Unveiling Earth's Ancient Mysteries: The Astonishing Rhynie Chert Fossils

We invite you to imagine a world over 400 million years ago, a time when Life on Earth was vastly different from what we know today. The Rhynie Chert, an iconic geological site in Scotland, offers a captivating glimpse into this distant past, holding secrets of an ancient terrestrial environment.
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The Rhynie Chert is a remarquable site that has been instrumental in unravelling the early development of life on land though over a century of study, which began with the early research of the paleobotanists Robert Kidston and William Lang.

Chert is a fine-grained sedimentary rock composed of microcrystalline quartz that at Rhynie formed as a deposit from a hot spring system. Under these special conditions, water rich in dissolved minerals flooded the landscape, entombing the organisms living there and preserving them in exquisite detail. Alongside ancient plants, you will find a thriving community of animals, primarily arthropods, and diverse microscopic organisms, including cyanobacteria, algae, amoebozoa, various fungal groups, and fungal-like oomycetes. Fungi were observed here from the outset, but they have come into focus more recently as their diversity and importance in the modern world became better understood. It was the intricate interactions between plants and fungi that caught my attention and that of my colleagues several years ago....

 

Rhynie Chert landscape (© Victor Leshyk)

 

Exploring museum collections of Rhynie Chert fossils is like embarking on a time-travel adventure through Earth's ancient history. We have been studying these meticulously catalogued and preserved thin sections (paper-thin slices of rock glued to microscope slides) though a variety of means – from both traditional light microscopy to the most modern imaging techniques.

 These thin slivers of rock have introduced us to the importance and diversity of fungi in early terrestrial ecosystems, and historically the imaging method of choice has been standard white light microscopy. Notably, in the Rhynie Chert we find the earliest mutualistic symbiotic associations between fungi and plants. The ability of fungi to form mycorrhizas with plants is one of the most remarkable and enduring adaptations to life on land, occurring in about 85% of living plants. Mycorrhizas in the Rhynie Chert plants were first brought to light in the 1970’s by B. Boullard and Y. Lemoigne and documented in more detail by W. Remy, T.N. Taylor and their collaborators. In 2014, we described a mycorrhizal-like colonization of a Rhynie Chert plant by two different fungi, which resembles certain types seen in some living bryophytes and lycophytes. Additionally, zoosporic fungi, known for reproducing with flagellated spores, make their appearance. These were the most common fungi in the Rhynie chert environment, and many species have been documented in work led by T. N. Taylor and M. Krings.  

 

Mycorrhizas in Horneophyton lignieri
Mycorrhizas in Horneophyton lignieri (from: Strullu-Derrien et al., New Phytologist, 2018. 220: 1012–1030. doi: 10.1111/nph.15076)

 

 The development of confocal laser scanning microscopy has provided us with a new tool to investigate the world of the Rhynie Chert. Through numerous trial-and-error experiments over the past decade at the Imaging and Analysis Centre of the Natural History Museum London, we have learnt how to apply this relatively novel technique to these cherts. Unlike traditional bright-field microscopy, confocal laser microscopy significantly enhances the image's clarity and detail. This allows researchers to visualize minute three-dimensional structures with unprecedented precision. The confocal datasets also allow us to digitally reconstruct the fungal structures using various imaging softwares. The delicate and intricately preserved features of Rhynie Chert fossils are brought to life in vivid detail. This approach has enabled us to describe several zoosporic fungi (see: Strullu-Derrien et al., 2015. Botanical Journal of the linnean Society 179, 201–213; Strullu-Derrien et al., 2016. PLoS ONE 11(12): e0167301; Strullu-Derrien et al., 2018. Philosophical Transactions of the Royal Society B 373: 20170146).

