Biologically mediated weathering in modern cryptogamic ground covers and the early Paleozoic fossil record

Specific micro-weathering features and biochemically derived residues formed by living organisms can be used as biomarkers to infer the presence of biological communities within sedimentary units of ancient ecosystems. We examined basaltic soil minerals from modern cryptogamic ground covers (CGCs) in Iceland and compared these with two early Paleozoic fossil systems. Nine biologically mediated weathering features (BWFs) were identified in modern soils including micron-scale surface trenching and penetrative tunnels, which are attributed to the actions of bacteria, fungi and exudates. Specific BWFs are associated with Fe residues, and with Fe-rich bio-precipitated nodules. Further, putative comparable features and Fe enrichment are identified in palaeosols from the late Silurian (Llansteffan, south Wales) and the Early Devonian (Rhynie chert, Scotland). Although we are cautious about attributing biological affinity to individual isolated features, our results demonstrate the potential of using multiple BWF types as a collective together with their chemical signatures as new proxies to understand community structure and interactions in early terrestrial ecosystems. This new information is the first evidence of interactions between ancient CGC-like organisms and substrate or soil inorganic components in the fossil record, and demonstrates the ability of CGC-like biospheres to contribute to mineral weathering, soil development and biogeochemical cycling during the early Paleozoic. Supplementary material: Fieldwork geomorphological information and triplot SEM-EDS data are available at https://doi.org/10.6084/m9.figshare.c.437371

A New Chytridiomycete Fungus Intermixed with Crustacean Resting Eggs in a 407-Million-Year-Old Continental Freshwater Environment

Copyright: © 2016 Strullu-Derrien et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

Evidence of parasitic Oomycetes (Peronosporomycetes) infecting the stem cortex of the Carboniferous seed fern <i>Lyginopteris oldhamia</i>

Thin sections of petrified fossils made during the latter part of the nineteenth and early twentieth centuries to investigate the internal tissue systems of plants now provide an important new source of information on associated micro-organisms. We report a new heterokont eukaryote (Combresomyces williamsonii sp. nov.) based on exquisitely preserved fossil oogonia, antheridia and hyphae from the Carboniferous (Pennsylvanian: Bashkirian stage) of UK. The structure of the oogonia and antheridia and features observed within the hyphae demonstrate a relationship with Oomycetes (Peronosporomycetes). The fossil micro-organism was documented in situ in petrified stem cortex and rootlets of the extinct seed fern Lyginopteris oldhamia (Pteridospermales). The main observed features point towards a pythiaceous Oomycete but links to biotrophic Albuginales or Peronosporaceae cannot be ruled out owing to the observation of a possible haustorium. Our study provides the earliest evidence for parasitism in Oomycetes

Cryptogamic ground covers as analogues for early terrestrial biospheres: Initiation and evolution of biologically mediated proto-soils

Modern cryptogamic ground covers (CGCs), comprising assemblages of bryophytes (hornworts, liverworts, mosses), fungi, bacteria, lichens and algae, are thought to resemble early divergent terrestrial communities. However, limited in-situ plant and other fossils in the rock record, and a lack of CGC-like soils reported in the pre-Silurian sedimentological record, have hindered understanding of the structure, composition, and interactions within the earliest CGCs. A key question is how the earliest CGC-like organisms drove weathering on primordial terrestrial surfaces (regolith), leading to the early stages of soil development as proto-soils, and subsequently contributing to large-scale biogeochemical shifts in the Earth System. Here, we employed a novel qualitative, quantitative and multi-dimensional imaging approach through X-ray micro-computed tomography, scanning electron, and optical microscopy to investigate whether different combinations of modern CGC organisms from primordial-like settings in Iceland develop organism-specific soil-forming features at the macro- and micro-scales. Additionally, we analysed CGCs growing on hard rocky substrates to investigate the initiation of weathering processes non-destructively in 3D. We show that thalloid CGC organisms (liverworts, hornworts) develop thin organic layers at the surface (<1 cm) with limited subsurface structural development, whereas leafy mosses and communities of mixed-organisms form profiles that are thicker (up to ~7 cm), structurally more complex, and more organic-rich. We term these thin layers and profiles proto-soils. Component analyses from X-ray micro-computed tomography data show that thickness and structure of these proto-soils are determined by the type of colonising organism(s), suggesting that the evolution of more complex soils through the Palaeozoic may have been driven by a shift in body plan of CGC-like organisms from flattened and appressed to upright and leafy. Our results provide a framework for identifying CGC-like proto-soils in the rock record and a new proxy for understanding organism-soil interactions in ancient terrestrial biospheres and their contribution to the early stages of soil-formation

