Systematics Of Fungi

In the last edition of this book (Taylor and Taylor, 1993), fungi and fungal-like organisms were described within a stratigraphic framework, and when possible, comments were offered on where they might fit within a modern classification of the Kingdom Fungi. With more information now available about fungal diversity through time, and many more specimens known in greater detail, many of the fossil taxa can now be discussed within the context of modern fungal groups.

Phylogeny of the fungi was once based on morphology and, in some cases, characteristics in laboratory cultures. Today, the fungal tree (FIG. 3.1) of life is constantly refined using various molecular sequences. Most analyses include five Phyla within the fungi, three of which, the Glomeromycota, Ascomycota, and Basidiomycota, are considered monophyletic. The other fungi, which are considered to be the earliest-diverging fungi based on molecular phyl-ogenies, include the paraphyletic groups, Chytridiomycota and Zygomycota. See Blackwell et al. (2006) for a summary of progress on the fungal tree of life, as well as the special issue of Mycologia, A Phylogeny for Kingdom Fungi (98(6), December 2006).

Chytridiomycota

Members of this phylum are the only fungi that produce motile spores (zoospores) at some stage in their life cycle. Today chytrids are found in both soil and freshwater, with many functioning as saprotrophs and some as parasites (FIG. 3.16). Phylogenetic studies based on molecular markers view the chytrids as an early diverging, probably para-phyletic group within the Kingdom Fungi and the sister group of the remaining non-flagellated fungi (Zygomycota, Glomeromycota, Ascomycota, Basidiomycota) (James et al., 2006a). Increased resolution within the classification of living members of the Chytridiomycota is occurring at several levels (Letcher et al., 2005; James et al., 2006b). For

FIGURE 3.16 Chytrid (arrow) with discharge papillae attached to pollen grain (Extant). Bar = 25 pm. (Courtesy D. Barr.)
FIGURE 3.17 Chytrid zoosporangia embedded in outer wall of Palaeonitella cranii cell. Bar = 20 pm.

FIGURE 3.18 Detail of chlamydospore wall showing mycoparasite developing between wall layers (Devonian). Bar = 12pm.

FIGURE 3.19 Chlamydospore with mycoparasite developing between wall layers (arrow) (Devonian). Bar = 20 pm.
FIGURE 3.20 Several chytrid zoospores. Arrow indicates flagel-lum (Devonian). Bar = 10 pm.

FIGURE 3.21 Several chytrid zoosporangia on the surface of a land plant spore. Arrow shows zoosporangium exit site (Devonian). Bar = 10 pm.

FIGURE 3.18 Detail of chlamydospore wall showing mycoparasite developing between wall layers (Devonian). Bar = 12pm.

FIGURE 3.21 Several chytrid zoosporangia on the surface of a land plant spore. Arrow shows zoosporangium exit site (Devonian). Bar = 10 pm.

example, at the molecular level, the relationship between members of the Chytridiomycota and Glomeromycota is strengthened by the presence of certain tubulin genes in both groups (Corradi et al., 2004).

Although there have been some putative chytrids described from Cambrian rocks (see Butterfield, 2005 for a review), the best-preserved forms are from the Lower Devonian Rhynie chert (FIG. 3.17) (Illman, 1984; Taylor et al., 1992). These fossils possess thalli and discharge tubes (FIGS. 3.18 and 3.19) similar to those in certain modern chytrids, and the preservation is so detailed that it is possible to demonstrate the presence of a single flagellum (FIG. 3.20) on a fossil zoospore (Taylor et al., 1992). These fossil chytrids possess thalli that are epi- and endobiontic (living on or within other organisms), and are associated with land plants, spores (FIG. 3.21), and algae (FIG. 3.22), as well as occurring isolated in the matrix. One especially interesting form is Palaeoblastocladia (Remy et al., 1994), a fungus that shares many features with members of the extant Blastocladiales

FIGURE 3.22 Chytrid zoosporangium. Arrow indicates position of discharge tube (Devonian). Bar = 20 pm.

