Carla J. Harper

Microfossils from the Lower Devonian Rhynie Chert with Suggested Affinities to the Peronosporomycetes

Abstract A conspicuous silicified microfossil, Frankbaronia polyspora n. gen. n. sp., occurs in plant litter and as an inhabitant of microbial mats from the Lower Devonian Rhynie chert, Aberdeenshire, Scotland. Specimens are elongate-cylindrical, oval, or spherical, thin-walled, and may possess conical or column-like surface projections. Most specimens occur isolated, some are arranged in pairs or short chains. Each specimen contains several small spheres, each in turn with a (sub)centric opaque inclusion. Immature specimens indicate that ontogenesis in this fossil includes the formation of a single centric body of opaque material that subsequently is apportioned among the developing small spheres. Frankbaronia polyspora is quite similar in size and morphology to the oogonia containing oospores seen in certain extant members of the Peronosporomycetes. The Rhynie chert is known to contain the oldest fossil evidence of the Peronosporomycetes but only a single form (Hassiella monospora) has previously been documented. The discovery of a second putative representative of this group of organisms proves that this paleoecosystem is still an important source of new information on the paleodiversity of microbial life.

Structurally preserved fungi from Antarctica: diversity and interactions in late Palaeozoic and Mesozoic polar forest ecosystems

Abstract Chert and silicified wood from the Permian through Cretaceous of Antarctica contain abundant information on fungal diversity and plant–fungal interactions. The chert deposits represent a particularly interesting setting for the study of plant–fungal interactions because they preserve remains of distinctive high latitude forest ecosystems with polar light regimes that underwent a profound climate change from icehouse to greenhouse conditions. Moreover, some of the cherts and wood show the predominance of extinct groups of seed plants (e.g. Glossopteridales, Corystospermales). Over the past 30 years, documentation of fossil fungi from Antarctica has shifted from a by-product of plant descriptive studies to a focused research effort. This paper critically reviews the published record of fungi and fungal associations and interactions in the late Palaeozoic and Mesozoic cherts and silicified wood from Antarctica; certain fungal palynomorphs and fungal remains associated with adpression fossils and cuticles are also considered. Evidence of mutualistic (mycorrhizal), parasitic and saprotrophic fungi associated with plant roots, stems, leaves and reproductive organs is presented, together with fungi occurring within the peat matrix and animal–fungus interactions. Special attention is paid to the morphology of the fungi, their systematic position and features that can be used to infer fungal nutritional modes.

Fungi and fungal interactions in the Rhynie chert: a review of the evidence, with the description of Perexiflasca tayloriana gen. et sp. nov.†

The Lower Devonian Rhynie chert is one of the most important rock deposits yielding comprehensive information on early continental plant, animal and microbial life. Fungi are especially abundant among the microbial remains, and include representatives of all major fungal lineages except Basidiomycota. This paper surveys the evidence assembled to date of fungal hyphae, mycelial cords and reproductive units (e.g. spores, sporangia, sporocarps), and presents examples of fungal associations and interactions with land plants, other fungi, algae, cyanobacteria and animals from the Rhynie chert. Moreover, a small, chytrid-like organism that occurs singly, in chain-like, linear arrangements, planar assemblages and three-dimensional aggregates of less than 10 to individuals in degrading land plant tissue in the Rhynie chert is formally described, and the name Perexiflasca tayloriana proposed for the organism. Perexiflasca tayloriana probably colonized senescent or atrophied plant parts and participated in the process of biological degradation. The fungal fossils described to date from the Rhynie chert constitute the largest body of structurally preserved evidence of fungi and fungal interactions from any rock deposit, and strongly suggest that fungi played important roles in the functioning of the Early Devonian Rhynie ecosystem. This article is part of a discussion meeting issue ‘The Rhynie cherts: our earliest terrestrial ecosystem revisited’.