An expanded diversity of oomycetes in Carboniferous forests: Reinterpretation of Oochytrium lepidodendri (Renault 1894) from the Esnost chert, Massif Central, France

335–330 million-year-old cherts from the Massif Central, France, contain exceptionally well-preserved remains of an early forest ecosystem, including plants, fungi and other microorganisms. Here we reinvestigate the original material prepared by Renault and Roche from collections of the Muséum National d’Histoire Naturelle, Paris, and present a re-evaluation of Oochytrium lepidodendri (Renault 1894), originally described as a zoosporic fungus. Confocal laser scanning microscopy (CLSM) was used to study the microfossils, enabling us in software to digitally reconstruct them in three-dimensional detail. We reinterpret O. lepidodendri as a pseudofungus and favour placement within the oomycetes, a diverse clade of saprotrophs and both animal and plant parasites. Phylogenetically, O. lepidodendri appears to belong to a group of oomycetes distinct from those previously described from Paleozoic rocks and most likely related to the Peronosporales s.l. This study adds to our knowledge of Paleozoic eukaryotic diversity and reinforces the view that oomycetes were early and diverse constituents of terrestrial biotas, playing similar ecological roles to those they perform in modern ecosystems

Unique cellular organization in the oldest root meristem

Roots and shoots of plant bodies develop from meristems—cell populations that self-renew and produce cells that undergo differentiation—located at the apices of axes [1].The oldest preserved root apices in which cellular anatomy can be imaged are found in nodules of permineralized fossil soils called coal balls [2], which formed in the Carboniferous coal swamp forests over 300 million years ago [3, 4, 5, 6, 7, 8 and 9]. However, no fossil root apices described to date were actively growing at the time of preservation [3, 4, 5, 6, 7, 8, 9 and 10]. Because the cellular organization of meristems changes when root growth stops, it has been impossible to compare cellular dynamics as stem cells transition to differentiated cells in extinct and extant taxa [11]. We predicted that meristems of actively growing roots would be preserved in coal balls. Here we report the discovery of the first fossilized remains of an actively growing root meristem from permineralized Carboniferous soil with detail of the stem cells and differentiating cells preserved. The cellular organization of the meristem is unique. The position of the Körper-Kappe boundary, discrete root cap, and presence of many anticlinal cell divisions within a broad promeristem distinguish it from all other known root meristems. This discovery is important because it demonstrates that the same general cellular dynamics are conserved between the oldest extinct and extant root meristems. However, its unique cellular organization demonstrates that extant root meristem organization and development represents only a subset of the diversity that has existed since roots first evolved.</p

Investigating Devonian trees as geo-engineers of past climates: linking palaeosols to palaeobotany and experimental geobiology