(FIG. 3.23). Palaeoblastocladia milleri consists of thalli that were produced beneath the cuticle of stems of Aglaophyton and extended out from the surface about 0.5mm (FIG. 3.24). Some thalli had terminal zoosporangia (FIG. 3.25 ), whereas others produced pairs of terminal gametangia (FIG. 3.26 ) . This complement of characters suggests that P. milleri possessed an isomorphic alternation of generations with sexual reproduction, a combination of features that is very rare in modern fungi. It is suggested that P. milleri was a sapro-trophic, but other Rhynie chert chytrids are believed to have been parasites. Despite the small size of chytrids, their ubiquity in the Rhynie chert provides the opportunity to study their life history biology (FIG. 3.27), since various developmental stages are preserved.

Geologically younger fossil chytrids are also known (FIG. 3.28). Some of the first late Paleozoic chytrids to

FIGURE 3.23 Life history of Palaeoblastocladia milleri.

FIGURE 3.24 Two tufts (arrows) of Palaeoblastocladia milleri extending from epidermis of Aglaophyton axis (Devonian). Bar = 400 pm.

FIGURE 3.22 Chytrid zoosporangium. Arrow indicates position of discharge tube (Devonian). Bar = 20 pm.

FIGURE 3.24 Two tufts (arrows) of Palaeoblastocladia milleri extending from epidermis of Aglaophyton axis (Devonian). Bar = 400 pm.

FIGURE 3.25 Zoosporangium of Palaeoblastocladia milleri showing zoospores with dark central body (Devonian). Bar =15 |im.
FIGURE 3.27 Life history of a Devonian chytrid.
FIGURE 3.28 Thick-walled lycopsid spore containing fungal spores (chytrids?) (Pennsylvanian). Bar = 225 pm.
FIGURE 3.29 Oochytrium lepidodendri in Lepidodendron trac-heids (Mississippian). Bar = 20 pm. (Courtesy N. Dotzler.)

be accurately identified were Grilletia spherospermii and Oochytrium lepidodendri (FIG. 3.29) which occur in Carboniferous gymnosperm seeds and anatomically preserved tissues of the lycopsid Lepidodendron sp. (Renault and Bertrand, 1885a (FIG. 3.32 ) ; Renault, 1895, 1896a). These authors not only related these fossils to modern chytrid genera but also suggested that they represented parasitic fungi. Other microfungal remains associated with permineralized Lepidodendron tissues are more difficult to interpret (FIGS. 3.30, 3.31). Fossil chytrids (FIG. 3.33),

FIGURE 3.30 Arthroon rochei, thick-walled spore in periderm of Lepidodendron (Mississippian). Bar = 100 pm. (Courtesy N. Dotzler.)
FIGURE 3.31 Palaeomycesgracilis. (Mississippian). Bar = 35 pm. (Courtesy N. Dotzler.)

FIGURE 3.32 Paul Bertrand.

FIGURE 3.34 Several chytrids attached to substrate (Extant). Bar = 50pm. (Courtesy D. Barr.)

FIGURE 3.32 Paul Bertrand.

FIGURE 3.33 Numerous chytrids on surface of fungal spores (Devonian). Bar = 20 pm.

FIGURE 3.35 Saccate pollen grain with two chytrid zoospor-angia (arrows) attached (Pennsytvanian). Bar = 25 pm.

like their modern relatives, are often found on spores and pollen grains (FIG. 3.34) in bodies of water. Millay and Taylor (1978a) described epibiotic and endobiotic chytrid thalli (FIGS. 3.35, 3.36) in association with Pennsylvanian cordaitean pollen grains (Millay and Taylor, 1978a). Some of the chytrid zoosporangia recovered from the Eocene Green River Formation, which is known for its excellent preservation, are so nearly identical to those of modern forms that the fossils are assigned to living genera (Bradley, 1964, 1967).

Zygomycota

Zygomycetous fungi are distinguished by the production of thick-walled zygospores (non-flagellated) that form in a

FIGURE 3.36 Epibiontic chytrid zoosporangium extending from corpus wall of pollen grain (Pennsylvanian). Bar = 10 pm.
FIGURE 3.37 Suggested reconstruction of Endochaetophora antarctica thought to represent an ascomycete sporocarp (Triassic).

special sporangium, the zygosporangium, following gametang-ial fusion. Hyphae are generally aseptate and asexual reproduction occurs by the formation of internally produced spores. The group is highly diverse and includes saprotrophs (e.g., black bread mold) and certain pathogens, including some that infect other fungi, called mycoparasites. Some forms live as obligate symbionts within the gut of various arthropods (Lichtwardt et al., 1999; 2001). The Zygomycota are currently interpreted as paraphyletic and are believed

FIGURE 3.38 Dubiocarpon (Pennsylvanian). Bar = 175 pm.

to have diverged from the chytrids before the colonization of the land. Two classes are currently recognized (White et al., 2006): Zygomycetes and Trichomycetes. The only fossil record for the Trichomycetes will be discussed under the section "Fungi-Animal Interactions".