REINVESTIGATING CARBONIFEROUS ''ACTINOMYCETES'': AUTHIGENIC FORMATION OF BIOMIMETIC CARBONATES PROVIDES INSIGHT INTO EARLY DIAGENESIS OF PERMINERALIZED PLANTS

ABSTRACT Paleoecological interactions among fossil microorganisms have garnered significant interest within the paleobotanical community; however, an understanding of the early diagenesis of associated plant material is of critical importance when assessing putative body fossils of fungi and bacteria. Structures preserved within permineralized petioles of the Carboniferous fern Botryopteris tridentata Felix (Scott) have been interpreted as the earliest remains of Actinobacteria found in association with vascular plants, but re-examination of the specimens indicates instead that these biomimetic structures (BMS) are authigenic carbonate minerals. Using spinning disk confocal microscopy, we generated monochromatic luminescence maps of BMS found within the phloem cells of Botryopteris. Luminescence was captured at wavelengths of 665 nm, consistent with an interpretation of these structures as disordered dolomites, an inference subsequently corroborated with energy-dispersive X-ray spectrometry (SEM-EDS). The presence of high-magnesium carbonates within Botryopteris is suggestive of an early anaerobic stage of plant tissue degradation characterized by metabolic activities of sulfate-reducing bacteria. Anaerobic biodegradation may also have been performed by chytridiomycetes, and we interpret larger (5–8 µm) unicells found within the specimens as fossils of chytrid zoosporangia. Understanding microbial contribution to the early diagenesis of plants preserved within calcium carbonate concretions (coal balls) is dependent upon both characterizing diversity of microbial communities within fossil plants, and elucidating the geomicrobiological parameters of mineralization. As such, this study underscores the necessity of integrating geomicrobiology with plant taphonomy in investigations of the microbial component of ancient ecosystems.

A Putative Zygomycetous Fungus with Mantled Zygosporangia and Apposed Gametangia from the Lower Coal Measures (Carboniferous) of Great Britain

Several specimens of a new fungal reproductive unit, Halifaxia taylorii nov. gen. et spec., occur within the tracheids of a structurally preserved fern axis from the Lower Pennsylvanian of Great Britain. The reproductive units, which appear to be lateral outgrowths of tubular hyphae, consist of a mantled sphere (80–90 μm in diameter) borne terminally on an inflated subtending structure, which may also be mantled. A smaller element clasps the proximal portion of the subtending structure; one arm of this element extends further up along and appears to eventually fuse laterally with the subtending structure. The reproductive units are interpreted as zygosporangium-apposed gametangia complexes of a zygomycetous fungus. Although several structural features of H. taylorii resemble features seen in the zygosporangium-gametangia complexes of certain modern zygomycetes, the precise systematic affinities of the fossils remain unresolved. Nevertheless, the discovery is important because it provides new information on the morphology and evolutionary history of the zygomycetous fungi, which are poorly resolved on the basis of fossils.

Fungal decay in Permian Glossopteridalean stem and root wood from Antarctica

Evidence of fungal decay is frequently encountered in silicified wood. However, studies focusing on fossil fungal wood degradation remain rare. A characteristic pattern of degradation and decay symptoms congruent with present-day white pocket rot occur in Late Permian silicified glossopteridalean stem and root wood (Australoxylon sp.) from Skaar Ridge, Antarctica. Co-occurring with the decay symptoms are fungal hyphae with clamp connections. Hyphae usually progress through the pit apertures, but some may also penetrate tracheid walls. The individual wall layers in some of the infected tracheids are separated from each other, apparently forming appositions. Small, opaque bodies (? arthropod coprolites) occur in some of the decay pockets. The abundance of infected specimens among the silicified woods from Skaar Ridge suggests that white pocket rot fungi were important decomposers in late Paleozoic high-latitude forest ecosystems.