We present the rationale for a cross-disciplinary investigation addressing the ‘Devonian plant hypothesis’ which proposes that the evolutionary appearance of trees with deep, complex rooting systems represents one of the major biotic feedbacks on geochemical carbon cycling during the Phanerozoic. According to this hypothesis, trees have dramatically enhanced mineral weathering driving an increased flux of Ca2+ to the oceans and, ultimately, a 90% decline in atmospheric CO2 levels through the Palaeozoic. Furthermore, experimental studies indicate a key role for arbuscular mycorrhizal fungi in soil–plant processes and especially in unlocking the limiting nutrient phosphorus in soil via Ca-phosphate dissolution mineral weathering. This suggests co-evolution of roots and symbiotic fungi since the Early Devonian could well have triggered positive feedbacks on weathering rates whereby root–fungal P release supports higher biomass forested ecosystems. Long-standing areas of uncertainty in this paradigm include the following: (1) limited fossil record documenting the origin and timeline of the evolution of tree-sized plants through the Devonian; and (2) the effects of the evolutionary advance of trees and their in situ rooting structures on palaeosol geochemistry. We are addressing these issues by integrating palaeobotanical studies with geochemical and mineralogical analyses of palaeosol sequences at selected sites across eastern North America with a particular focus on drill cores from Middle Devonian forests in Greene County, New York State

Fertile Prototaxites taiti: a basal ascomycete with inoperculate, polysporous asci lacking croziers

The affinities of Prototaxites have been debated ever since its fossils, some attaining tree-trunk proportions, were discovered in Canadian Lower Devonian rocks in 1859. Putative assignations include conifers, red and brown algae, liverworts and fungi (some lichenised). Detailed anatomical investigation led to the reconstruction of the type species, P. logani, as a giant sporophore (basidioma) of an agaricomycete (= holobasidiomycete), but evidence for its reproduction remained elusive. Tissues associated with P. taiti in the Rhynie chert plus charcoalified fragments from southern Britain are investigated here to describe the reproductive characters and hence affinities of Prototaxites. Thin sections and peels (Pragian Rhynie chert, Aberdeenshire) were examined using light and confocal microscopy; Přídolí and Lochkovian charcoalified samples (Welsh Borderland) were liberated from the rock and examined with scanning electron microscopy. Prototaxites taiti possessed a superficial hymenium comprising an epihymenial layer, delicate septate paraphyses, inoperculate polysporic asci lacking croziers and a subhymenial layer composed predominantly of thin-walled hyphae and occasional larger hyphae. Prototaxites taiti combines features of extant Taphrinomycotina (Neolectomycetes lacking croziers) and Pezizomycotina (epihymenial layer secreted by paraphyses) but is not an ancestor of the latter. Brief consideration is given to its nutrition and potential position in the phylogeny of the Ascomycota

Fungal-host diversity among mycoheterotrophic plants increases proportionally to their fungal-host overlap

The vast majority of plants obtain an important proportion of vital resources from soil through mycorrhizal fungi. Generally, this happens in exchange of photosynthetically fixed carbon, but occasionally the interaction is mycoheterotrophic, and plants obtain carbon from mycorrhizal fungi. This process results in an antagonistic interaction between mycoheterotrophic plants and their fungal hosts. Importantly, the fungal‐host diversity available for plants is restricted as mycoheterotrophic interactions often involve narrow lineages of fungal hosts. Unfortunately, little is known whether fungal‐host diversity may be additionally modulated by plant–plant interactions through shared hosts. Yet, this may have important implications for plant competition and coexistence. Here, we use DNA sequencing data to investigate the interaction patterns between mycoheterotrophic plants and arbuscular mycorrhizal fungi. We find no phylogenetic signal on the number of fungal hosts nor on the fungal hosts shared among mycoheterotrophic plants. However, we observe a potential trend toward increased phylogenetic diversity of fungal hosts among mycoheterotrophic plants with increasing overlap in their fungal hosts. While these patterns remain for groups of plants regardless of location, we do find higher levels of overlap and diversity among plants from the same location. These findings suggest that species coexistence cannot be fully understood without attention to the two sides of ecological interactions. Keywords: mycoheterotrophic interactions; mycorrhizal cheaters; niche overlap; niche width; plant coexistence; plant–belowground interaction

First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2

© 2014 The Authors. New Phytologist © 2014 New Phytologist Trust. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. The attached file is the published version of the article