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Palaeo-Electronica.Org Palaeontologia Electronica http://palaeo-electronica.org A POSSIBLE ENDOPARASITIC CHYTRIDIOMYCETE FUNGUS FROM THE PERMIAN OF ANTARCTICA J.L. García Massini Department of Geological Sciences, Southern Methodist University PO Box 750395 Dallas TX 75275-0395 ABSTRACT Several stages of the life cycle of an endoparasitic fungus of the Chytridiomycota, here assigned to the extant genus Synchtrium, are described as the new species per- micus from silicified plant remains from the Late Permian (~250 Ma) of Antarctica. The thallus of Synchtrium permicus is holocarpic and monocentric and consists of thick- walled resting sporangia, thin-walled sporangia, and zoospores in different stages of development. A life cycle is hypothesized from the range of developmental stages. The life cycle begins when zoospores encyst on the host cell surface, subsequently giving rise to thin-walled sporangia with motile spores. Some zoospores (haploid) function as isogamous gametes that may fuse to produce resting sporangia (diploid). Roots, leaves, and stems of plants are among the tissues infected. Host response to infection includes hypertrophy. Morphological and developmental patterns suggest similarities with the Synchytriaceae (Chytridiales), particularly with Synchytrium. Previous records of chytridiomycetes are known from the Devonian Rhynie Chert and from the Carbonif- erous and the Eocene of the northern hemisphere; this report is the first on chytridio- mycetes from the Permian. KEY WORDS: Endoparasitic fungi, fossil fungi, chytridiomycetes, Synchytrium INTRODUCTION genetic studies using protein sequences suggest that they originated in the Precambrian, 1400-1600 The Chytridiomycota are considered to be million years ago (Heckman et al. 2001). An primitive organisms whose affinities with all other ancient origin for the group is indicated by the fungi are debatable (Bowman et al. 1992; Powell diversity of life forms (parasites, saprotrophs, and 1993; Barr 2001; Lutzoni et al. 2004). They are mutualists), the variety of modes of sexual repro- regarded as basal to the remaining fungi based on duction, the characteristic flagellar apparatus, the their simple thalli and the formation of flagellated simple but diverse thallus morphology, and the spores (Alexopoulos et al. 1996; Paquin et al. strict dependence on moist conditions (Sparrow 1997; Webster and Weber 2007). Molecular phylo- 1960; Karling 1977; Powell 1993). In addition, a PE Article Number: 10.3.16A Copyright: Palaeontological Association December 2007 Submission: 17 October 2007. Acceptance: 7 November 2007 García Massini, J.L., 2007. A Possible Endoparasitic Chytridiomycete Fungus from the Permian of Antarctica. Palaeontologia Electronica Vol. 10, Issue 3; 16A:14p; http://palaeo-electronica.org/2007_3/121/index.html GARCÍA MASSINI: PERMIAN ENDOPARASITIC FUNGUS number of studies have shown that chytridio- and Stubblefield 1987). Included are epibiotic and mycetes are polyphyletic, which is consistent with endobiotic zoosporangia on cordaitean pollen the morphological and ecological diversity of its grains (Millay and Taylor 1978) and several stages members (James et al. 2000; Lutzoni et al. 2004). of the life cycle of holocarpic and eucarpic forms Chytridiomycetes comprise five orders based (Taylor et al. 1992). The objective of this paper is to on both morphological and molecular characters report the presence of well-preserved zoospores, (Barr 1980, 2001; James et al. 2000). Barr (1980) and thin-walled and thick-walled sporangia com- introduced zoospore ultrastructure as the main prising several stages of the life cycle of a fungus diagnostic character for chytridiomycete phylog- that is morphologically and developmentally eny. Other morphological features include the pres- assignable to endobiotic chytridiomycetes, particu- ence or absence of a lid-like operculum, zoospore larly Synchytrium. ultrastructure and size, and flagellum length (Barr et al. 1987; Fuller and Clay 1993). Sexual repro- MATERIALS AND METHODS duction is also valuable in understanding the phy- The specimens are preserved in silicified peat logeny and taxonomy of chytridiomycetes (Barr collected from the Skaar Ridge site (Beardmore 1978; James et al. 2000); however, this has only Glacier area, Queen Alexandra Range) in the cen- been rarely observed in members of this group tral Transantarctic Mountains (84°49'15.8" S, (Powell 1993). 