Various spore-like bodies that are now interpreted as zygo-mycetous fungi occur in permineralized peat (FIG. 3.37), especially in Carboniferous coal balls. The discovery of these unique structures, termed sporocarps, is no doubt directly related to the long history of the study of vascular plants in coal balls. The fungal affinities of these fossils are based on the structure of the wall, which consists of aseptate, interlaced hyphae. Some of the most common forms are spherical and < 1 mm in diameter. The most common morphogenera include Sporocarpon, Dubiocarpon (FIG. 3.38), Mycocarpon, Coleocarpon, and Traquairia (FIG. 3.39) (Stubblefield et al., 1983). Mycocarpon, a common Middle Pennsylvanian form, consists of a central spore-like structure ~550pmin diameter surrounded by a wall of interlaced, hypha-like cells four layers thick. Inside is an amorphous, cuticle-like membrane. In some species, for example M. bimuratus, the central cavity is filled with small spores. In Sporocarpon, the sporocarp is smaller (200 pm) and constructed of a pseudoparenchymatous tissue,

FIGURE 3.39 Traquairia williamsonii sporocarp (Carboniferous). Bar = 1GGpm.

which extends outward into numerous narrow, conical processes, each 6-7 cells high and 1-3 cells wide. Another form, Dubiocarpon , is distinguished by radially oriented, elongate cells that extend out from the sporocarp wall as spines, some with bifid tips. The most ornate form is Traquairia , a fungus that was initially described from the Lower Coal Measures of Great Britain by Carruthers (1872a) , Since that time, numerous specimens have been reported from many localities in Pennsylvanian rocks (Stubblefield and Taylor, 1983). Individual specimens are roughly spherical and up to 1 mm in diameter. The wall is complex, with the outer portion constructed of branching hyphae, some of which are organized into hollow spines. In Roannaisia , from the Visean of central France, the hyphae branch and the lumen of the sporocarp contains a single, multilayered spore (Taylor et al., 1994b).

As noted earlier, some of these sporocarps contain one to several spherical structures in the central lumen (FIG. 3.40). Initially these fungi were interpreted as ascomycetes, and the sporocarps as closed ascocarps (cleistothecia). Larger spherical structures inside would represent asci (sporangia), and smaller ones, ascospores (Stubblefield and Taylor, 1988). These sporocarps are now interpreted as zygomyc-etes, however, and the large, inner spore-like body represents a zygospore, similar to those produced in mycelial sporocarps of modern Mucorales (White and Taylor, 1989a) , The smaller internal spores reported in some sporocarps (formerly interpreted as ascospores) are now regarded as mycoparasites, most likely some type of chytrid.

FIGURE 3.40 Sporocarp of Dubiocarpon containing several larger spores (Pennsylvanian). Bar = 225 |m.

An interesting fossil believed to be a zygomycete is Protoascon missouriensis, a fungus found within a seed-like structure in a Pennsylvanian coal ball from Missouri, USA (Batra et al., 1964). The description is based on multiple specimens of a bulb-like structure ~ 150 pm diameter (FIG. 3.41). At one end is a whorl of 12 elongate, aseptate appendages (FIG. 3.42). The appendages are curved to form a loose, basket-like structure which surrounds a highly ornamented sporangium containing a single, thick-walled spore. As the name suggests, this fossil was initially thought to be an asco-mycete, but later reinterpreted as a chytrid (Baxter, 1975), and most recently as a zygomycete (Taylor et al., 2005a). Based on reexamination of the type material and additional specimens, Taylor et al. (2005a) concluded that the aseptate appendages (or suspensors) partially enclose a sporangium, which is either an azygosporangium (asexual) or a zygospor-angium, containing a single, thick-walled spore (FIG. 3.43).

Glomeromycota

The Glomeromycota are a clade that was instituted based on rDNA phylogenies of living members (Schüssler et al., 2001; Redecker and Raab, 2006). The phylum, which includes the arbuscular mycorrhizal (AM) fungi, was formerly included

CHAPTER 3 FUNGI, BACTERIA, AND LICHENS SS

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