Structural, physiological, and stable carbon isotopic evidence that the enigmatic Paleozoic fossil Prototaxites formed from rolled liverwort mats

Abstract

New structural, nutritional, and stable carbon isotope data may resolve a long-standing mystery-the biological affinities of the fossil Prototaxites, the largest organism on land during the Late Silurian to Late Devonian (420-370 Ma). The tree trunk-shaped specimens, of varying dimensions but consistent tubular anatomy, first formed prior to vascular plant dominance. Hence, Prototaxites has been proposed to represent giant algae, fungi, or lichens, despite incompatible biochemical and anatomical observations. Our comparative analyses instead indicate that Prototaxites formed from partially degraded, wind-, gravity-, or water-rolled mats of mixotrophic liverworts having fungal and cyanobacterial associates, much like the modern liverwort genus Marchantia. We propose that the fossil body is largely derived from abundant, highly degradation-resistant, tubular rhizoids of marchantioid liverworts, intermixed with tubular microbial elements. Our concept explains previously puzzling fossil features and is consistent with evidence for liverworts and microbial associates in Ordovician-Devonian deposits, extensive ancient and modern marchantioid mats, and modern associations of liverworts with cyanobacteria and diverse types of fungi. Our interpretation indicates that liverworts were important components of Devonian ecosystems, that some macrofossils and microfossils previously attributed to "nematophytes" actually represent remains of ancient liverworts, and that mixotrophy and microbial associations were features of early land plants.

Fungal symbioses in bryophytes: New insights in the Twenty First Century

“…We take serious issue with both the evidence Graham et al (2010a) present and their conclusions. 1) Their figure (4D) purporting to show a septum in a smooth rhizoid in Marchantia like those in Prototaxites is simply a tubular overgrowth of host wall over a fungal hypha which is commonly seen in extant liverworts.…”

“…Given their extraordinary claims it is unsurprising that the Graham et al (2010a) article stimulated both a letter (Boyce & Hotton 2010) and a commentary (Taylor et al 2010), which were followed by a rapid response from Graham et al (2010b). Whereas our critique comes from a bryophyte perspective, the equally sceptical views of Boyce & Hotton (2010) and Taylor et al (2010) focus on the methodology of Graham et al (2010a) including taphonomy, stable isotope analyses and interpretation of Prototaxites from a palaeobotanical standpoint. Graham et al (2010b) fail to produce any convincing counter evidence: for their claim of liverwort mats rolling down a Devonian slope to have any credibility whatsoever at the very least a convincing demonstration from extant plants is required.…”

“…Setting aside this speculative consideration based on sound morphological evidence, this overview would not be complete without reference to the truly remarkable suggestions by Graham et al (2010a). These are based on a new look at the enigmatic Late Silurian to Late Devonian fossil Protaxites variously interpreted previously as a giant alga, fungus or lichen (Selosse 2002).…”

“…These are based on a new look at the enigmatic Late Silurian to Late Devonian fossil Protaxites variously interpreted previously as a giant alga, fungus or lichen (Selosse 2002). Building on their earlier study (Graham et al 2004) Graham et al (2010a) suggest that Prototaxites was formed from partially degraded wind-, gravity-or water-rolled mats of mixotrophic liverworts having fungal and cyanobacterial associates much like Marchantia. They go on to argue that Prototaxites was derived from degradation-resistant rhizoids of marchantioid liverworts intermixed with tubular microbial elements, that liverworts were important components of Devonian ecosystems and that fossils previously attributed to nematophytes actually represent the remains of thalloid liverworts.…”

Direction of illumination controls gametophyte orientation in seedless plants and related algae

“…Previous experiments with the same isolates of Sphagnum compactum, Marchantia polymorpha and Coleochaete that had been cultivated similarly revealed the occurrence of carbon limitation relieved by exogenous organic carbon. [37][38][39] In the present study, any such carbon limitation would have affected all experimental materials equally. To facilitate careful evaluation of results, investigations of the 5 selected taxa were conducted serially, with care taken to ensure that temperature and irradiance levels were the same during each experiment conducted with near-saturating levels of photosynthetically active radiation (PAR).…”