Pirozynski Fossil 2016

FIGURE 3.65 Aspergillus collembolorum, conidial head with radial chains of conidia (see FIG. 3.64) (Eocene). Bar = 25 pm. (Courtesy A. Schmidt.)

FIGURE 3.64 Aspergillus collembolorum, sporulating conidio-phores (see FIG. 3.63) (Eocene). Bar = 50pm. (Courtesy A. Schmidt.)

Stigmatomyces succini is a parasitic ascomycete that has been found attached to the thorax of a stalk-eyed fly preserved in Baltic amber (Rossi et al., 2005). It represents the earliest fossil account for the ascomycete order Laboulbeniales, an enigmatic group which is now considered to represent ascomycetes (Weir and Blackwell, 2001).

Basidiomycota

The Basidiomycota, a monophyletic sister group to the Ascomycota, includes ~3 0,000 extant species divided into three major lineages (subphyla): the rusts (Puccinomycotina), smuts (Ustilagomycotina), and mushrooms (Agaricomycotina). They are known from both terrestrial and aquatic habitats around the world and include important plant pathogens (e.g., wheat rust, corn smut), as well as the edible mushrooms. The most diagnostic feature of the basidiomycetes is the basidium (pl. basidia), a generally club-shaped cell where nuclear fusion (karyogamy) takes place and the structure upon which the sexual spores (basid-iospores) are produced. Some basidia are borne on complex, multicellular fruiting bodies, for example the mushrooms (FIG. 3.66). Other basidiomycete features include hyphal outgrowths termed clamp connections, and the presence of a dikaryon phase in the life cycle, a condition in which each cell in the thallus contains two nuclei. Some basidiomycetes are involved in ectomycorrhizal associations, whereas others are symbiotically associated with various insects, for example with leaf-cutter ants and termites. One example of a fungus-termite interaction is the Miocene-Pliocene termite trace fossil Microfavichnus, this ichnogenus is thought to represent fungus combs of fungus-growing termites (Duringer et al., 2007). The combs consist of alveolar masses in which the walls have a pelletal structure.

The Basidiomycota today play an important role in the carbon cycle by decaying organic matter, including wood;

Pair of nuclei fuse

Fertilization

Basidium \ Q

Portion of gill

Button

Diploid nucleus undergoes meiosis

Pair of nuclei fuse

Diploid nucleus undergoes meiosis

Basidiospores Sterigmata

Basidium

Meiosis

Basidiospores Sterigmata

Basidium

Basidium \ Q

Portion of gill

Button

Spore

Monokaryotic mycelium

Dikaryotic mycelium

FIGURE 3.66 Life history of basidiomycete fungus. (From Taylor and Taylor, 1993.)

Meiosis

Dikaryotic mycelium

Spore

Monokaryotic mycelium

FIGURE 3.66 Life history of basidiomycete fungus. (From Taylor and Taylor, 1993.)

presumed basidiomycetous fungi have been found as early as the Middle Devonian, not long after land plants first began producing secondary growth. There are a number of Carboniferous fossils that superficially resemble modern basidiomycetous fruiting bodies, or basidiocarps (Lindley and Hutton, 1831-1837; Lesquereux, 1877; Herzer, 1893; Hollick, 1910) (FIG. 3.67). Almost all of these reports, however, were later questioned and the specimens reinterpreted as non-fungal (Pirozynski, 1976b). The fact that there are so few reports of basidiomycetes associated with fossil wood is perplexing, since today they are the major decomposers of cellulose and lignin, the major components of plant cell walls.

One well-documented basidiomycete from the Pennsylvanian is Palaeoancistrus martinii, a fungus found in the tracheids of the fern Zygopteris (Dennis, 1970). There are several features of this fungus that suggest affinities with living saprotrophic members of the Basidiomycota. One of these is the presence of smooth, narrow, septate hyphae

(4.8 pm in diameter) that follow a straight course within the tracheids. Associated with the hyphae are both terminal and intercalary chlamydospores. Some hyphae possess incomplete clamp connections in which the hook of the clamp does not form a complete union with the hypha, whereas in others the clamp connections are well developed.

