A Taxonomic Summary of Chytriomyces (Chytridiomycota)

A TAXONOMIC SUMMARY OF CHYTRIOMYCES (CHYTRIDIOMYCOTA)

PETER M. LETCHER and MARTHA J. POWELL

Department of Biological Sciences, The University of Alabama

Tuscaloosa, Alabama35487

ABSTRACT

The genus Chytriomyces was established by Karling to accommodate two similar species, C. hyalinus and C. aureus. The generic concept of Chytriomyces has become altered substantially from its original circumscription, mainly through attrition of utilizable generic characters, to its present simpler, yet less precise definition.Remaining reliable characters that help define Chytriomyces are: an epibiotic and operculate sporangium, and epibiotic resting spores. For each of the 34 species of Chytriomyces, a taxonomic description and ecological/distributional data are presented. The type of Chytriomyces is designated herein, and terminology pertinent to morphological features is discussed. A taxonomic key based on readily observable morphological character states, and figures derived primarily from the original literature, are presented to assist in species identification.

Key Words: chytrid, Chytridiomycetes, distribution, ecology, taxonomy.

INTRODUCTION

Karling (1945) established the genus Chytriomyces to accommodate two newly discovered aquatic chitinophilic species of zoosporic fungi. Chytriomyces hyalinus and Chytriomyces aureus were characterized by epibiotic operculate sporangia, extensive endobiotic rhizoids extending from a single rhizoidal axis that typically bore an apophysis or subsporangial swelling, posteriorly uniflagellate zoospores that swarmed in a vesicle outside the sporangium prior to release into the environment, and epibiotic resting spores that functioned as prosporangia in germination. Sexual reproduction and the sexual origin of the resting spore in C. hyalinus have been well documented (Koch 1959, Moore and Miller 1973, Miller 1977, Miller and Dylewski 1981).

The name Chytriomyces was proposed because of the characteristic Chytridium-like thallus exhibited by the newly described taxa. Karling (1945:363, 368) noted that except for the operculate sporangium, species of Chytriomyces were similar to species of Rhizidium (sensu Karling 1944), Phlyctochytrium, and Rhizophydium.Chytriomyces hyalinus and C. aureus were similar except for thallus color, and Karling did not designate one or the other as the type, nor has any other investigator.

As new species were discovered, the generic concept ofChytriomyces rapidly evolved. Karling may have anticipated such a process, for the original diagnosis, description, and discussion (Karling 1945) have subtle, implied, and occasionally contradictory addenda to the rather sparse original generic diagnosis, leaving open the potential for inclusion of wide morphological variation among the defining generic characters. Subsequent to Karling’s establishment of the genus, discoveries were made of epibiotic, operculate fungi that lacked one or more of the fundamental morphological generic characters (Fay 1947, Karling 1947, 1949). Incorporation of informal alterations to the generic concept ofChytriomyces by Karling (1948:332, 1949:352) and Dogma (1976:136) as well as formal amendments (Sparrow1960:538, Bostick 1968:98, Dogma1983:385) included the absence of fundamental generic characters.The conceptual evolution of the genus may simply be a natural progression from a narrow and restricted generic concept based on two similar specific taxa, to a much broadened concept useful for inclusion of taxa exhibiting wide morphological variation. However, defining species of Chytriomyces through the exclusion of hallmark generic characters(features such as an apophysis or subsporangial swelling, an exogenous discharge vesicle, zoospores swarming in that vesicle prior to release into the environment, and an epibiotic resting spore) is inconsistent with the original generic concept. In the extreme, the genus has evolved to incorporate species in which the sporangium is simply epibiotic and operculate. Those two characters alone cannot justify species inclusion in the genus Chytriomyces, for they also delineate the genus Chytridium Braun (cf. Sparrow 1960).

The purpose of this taxonomic summary is to assemble taxonomic descriptions, illustrations, geographical distributions, substrates, hosts, and references for all species described to date. Assembly of this publication updates prior monographs and taxonomic summaries(Sparrow 1960, Longcore 1996). An identification key based on morphological characters is provided. Figures have beenredrawneither from original literature with permission, as all living authors and extant publications have been asked (see Acknowledgments), or from living material.

