorids and other similar organisms. Kluwer Academic Publishers.

[HM88] Hoshaw, R. W., & R. M. McCourt. 1988. The Zygnemataceae (Chlorophyta): a twenty-year update of research. Phycologia 27 (4): 511–548.

Johnson, T. W., Jr, R. L. Seymour & D. E. Padgett. 2002. Biology and systematics of the Saprolegniaceae. http://dl.uncw.edu/digilib/biology/fungi/taxonomy%20and%20systematics/padgett%20book/.

[KC01] Kirk, P. M., P. F. Cannon, J. C. David & J. A. Stalpers. 2001. Ainsworth & Bisby’s Dictionary of the Fungi 9th ed. CAB International: Wallingford (UK).

[LE18] Lax, G., Y. Eglit, L. Eme, E. M. Bertrand, A. J. Roger & A. G. B. Simpson. 2018. Hemimastigophora is a novel supra-kingdom-level lineage of eukaryotes. Nature 564: 410–414.

[MNI02] Moriya, M., T. Nakayama & I. Inouye. 2002. A new class of the stramenopiles, Placididea classis nova: description of Placidia cafeteriopsis gen. et sp. nov. Protist 153: 143–156.

[OC09] Okamoto, N., C. Chantangsi, A. Horák, B. S. Leander & P. J. Keeling. 2009. Molecular phylogeny and description of the novel katablepharid Roombia truncata gen. et sp. nov., and establishment of the Hacrobia taxon nov. PLoS One 4 (9): e7080.

[PHK96] Prescott, L. M., J. P. Harley & D. A. Klein. 1996. Microbiology 3rd ed. Wm. C. Brown Publishers: Dubuque (Iowa).

[SM03] Saldarriaga, J. F., M. L. McEwan, N. M. Fast, F. J. R. Taylor & P. J. Keeling. 2003. Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage. International Journal of Systematic and Evolutionary Microbiology 53: 355–365.

[VBD99] Voglmayr, H., L. J. Bonner & M. W. Dick. 1999. Taxonomy and oogonial ultrastructure of a new aero-aquatic peronosporomycete, Medusoides gen. nov. (Pythiogetonaceae fam. nov.) Mycological Research 103 (5): 591–606.

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