Another basidiomycete has been described in the secondary xylem of several Paleozoic and Mesozoic woods from Gondwana (FIG. 3.68), but in this case it is the symptoms caused by the fungus, in association with the fungus itself that provides the identification. The activities of this fungus result in the formation of numerous longitudinally oriented, spindle-shaped pockets of decay in the secondary xylem (FIG. 3.69), called pocket rot (Stubblefield and Taylor, 1986). In other regions of the secondary xylem, for example in the root Vertebraria and stems assigned to the morphoge-nus Araucarioxylon, septate hyphae with simple and medallion clamp connections are present (FIG. 3.70 ). The elongate,

CHAPTER 3 FUNGI, BACTERIA, AND LICHENS 95

FIGURE 3.67 Arthur Hollick.
Araucarioxylon
FIGURE 3.68 Cross section of Araucarioxylon wood showing symptom (white areas) of white pocket rot (Triassic). Bar = 2 cm.

spindle-shaped areas in the fossil are identical to the symptoms caused by modern white pocket rot fungi (Blanchette, 1980). Other structural features in the fossil woods indicate the sequential delignification of the secondary cell wall (FIG. 3.71), for example the loss of the middle lamella between the wood cells, and these are also characteristic of modern white rot fungi. Palaeofibulus is another fossil fungus with clamp connections (FIG. 3.72 ) and thick-walled

FIGURE 3.69 Fractured surface of extant wood showing elongate spindles (white) of white pocket rot. Bar = 1 cm.
FIGURE 3.70 Medallion clamp connection (arrow) i Araucarioxylon wood infested by pocket rot (Triassic). Bar : 20 pm. (From Stubblefield and Taylor, 1986.)

spores, known from Middle Triassic permineralized peat of Antarctica (Osborn et al., 1989). Investigations of wood-rotting fossil fungi offer the potential to indirectly examine the biochemical evolution of fungi, based on patterns and features associated with delignification and removal of cellulose from the host cell wall.

Some of the most common members of the Basidiomycota are the mushrooms (Hibbett, 2006). To date the oldest gilled mushrooms (Agaricales or agarics) come from amber. The oldest of these is Archaeomarasmius leggeti (FIG. 3.73) entombed in a piece of Late Cretaceous (Turonian; 9490 Ma) amber from the Raritan Formation of New Jersey, USA (Hibbett et al., 1997). The pileus, or cap of the mushroom, ranges from 3-6 mm in diameter and contains elliptical

FIGURE 3.71 Separation of wood cell wall layers due to fungal degradation (Triassic). Bar = 55 |m.
FIGURE 3.72 Palaeofibulus showing hyphae, spores, and clamp connection (arrow) (Triassic). Bar = 35 |m.

basidiospores up to 8|m long. Another gilled form is Protomycena electra from the younger Dominican amber (Miocene; 20-15Ma) (Hibbett et al., 1997); this mushroom is similar to the extant leaf-litter and wood-rotting genus Mycena. Coprinites dominicana is another gilled mushroom found in Dominican amber. It has a cap ~3.5mm in diameter with 28 gills extending from the lower surface (Poinar and Singer, 1990). The most recent homobasidiomycete reported from Dominican amber is Aureofungus yanig-uaensis (Hibbett et al., 2003). It is similar to the other fossil agarics in amber, and suggests that among certain homoba-sidiomycete lineages there has been relatively little morphological change since the Cenozoic, at least in those features that can be compared within the amber matrix.

Basidiomycetes that lack gills but possess large basidi-ocarps with poroid hymenophores (spore producing layers in the fruiting bodies) have been described from the

FIGURE 3.73 Archaeomarasmius leggeti (Cretaceous). (Courtesy D. Hibbert.)

fossil record as bracket, shelf, or polypore fungi (surveyed in Fleischmann et al., 2007). Members of this group are generally saprotrophs involved in the degradation of cellulose and lignin, but some are also parasites of woody plants. Quatsinoporites cranhamii is a fragment of an Early Cretaceous (Barremian) basidiocarp described from permineralized marine calcareous concretions of British Columbia, Canada (Smith et al., 2004). The hymenophore consists of numerous parallel tubes, each up to 540 |m in diameter. Appianoporites is also a poroid (bracket) fungus constructed of smaller tubes, from younger Eocene rocks from the eastern side of Vancouver Island, British Columbia. Both specimens possess septate hyphae; the basidiocarps are interpreted as persistent and placed in the Hymenochaetales. Another fossil polyporous fungus is Ganodermites liby-cus (FIG. 3.74) from the lower-middle Miocene (Neogene) of North Africa (Fleischmann et al., 2007). The basidia are clavate and produce elliptical basidiospores, each up to 6.5 |m long with two wall layers. The basidiocarp shows evidence of incremental growth and is placed in the extant family Ganodermataceae, a predominantly tropical group of fungi that are characterized by basidiospores with a double (so-called ganodermatoid) wall. The presence of tunnels containing fecal pellets in the basidiocarp indicates that this bracket fungus was visited by fungivores.