THE TYPE OF CHYTRIOMYCES

As for most Chytridiomycota, inChytriomyces no actual specimen remains from the original material that Karling examined and based his description. For the genus Chytriomyces, C. aureus and C. hyalinus were described sequentially in the same publication (Karling 1945), yet neither was designated as the type. Except for sporangial color, the two species are similar (Scogin and Miller 1971), and neither species is more like the generic description than the other. However, significantly more research (Koch 1959, Bostick 1968, Hasija and Miller 1971a,b, Scogin and Miller 1971, Moore and Miller 1973, Miller 1977, Miller and Dylewski 1981, Dorward and Powell 1982, 1983, Powell 1983, 1994) has been devoted to C. hyalinus, the form that appears more prevalent in nature, than to C. aureus (Willoughby 1959, Hasija and Miller 1971, Scogin and Miller 1971, Dorward and Powell 1982, 1983). In a practical sense, C. hyalinus is the species that is most frequently encountered when culturing from substrata, and therefore is most readily identified with the original generic description. Consequently, we herein designate Chytriomyces hyalinus Karling (1945), Am. J. Bot. 32:362-369, figs. 46-61 as the lectotype of the genus (ICBN Article 9.2, ICBN 2000).

Dogma (1976) synonymized Amphicypellus (Ingold 1944) with Chytriomyces, indicating that Chytriomyces (the later of the two genera to be described) is a “nomen conservandum”, but no conservation of the name in the International Code of Botanical Nomenclature (2000) has been achieved. Thus, in our summary we are following the precedent set by Dogma, with the observationfor this genus to be legitimate, conservation of the name Chytriomyces would have to be achieved.

TERMINOLOGY

For clarity it is essential to define several morphological terms. The thallus is considered to be the entire fungus, which may be differentiated at maturity into fertile and somatic portions. Zoospores, sporangia, rhizoidal systems, and resting spores are all parts of the thallus, even though they may be physically distinct and exist in different temporal and spatial situations. The rhizoidal system is the extension of the chytrid thallus that functions as an anchoring and absorptive apparatus and is composed of rhizoids and, on occasion, a single (rarely more than one) apophysis, which is synonymous with the terms subsporangium andsubsporangial swelling (Karling 1936). The three terms that refer to the apophysate condition have been used synonymously and indiscriminately for morphologically similar but developmentally distinct structures (cf. Karling 1936, 1945,Sparrow 1936, Johnson 1971). Karling (1936) used the terms to describea swelling of the germ tube subsequent to exogenous migration of the nucleus from the zoospore cyst/case into the germ tube. This nuclear event and the concurrent apophysate morphological condition occurs in many species of Chytridium, and the apophysis usually forms within(and rarely externally upon) the substrate. Subsequent to the exogenous (undergoing development outside of the zoospore case) nuclear migration, the nucleus returns to the zoospore case by way of the germ tube. Thereendogenous development (undergoing development inside the zoospore case, which at this point is termed the incipient sporangium) leads to development of a multinucleate sporangium. The entire process is known as endo-exogenous development (Karling 1936). In this context, an apophysis is a structural condition and component of the rhizoidal system resulting from a nuclear event. The timing of this type of development is sequential in that the apophysis forms prior to enlargement of the incipient sporangium.Conversely, in many species of the Chytridiales, and in the absence of endo-exogenous development, the initial rhizoidal axis may nonetheless become swollen, inflated, or bulbous in varying degrees (Barr 1984). Anapophysis or subsporangial swelling of that nature is simply a structural condition of the rhizoidal system, developed independent of any functional, migratory, nuclear event. The timing of this type of developmental pattern is such that the endogenous development of the incipient sporangium and the development of the apophysis occur simultaneously.

