Rise of the Fungi

Australia: The Land Where Time Began

Rise of the Fungi

According to Moore¹ in recent years a fossil record of fungi has accumulated, though there are not many unique morphological features and fungal hyphae do not generally fossilise well to be preserved over long time periods.

See Prototaxites

Moore suggests that when all the evidence is taken together the conclusion is inescapable to him that these very large organisms that were the largest terrestrial organisms to have evolved by their time were actually giant terrestrial saprophytic fungi, with affinities to extant Basidiomycota, dolipore septa, clamp connections and sterigmata.

The Rhynie Chert of 410 Ma in the Devonian age, located in Aberdeenshire, north Scotland, fungal fossils were preserved in exquisite detail, the site also containing fossils of primitive plants, which had cells that were water-conducting but no true leaves, along with arthropods, lichens, algae and fungi. In this sedimentary deposit representatives of close to a complete range of fungal lifestyles and developmental patterns that are present in extant fungi have been found (Taylor, Hass & Kerp, 1997; Taylor et al., 2004; Taylor, Krings & Kerp, 2006).

The lifestyles represented by the fungi from the Rhynie Chert are:

An Oomycota fungus, a phylum of filamentous protists called water moulds or downy mildews which are not actually fungi; rather they are primitive organisms that are fungus-like. Many Oomycota are important pathogens of plants at the present, such as species of Phytophthora. An antheridium contacting an oogonium has been found on several of the specimens from the Rhynie Chert, which demonstrates clearly the existence of a sexual reproduction process that was fully differentiated, including male and female gametes that are fully differentiated, and all that goes with them, including sex hormone receptors and male to female cell targeting.

It is inferred by another specimen with a fully differentiated chytrid zoosporangia that at the time the sediment was deposited the complete chytrid cell body of the chytrids – thallus, rhizoids, free cell formation, motile zoospores, etc. – was fully established. There were also examples of chytrids parasitising other fungi among the specimens found in the Rhynie Chert, which demonstrates again that by 400 Ma the fungal lifestyle was so firmly established that fungi were parasitising other fungi.

In the Rhynie Chert there are also higher fungi represented, with particularly fine ascomycete specimens that show development of ascospores that is typical of the present, and emerging through the epidermis of a plant, which suggest a fully developed plant pathogen at extremely early stage in the evolution of plants. It appears, however, that though the associated plants are at an early stage, the ascomycete fungal fossils are already highly evolved. The hyphae are regularly septate; there are specimens including perithecia, fruiting bodies of ascomycetes that are apparently identical to extant forms, from which it can be inferred that a fully formed evolved fungal developmental biology that was capable of producing extreme differentiation of hyphae, cell signalling, cell sorting, pattern formation and the formation of tissues that have different functions, all of which are still typical at the present. There are also sections of a thallus of a cyanolichen, which again indicates a fungal developmental process that is highly evolved at this very ancient time. Moore suggests that it evident that fungi were capable of entrapping cyanobacteria, form differentiate fungal thalli and invade the land 400-500 Ma.

This wide diversity of fungi occurred in other places as well as in the Rhynie Chert of Scotland. One such place is Wisconsin, where Glomeromycotan fossils were found in 460 Ma Ordovician rocks. The fossil material from this site consisted of entangled, non-septate hyphae that branched occasionally together with globose spores. At 460 Ma they were older than the earliest known vascular plants, at a time when the land flora was made up of bryophytes, lichens and cyanobacteria. An arbuscular mycorrhizal symbiosis is formed by extant Glomeromycota, which is ubiquitous in modern plants, and it has also been reported in association with extant hepatics and hornworts. It is reasonable to suppose that an important role in the success of early terrestrial plants was played by arbuscular mycorrhiza (Blackwell, 2000; Redecker, Kodner & Graham, 2000), i.e. the plants were enabled to migrate to the land by mycorrhizal fungi.

It is shown by convincing fossil evidence that fungi were important, to the point of being dominant, members of terrestrial ecosystems worldwide at least 500 Ma. Moore suggests that well-developed filamentous fungi must have appeared a long time before that; it must have taken a fair amount of time for the ancestral taxa of the water moulds in the Rhynie Chert, chytrids, Glomeromycota, lichens and Ascomycota to evolve the ability to form structures that are microscopically indistinguishable from those in extant forms. Moore asks how long it would take for the ancestral forms of Prototaxites to evolve a club fungus that was 8 m tall and become distributed around the world. Other fossils have been found that are dated to between 800 Ma and 900 Ma, though not all accept these.

Fossils from formations in northwestern Canada that have been dated to 800-900 Ma have been assigned to the form-genus Tappania (Butterfield, 2005), describing them as benthic, multicellular organisms that were capable of substantial differentiation. Most notably, as septate, branching, filamentous processes that were able to fuse secondarily, a synapomorphy (a trait shared by) of the extant ‘higher fungi’. Tappania is identified reliably, if not conclusively, as a fungus, when combined the evidence above is characteristics such as phylogenetic, taphonomic and functional morphologic evidence, such as ‘hyphal fusion’, which was probably a sister group to the ‘higher fungi’ (Dikarya), though more derived than the zygomycetes (Butterfield, 2005, abstract).

According to Moore the form genus Tappania is spread widely, being found in Australia, Canada and China, where it is found in carbonaceous ancient shoreline deposits. Fossilised specimens from shale deposits in northern Australia have been dated to almost 1.5 Ga.

According to Javaux, Knoll & Walter Tappania populations consist of irregularly spheroidal organic vesicles up to 160 μm in diameter. They are distinguished by bulbous protrusions, and from 0-20 hollow, cylindrical protrusions. The terminations of the processes are closed and expanded slightly and may branch dichotomously. The processes are distributed on the surface of the vesicle irregularly and asymmetrically. The irregular number and length, asymmetric distribution, and process branching in Tappania suggest either a germinating cyst or an actively growing cell. In some specimens the bulbous protrusions further suggest vegetative reproduction by budding (Javaux, Knoll & Walter, 2001).

Javaux et al. (2001) interpret the asymmetric branching of processes and bulbous protrusions as representing dynamic cell remodelling of a sort that can only be possible in cells with a cytoskeleton and signalling pathways of eukaryotes. According to Javaux et al. the systematic relationships of Tappania are not certain, but it is indicated by its distinctive morphology that ‘cytoskeletal architecture and regulatory networks that are characteristic of extant eukaryote protists’ had already evolved in organisms that were fossilised 1.5 Ga. These and other putative pre-Devonian fungi have been discussed (Butterfield, 2005), concluding that a case can be made for an extended record of relatively diverse fungi in the Proterozoic. There are others who agree with Butterfield’s identification (Cavalier-Smith, 2006, pp. 983-984) of Tappania as sporangial entities that had broken from a branching hyphal network, though disagree that these fossils are probably fungi. He suggests instead that they could be actinobacterial pseudosporangia, an opinion that Moore does not find very convincing.

Sources & Further reading