FIGURE 3.74 Ganodermites libycus, longitudinal thick section (polished surface) through the basidiocarp showing hymenophoral strata (H) (Miocene). Bar = 2 cm. (Courtesy BSPG.)

Basidiomycetes also form a variety of symbiotic associations with other organisms, including many families of temperate forest trees, for example Fagaceae and Pinaceae. Distinctive among these are ectomycorrhizae, estimated to occur on ~10% of plants. Ectomycorrhizae are characterized by intercellular hyphae that often form a loose aggregation, called a Hartig net, around the root tip. In addition, the fungal association can also cause a change in root morphology, making the roots shorter, wider, and more branched. The oldest evidence of ectomycorrhizae to date comes from the middle Eocene (50 Ma) Princeton chert of the Allenby Formation, British Columbia, an extraordinary site in which many whole plants are permineralized by silica (LePage et al., 1997). Ectomycorrhizal roots of Pinus from this site contain a dense aggregation of small septate hyphae that extend into the cortex of the roots and represent the Hartig net. This discovery represents another example of the long standing symbiotic relationship in a particular group of seed plants. It is unclear why the majority of living ectomycor-rhizae coevolved with woody rather than herbaceous plant hosts. Perhaps the structure and organization of the root, soil type, microbial community, or some other combination of biotic and abiotic factors favored ectomycorrhizal fungi over endomycorrhizal forms in certain hosts.

A striking example of the diversity of fossil basidi-omycetes is seen in a fossil specimen assignable to the Gasteromycetes, the group that contains the puffballs and some of the earthstars. Geastrum tepexensis (FIG. 3.75) is a compressed late Eocene basidiocarp (called a peridium in this group) approximately 2.5 cm in diameter from the Coatzingo Formation in Puebla, Mexico (Magallon-Puebla and Cevallos-Ferriz, 1993). The endoperidium (inner layer of the peridium) is circular and characterized by a small ostiole; ornamented spores <7pm in diameter were also

FIGURE 3.75 Geastrum tepexensis showing central endoperid-ium surrounded by triangular-shaped segments of the exoperidium (Cenozoic). Bar = 7.5 mm. (Courtesy S. R. S. Cevallos-Ferriz.)

found in the structure. Although the morphological features of the fossil make it difficult to place within a modern genus, this discovery does expand the geographic distribution of the Lycoperdales into the tropics during the Cenozoic. Extending the range further back into the Cretaceous is Geastroidea lobata, a compressed earthstar from Mongolia (Krassilov and Makulbekov, 2003).

Other Fungal Remains

Another group of fossil fungal remains includes the asexual stages (anamorphs) of Ascomycota and Basidiomycota; these have historically been called deuteromycetes, fungi imperfecti, conidial, or mitosporic fungi. Today most of these organisms are saprotrophs or weak parasites of terrestrial plants and a few aquatics. Since information on their sexual reproduction is incomplete, they are therefore placed in artificial groups, which are based on conidial characters, that is, asexual reproduction. Many of the small spores recovered from palynological samples represent conidiospores of these fungi.

The Coelomycetes are an artificial group known from temperate and tropical regions today. One form from the Cretaceous of Japan is Archephoma cycadeoidellae (Watanabe et al., 1999). It consists of mature pycnidia up to 250 pm wide that contain numerous smooth, aseptate conidia. In another form the conidia are elliptical and divided by a dark septum.

Other coelomycetes have been reported as epiphytes on dicot and grass leaves preserved in amber (Poinar, 2003).

Although paleomycology represents a very old subdiscipline of paleobotany, for reasons noted earlier almost all of the studies to date have focused on the description and identification of the fungi. The study of fossil fungi does, however, provide the opportunity to examine several levels of biotic and abiotic interactions that extend beyond the description and classification of the organisms (Stubblefield and Taylor, 1988). Studies of fossil fungi may examine symptoms of the host as well as the fungi themselves, and can reveal different levels of interaction, as well as providing indirect evidence of coevolutionary relationships between fungi and land plants. In some instances these may be beneficial levels of biological cooperation (e.g., mycorrhizae, lichens), whereas in others they indicate parasitic and pathogenic associations. Following are several examples of such interactions that have been determined based on the fossil record of fungi.

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