Endo-exogenous development has not been directly observed in any of the species of Chytriomyces. Karling (1947:338) elucidated the developmental course of the nucleus for all species of Chytriomyces studied to that date, and made no mention of the endo-exogenous development that he described (Karling 1936) for Chytridium lagenaria (cf.Blackwell et al. 2002) Additionally, Karling (1945:367) stated that the development of C. aureus and C. hyalinus was so similar to that of Rhizidium braziliensis and R. laevis (Karling 1944) that a detailed description was unnecessary. There is no mention of endo-exogenous development with either of those species of Rhizidium. It is clear that Karling used the term “apophysis” for a structural feature of the initial rhizoidal axis, both dependent on (as in Chytridium lagenaria) as well as independent of (as in Chytriomyces hyalinus) anuclear migration event. We now know that the various structures termed “apophysis,” “subsporangium,” and “subsporangial swelling” are not necessarily homologous structures. As examples of the terminology, the sporangium and resting spore of C. cosmaridis Karling (Figs. 36-39) and C. stellatus Karling (Figs. 66-68) were described as apophysate. The initial rhizoidal axis below the sporangium of C. nodulatus Haskins (Figs. 16, 19) was considered a subsporangial swelling.

It is from the germ tube, whether swollen into an apophysis or not, that the rhizoidal system develops.Rhizoids are usually filamentous, and may be widely extended andfinely branched. The sporangia of C. mortierellae (Figs. 137, 138) and C. multioperculatus (Fig. 141) illustrate this feature. Like a rhizoid, a haustorium is an absorbing organ, but strictly of aparasitic fungus, and is often sac-shaped, club-shaped, bluntly lobed or coralloid (Karling 1932:43). Haustoria bear little or no resemblance to the more delicate thread-like extensions that constitute rhizoids. The sporangia of C. gilgaiensis (Figs. 52, 53) are subtended bylobed haustoria, and C. cosmaridis (Figs. 36-38) by spherical haustoria.

The term epibiotic refers to a portion of the thallus living or making growth on the surface of the substrate, and here we synonymize it with the term extramatrical. All but one species of Chytriomyces have epibiotic sporangia. The term interbiotic refers to any portion of the thallus living among, near, or between substrata. Chytriomyces elegans (Figs. 22-26) has interbiotic sporangia. The term endobiotic refers to a portion of the thallus living or growing within the substrate. All members of Chytriomyces have endobiotic rhizoids or haustoria. In this work, endobiotic is synonymous with the term intramatrical.

In the taxonomic descriptions that follow, characteristics of the zoospore ultrastructure have not been included, as few species have been investigated at that level. For those species that have been investigated, the reference is cited within the description. However, the organization of the microbody-lipid globule complex has been elucidated (Powell 1978, 1983, Powell and Roychoudhury 1992) as it relates to taxonomic and phylogenetic implications, as have aspects of the flagellar apparatus (Barr 1980, 1988, 1990, 2001,Barr and Desaulniers 1988, Barr and Hadland-Hartmann 1978, Dorward and Powell 1982).

THE SPECIES OF CHYTRIOMYCES: TAXONOMIC DESCRIPTIONS, REFERENCES AND DISTRIBUTION

1. CHYTRIOMYCESANGULARIS Longcore

Mycologia 84:443, figs. 1-29. 1992.

PLATE 6, figs. 175-179

Vegetative: Thallus epibiotic. Reproductive: Sporangium longer than wide, ellipsoid, gibbose or angular, hyaline, diameter 12 µm, height 22 µm, sessile or having an extramatrical stalk; sporangial wall smooth, with rounded to angular projections. Rhizoidal system: Rhizoidal axis only slightly thicker than remainder of the rhizoids, rhizoids branch from main axis at some distance from the sporangium. Zoospore, discharge: Operculum present, not persistent, apical or subapical, saucer shaped, diameter 7-8 µm, discharge pore single; discharge vesicle absent, zoospore discharge as an initial burst, zoospores quiescent for 1-2 minutes after sporangial dehiscence and prior to motility,zoospore motility extrasporangial only. Zoospore, microscopic: Zoospores ovoid, 4-5µmin diameter,single lipid globule hyaline, flagellum 30 µm long.Zoospore, ultrastructure: Longcore 1992.Resting spore: Epibiotic, ovoid, angular or gibbose, thick-walled, smooth, hyaline. Ecology and Distribution: From water, on pollen, Longcore (loc. cit.: Maine),from soil, Letcher and Powell (unpublished observation, Virginia, North Carolina, and Utah), US.