 

 

Confocal image on screen

 

 

 

Retesporangicus lyonii, a zoosporic fungus. Confocal scanner scaning images and three-dimensional reconstructions of zoosporangia using SPIERSedit and SPIERSview (from: Strullu-Derrien et al., 2018. Philosophical Transactions of the Royal Society B 373: 20170146. doi.org/10.6084/m9)

One fungal resident of the Rhynie Chert, Paleopyrenomycites devonicus, stands out. Described as Ascomycota, it colonized the ancient plant Asteroxylon mackiei. Yet, the precise role it played – as a saprotroph, parasite, or pathogen – remains a tantalizing mystery. The relationships of its filamentous structures with the host tissues away from sporulating structures have eluded conclusive observations, keeping its trophic strategy shrouded in uncertainty.

 Ascomycota is the largest and most diverse phylum within the Fungi. They play a crucial role in terrestrial ecosystems and are of huge interest for medicine, industry, commerce. Some are also pathogens of plants and animals, including humans. Their early fossil record is poorly documented and often embroiled in controversy. While ascomycete-like hyphae and spores can be traced back to the Paleozoic Era, dispersed spores and other indications of a significant Ascomycota radiation only surface much later in the Mesozoic Era. It's within this context that Paleopyrenomycites devonicus, described by T.N. Taylor and collaborators in 1999 and 2005, assumes special significance as a recognized ascomycete. It has also played a pivotal role in calibrating the molecular phylogenetic trees of Fungi.However, interpreting the morphological characteristics of this ancient fungus poses a formidable challenge, as, not unexpectedly, it defies neat categorization within modern groups.

 

Enter Potteromyces asteroxylicola, our newly found filamentous fungus, also belonging to Ascomycota.

This intriguing species produces asexual spores, or conidia, and takes up residence on the outer cortex and epidermis Asteroxylon mackiei. Its resemblances to the asexual form of Paleopyrenomycites devonicus has opened new avenues for reassessing the affinity of the latter and the reliability of using these fossils to date phylogenies within Ascomycota.

 But the story doesn't end there. The plant's reaction to P. asteroxylicola represents a new discovery, revealing that the infection occurred before the host's demise. This marks the first clear evidence of a plant's reaction to a fungal interaction causing pathogenicity – a pathogen, in essence, i.e., a disease-causing parasite. Nowadays numerous plant diseases are caused by Ascomycota are responsible for example of Dutch elm disease, chestnut blight, ash die-back, apple scab or powdery mildew of grape. Our finding expands our understanding of the diverse fungal-plant interactions that played out in early terrestrial ecosystems and shows that fungal pathogenicity was an early development in Life on land.

 

 

Potteromyces asteroxylicola gen. et sp. nov. Confocal scanning laser images

 

Giving a name to a new fossil is an attractive game. In naming our new fungus, we pay tribute to Helen Beatrix Potter (1866–1943) the well-known children's author, whose work on fungi has been largely overlooked. In addition to being a writer, she was a keen amateur naturalist, who used her artistic abilities to draw and document a variety of fungi. She made detailed observations and was one of the first mycologists to study the growth of fungi from spores and appreciate that lichens were an association between an alga and a fungus.

 

Amanita excelsa, “Grey Spotted Amania”, Lennel, 22 July 1894. Watercolour and pencil on paper. Courtesy of the Armitt Trust. https://www.armitt.com

Taken together, our studies highlight the marriage of historical slide collections with modern imaging methods. This has allowed us to describe Potteromyces asteroxylicola and witnesses it’s pathogenicity frozen in the rock record. As we explore and develop these methods, we will continue to reveal a more vivid and detailed account of life on Earth that was previously beyond our reach.

 

 Christine Strullu-Derrien and Alan RT Spencer

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Ecology
Life Sciences > Biological Sciences > Ecology
Fungi
Life Sciences > Biological Sciences > Microbiology > Fungi
Imaging Techniques
Physical Sciences > Materials Science > Materials Characterization Technique > Imaging Techniques
Paleontology
Physical Sciences > Earth and Environmental Sciences > Earth Sciences > Paleontology

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