163°20'18.9" E, 2289 m altitude, Buckley Island Chytridiomycetes produce a globose or fila- Quadrangle, Barrett and Elliot 1973). The site is mentous coenocytic thallus, which includes thin- included in the Buckley Formation of the Beacon and/or thick-walled sporangia, and zoospores (Barr Supergroup and is considered Late Permian (~250 1992). The zoospore, which constitutes the initial Ma) based on palynological data (Farabee et al. means of chytridiomycetes attachment to its sub- 1991). These deposits are thought to have accu- strate (Lozupone and Klein 2002), is characterized mulated in a rapidly subsiding foreland basin by either a posteriorly directed whiplash flagellum formed along the ProtoPacific margin of Antarctica or, as in the Neocallimastigales, numerous flagella as a result of the tectonic activity that affected this are present (Li and Heath 1992). The morphologi- region during the Late Permian to the Early Trias- cally simpler chytridiomycetes live entirely within sic (Taylor et al. 1989). The landscape has been host cells (endobiotic). Other species live either on interpreted as one dominated by fluvial deposition, the surface of the host or substrate (epibiotic), or either through means of a meandering river or a within the host or substrate (interbiotic). Individuals braided system traversing a wetland environment, whose entire thallus is converted into one or more that was increasingly subjected to volcanic activity reproductive structures are termed “holocarpic.” (Collinson and Isbell 1986; Taylor et al. 1989). Peat Only a portion of the thallus is converted into a accumulated in ponded settings associated with reproductive structure in “eucarpic” species. other fluvial deposits, and its petrification is consid- Another character of systematic importance is type ered to have happened rapidly, favored by the of thallus development (Barr 2001). In the endoge- ingression of large loads of volcanic sediments into nous type the encysted zoospore may give rise to the basin (Taylor et al. 1989). The presence of a single sporangium (monocentric) or to a number organically connected plant organs and in some of sporangia (polycentric). When the nucleus of the cases the fine preservation of anatomical details encysted zoospore migrates to originate the spo- (i.e., the fungus described here) supports the rapid rangia, the development is termed exogenous deposition and the autochthony of the assemblage. (monocentric or polycentric). Within the exogenous The majority of the plant fragments observed polycentric development, the nucleus may divide show signs of fungal infection, in particular most with each new nucleus originating a prospo- plants showed the presence of at least a few rangium that collectively form a cluster of sporan- encysted zoospores. Infected are remains of differ- gia (colonialist type); alternatively, each new ent plant organs of the dominant Glossopteridales nucleus may move into a germ tube and divide, including leaves, stems, and roots (called Verte- with the resulting nuclei migrating into an indepen- braria when not found organically connected to the dent system of rhizoids (filamentous type). main plant), probable fragments of the fern In spite of the simplicity of the thallus and Skaaripteris, as well as other unidentifiable plant associated morphological structures, several fossil fragments (see e.g., Pigg 1990; Pigg and Taylor fungi have been assigned to extant chytridio- 1993; Galtier and Taylor 1994). However, mycetes (e.g., Renault 1895; Bradley 1967; Taylor zoospores usually occur either as a group of a few 2 PALAEO-ELECTRONICA.ORG individuals or singly, only possibly representing sporangia subspherical (77-89 x 70-87 µm), ellip- encystment on the available substrate at that soid (91-213 x 59-94 m); single-layered wall (up to moment and not necessarily encystment on a spe- 2 µm); some sporangia with internal contents con- cific host. Additionally, based on the morphology of sisting of segments of variable size and shape; the zoospores alone, it is not possible to determine thick-walled sporangia ovoid (35-43 x 23-25 µm), unequivocally whether the same or a different fun- pyriform (56-67 x 41-47 µm), or ellipsoid to curved- gus than the one described here is responsible for ellipsoid (56-130 x 52-98); wall of variable thick- the infection of the plant tissue. Zoospores of ness (up to 4 µm thick); zoospores and zoospore- extant endoparasites are known to swarm around like bodies (larger zoospores) (5-41 µm) spherical for some time searching for a potential substrate to ellipsoid, with centrally located opaque inclusion; after which they lose motility and encyst on any typically one sporangium per host cell. substrate available at that moment, although the Etymology. The specific epithet reflects the Per- infection only proceeds when encystment occurs mian age of the fossil. on the preferred host(s) (Karling 1964; Alexopoulos et al. 1996; Carlile et al. 2001; Webster and Weber Holotype. Slide #21644 (Figure 1.2), specimen 2007). Thin- and thick-walled sporangia as well as #11653 C-top. zoospores in different states of development are Paratypes.
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