2. CHYTRIOMYCES ANNULATUS Dogma

Nova Hedwigia 18:349, figs. 1-18. 1969.

PLATE 6, figs. 163-168

Vegetative: Thallus epibiotic or interbiotic. Reproductive: Sporangium pyriform or obpyriform, hyaline, diameter 10-31 µm, height 14-38 µm, having an extramatrical stalk; sporangial wall ornamented with 3-8 proximal collar-like annulations. Rhizoidal system: Apophysis spherical (not necessarily as a subsporangial swelling), diameter 8-15 µm, or saccate, 4-7 µm × 10-15 µm; filamentous rhizoids limited, sparsely branched. Zoospore, discharge: Operculum present, persistent, apical, saucer shaped, diameter 7-10 µm, not rigid after discharge, discharge pore single; discharge vesicle absent, zoospore discharge as a mass, zoospore motility extrasporangial only. Zoospore, microscopic: Zoospores spherical, 4.7-6.5 µm in diameter, single lipid globule hyaline, flagellum 29-30 µm long. Zoospore, ultrastructure: Unknown. Resting spore: Spherical or subspherical, 8-15 µm, hyaline, on an extramatrical stalk, containing a single globule. Ecology and Distribution: From leaf litter and soil samples, saprophytic on pine pollen, sweet gum pollen, and snake skin, weakly parasitic on Rhizophydium coronum sporangia and Rhizophlyctis rosea rhizoids, Dogma(loc. cit.: Michigan, Wisconsin, North Carolina, Maine, Virginia, New Hampshire, Vermont),on pollen, Letcher and Powell(2001:1031; 2002:766, Virginia), US; on pollen, Booth and Barrett(1971:362, E. Arctic), Lee(2000:60, Manitoba), CANADA; from water, on chitin, Czeczuga and Godlewska (1998), POLAND.

Based on actual observations of this organism (Letcher and Powell 2001, 2002), the species is emended as follows: Chytriomyces annulatus Dogma emend. Resting spore spherical, diameter 8-15 µm, subspherical or ovoid, 5-8 µm × 7-12 µm, the wall smooth or rarely with a single proximal collar-like annulation; with an extramatrical stalk and an endobiotic, spherical apophysis;contents of the resting spore a single large central hyaline globule occasionally surrounded by several smaller globules.

3. CHYTRIOMYCES APPENDICULATUS Karling

Bull. Torrey Bot. Club 74:335, figs. 16-37, 43-48. 1947.

PLATE 3, figs. 70-74

Vegetative: Thallus epibiotic. Reproductive: Sporangium highly variable in size and shape:ovoid, pyriform, transversely flattened or reniform, hyaline to brown, diameter 10-80-(250) µm, height 10-50 µm, sessile; sporangial wall appendiculate or smooth. Rhizoidal system: Subsporangial swelling rarely present; main rhizoidal axis up to 18µmin diameter; filamentous rhizoids well developed, branched, coarse. Zoospore, discharge: Operculum present, not persistent, apical, subapical or lateral, saucer shaped, diameter 6-14 µm, discharge pore single; discharge vesicle present; zoospore discharge as a mass, zoospores swarming in vesicle outside sporangium before dispersal, vesicle separating from sporangium, zoospore motility extrasporangial only. Zoospore, microscopic: Zoospores ovoid, 4-6 µm in diameter, single lipid globule hyaline, flagellum 28-32 µm long.Zoospore, ultrastructure: Unknown. Resting spore: Epibiotic, spherical, diameter 10-25 µm, or appendiculate, thick-walled, smooth, brown, and coarsely granular with a central vacuole; upon germination functions as a prosporangium . Ecology and Distribution: In water and soil, on chitin, Karling (loc. cit., Virginia, New Jersey, New York, Connecticut), in water, on chitin, Miller (1965:223, Virginia), from soil, Dogma (1969:355, Michigan), US; from soil and water, on chitin, Willoughby (1961:306), from soil, on chitin, Willoughby (1962:122), UK; from soil, on pollen and keratin, Booth (1971b:951, British Columbia), CANADA; from soil, on chitin, Karling (1967:122), NEW ZEALAND; from water, on chitin and keratin, Kiran (1993), INDIA.