Fossils of Arbuscular Mycorrhizal Fungi Give Insights Into the History of a Successful Partnership With Plants

Abstract The majority of land plants today live in mutually beneficial symbiosis with glomeromycotan fungi that occur in the form of arbuscular mycorrhizas (AM). Morphologically similar associations have also been recorded from the fossil record throughout the Phanerozoic. However, structural similarity does not necessarily equate to equivalence of function in these fossil associations, and the inherent nature of the fossil record does not normally permit assessment of the structure-function relationship in fossil fungal associations. Nevertheless, we regard it very likely that the best preserved fossil associations from the famous Lower Devonian Rhynie chert were functionally equivalent to extant AM because (1) arbuscules seem to have been as abundant as in modern AM; (2) there appear to be similar patterns of fungal colonization regulated by the anatomy of the host organ; (3) sporulation of the fungus is common near and in the host; (4) early land plants colonized by glomeromycotan fungi were dominants in their ecosystems, providing evidence of adequate mineral nutrition despite the lack of fine absorbing structures in soils; and (5) paleosols would not generally have been highly fertile, and thus we would still expect nutrients such as phosphorus to often be limiting for plant growth.

Fungal intruders of enigmatic propagule clusters occurring in microbial mats from the Lower Devonian Rhynie chert

Microbial mats in the Lower Devonian Rhynie chert represent diverse communities of organisms, which probably not only co-occurred in these structures, but also variously interacted with one another. However, little is known about these interactions. Three different types of fungi interact with clusters of small propagules that frequently occur within the Rhynie microbial mats. One of the fungi occurs in the form of small mycelia and single reproductive units within individual propagules, while the second is characterized by apophysate, epibiotic sporangia and multibranched rhizoidal systems that extend through the clusters and penetrate individual propagules. The third fungus consists of what is interpreted as a distal sporangium or spore from which a long, tubular stalk reaches into the propagule cluster. One specimen of the latter fungus occurs inside a specimen of the second fungus and, moreover, shows evidence suggestive of hyperparasitism in the form of conical callosities. This discovery supports the suggestion that microbial mats in the Rhynie paleoecosystem were complex structures based on the presence of numerous interactions between different organisms within the mats.

Looking for Arbuscular Mycorrhizal Fungi in the Fossil Record

Abstract The evolution and diversification of plants on land were profoundly influenced by mutually beneficial symbioses between the plants and certain fungi. The vast majority of fungi involved in these fossil associations are strikingly similar to present-day arbuscular mycorrhizal fungi (AMF), and their symbioses with plants closely resemble present-day arbuscular mycorrhizas (AM). Although fossil evidence of AM has variously been documented and illustrated throughout the late Palaeozoic to Cenozoic, the record in general remains exceedingly scant. However, we believe that more compelling evidence of AM and AMF in fossil plants can be gathered if paleobotanists are equipped with an accurate search image for mycorrhizal fungi and the core structural components of their associations with plants. This chapter presents an illustrated guide that provides researchers with a synopsis of important (i.e., recognizable in transmitted light) structural features of modern AM that facilitates the accurate identification of fossil members of this group of fungi and their discrimination from other, nonmycorrhizal fungi while examining structurally preserved plant fossils. Where available, fossil mycorrhizal fungi displaying the features included in this guide are also documented.

Reactive Oxygen Defense Against Cellular Endoparasites and the Origin of Eukaryotes

Abstract In this chapter, we propose a model for the early evolution of eukaryotic cells under pressure of intense endoparasitism. We define features of eukaryotes developed to defend against endoparasites (primarily bacteria), including a defensive system composed of an antioxidant sterol-enriched internal and external membrane system that could be used to entrap endoparasites and degrade them with superoxide produced on the membranes, cytoskeleton scaffolding for the membrane system, and a nuclear envelope to exclude endoparasites from reaching the genome. Mitochondria and chloroplasts evolved from the prokaryotes that developed ways to neutralize the reactive oxygen defense of the host. For mitochondria, hydrogen pumping to the exterior of the endoparasite enabled them to reduce superoxide to water, effectively defeating the host defense. Other features of eukaryotes that may have evolved from defense from endoparasitism include: autophagy, cell walls in fungi and plants, acquired immunity in animals, multicellularity, and apoptosis. We evaluate fossil data, where available, to provide additional information regarding the early evolution of eukaryotes and the prevalence of endoparasitic microbes.