“One of the peculiarities of this very distinct species is the tendency for some sporangia to form large amounts of “slime” beneath the area of discharge. In some material no vesicle was formed” (Sparrow 1960:544).

4. CHYTRIOMYCES AUREUS Karling

Am. J. Bot. 32:363, figs. 28-45. 1945.

PLATE 1, figs. 6-11

Vegetative: Thallus epibiotic. Reproductive: Sporangium spherical or ovoid, golden-red, diameter 8-40 µm, sessile, sporangial wall smooth. Rhizoidal system: Apophysis spherical or subspherical, diameter 3-6 µm, filamentous rhizoids well developed, branched or coarse. Zoospore, discharge: Operculum present, not persistent, apical, saucer shaped; discharge pore single; discharge vesicle present; zoospores swarming in vesicle outside sporangium before dispersal; vesicle continuous with sporangium, zoospore discharge as a mass, zoospore motility extrasporangial only. Zoospore, microscopic: Zoospores ovoid, 3-3.5 µm in diameter, single lipid globule golden-red, flagellum 22-25 µm long. Zoospore, ultrastructure: Dorward and Powell 1982, 1983. Resting spore: Epibiotic, spherical, 6-20 µm, or ovoid, 6-10 µm × 12-16 µm, thick-walled, smooth, golden brown, with numerous closely packed granules or globules. Ecology and Distribution: In water, in exuviae of mayflies and on chitin, Karling, (loc. cit., Connecticut, New York, Virginia), on pollen, Miller (1965:223, Virginia), in soil, on chitin, Dogma (1969:357, Michigan), Hasija and Miller (1970:1034, Ohio), US; in water, on chitin, keratin, and cellulose, Willoughby (1959:67, 1961:306), UK; in soil, on chitin, Karling (1967:121), NEW ZEALAND; in soil, on cellulose, Hassan (1993:35), EGYPT; in water, on chitin, Karling (loc. cit.), BRAZIL.

5. CHYTRIOMYCESCLOSTERII Karling

Bull. Torrey Bot. Club 76:352, figs. 1-5. 1949.

PLATE 1, figs. 29-35

Vegetative: Thallus epibiotic. Reproductive: Sporangium spherical or pyriform, hyaline, diameter 5-25 µm, sessile; sporangial wall smooth. Rhizoidal system: Rhizoids a single, sparsely branched axis, sometimes extending to 120 µm. Zoospore, discharge: Operculum present, not persistent, apical, saucer shaped, diameter 4-6 µm, discharge pore single, with a discharge papilla; discharge vesicle present, zoospores swarming in vesicle outside sporangium before dispersal, vesicle continuous with sporangium, zoospore discharge as a mass, zoospore motility extrasporangial only. Zoospore, microscopic: Zoospores spherical, 2-2.5 µm in diameter,single lipid globule hyaline, flagellum 9-12 µm long. Zoospore, ultrastructure: Unknown. Resting spore: Epibiotic, spherical or ovoid, 7-12 µm, hyaline, thick-walled, smooth, with a large central globule surrounded by several smaller ones. Ecology and Distribution: In water, parasitic on Closterium rostratum Karling (loc. cit.), US.

“Apparently confined to one host species. It does not attack other species of Closterium or members of other genera of green algae” (Sparrow 1960:541).

6. CHYTRIOMYCES CONFERVAE (Wille) Batko

Zarys Hydromikologiip. 210, fig. 319. 1975.