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Fungal virulence at the time of the end-Permian biosphere crisis?

Henk Visscher, Mark A. Sephton and Cindy V. Looy

ABSTRACT Throughout the world, latest Permian records of organic-walled microfossils are characterized by the common presence of remains of filamentous organisms, usually referred to the palynomorph genus Reduviasporonites. Although generally regarded as indicators of global ecological crisis, fundamental controversy still exists over the biological and ecological identity of the remains. Both fungal and algal affinities have been proposed. We seek to resolve this enigma by demonstrating close morphological similarity of the microfossils to resting structures (monilioid hyphae, sclerotia) of Rhizoctonia, a mod- ern complex of soil-borne filamentous fungi that includes ubiquitous plant pathogens. By analogy with present-day forest decline, these findings suggest that fungal virulence may have been a significant contributing factor to widespread devastation of arboreal vegetation at the close of the Permian Period.

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INTRODUCTION

One of the more puzzling biotic phenomena associated with the profound end-Permian biosphere crisis is the common presence, often in high frequencies, of filamentous organic-walled microfossils in Permian-Triassic (P-Tr) transition sections worldwide (Erwin, 2006)
. These remains are assignable to the broadly defined palynomorph genus Reduviasporonites (synonyms Tympanicysta and Chordecystia; see the GSA Data Repository1) and may occur in marine, lacustrine, and fluvia- tile sediments, regardless of bioprovinciality and climatic zonation (e.g., Visscher et al., 1996; Foster et al., 2002; Steiner et al., 2003; Peng et al., 2005). On morphological grounds, the microfossils have been interpreted as fungal remains, more specifically as ascomycete conidia and conidiophores (Elsik, 1999). Alternatively, on the basis of morphological (Afonin et al., 2001), but particularly chemical (Foster et al., 2002) criteria, an algal interpretation is regularly advocated. Notably, fresh- water green algae of the Zygnemataceae are regarded as nearest living relatives. Ecologically, these contentious identifications support fundamentally different scenarios of global environmental change at the end of the Permian. Proliferation of wood-decaying fungi could corroborate dieback of woody vegetation (Visscher et al., 1996), while blooms of filamentous algae could indicate excessive ponding and swamping of river systems (Afonin et al., 2001).

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At present, authoritative reviews of the end-Permian crisis (e.g., Erwin, 2006) tend to accept the cogency of organic-geochemical and carbon isotopic arguments in favor of an algal affinity of Reduviasporonites. Nevertheless, it was recently shown that the microfossils do not contain any distinctive biomarkers characteristic of either algae or fungi (Sephton et al., 2009).
The prevalence of n-alkene/n-alkane doublets in pyrolysis products of Reduviasporonites had been interpreted in terms of algaenan (Foster et al., 2002), an aliphatic biopolymer known from the cell walls of some (nonfilamentous) species of modern green algae. However, taphonomic studies on a variety of plant and animal remains indicate that post-burial polymerization commonly creates a similar signature in organic structures whose original composition was not aliphatic. Macromolecular constituents of Reduviasporonites not only resemble diagenetically altered chitin (Stankiewicz et al., 2000), the most prominent biopolymer in arthropod cuticles and fungal cell walls, but even the refractory diagenetic compounds in leaf cuticles of fossil lycopsid land plants (see the Data Repository).

However, the cellulosic walls of vegetative cells of Zygnemataceae and other extant families of filamentous green algae have a very poor preservation potential. Their fossil record is restricted to occurrences in late Holocene deposits.

Subordinate but distinctive aromatic moieties, particularly dibenzofuran, detected in Reduviasporonites (Foster et al., 2002; Sephton et al., 2009) can be associated with diagenetic products of soil-derived polysaccharides found in coeval sedimentary organic matter (Sephton et al., 2005a), rather than with green algae.

Since consumers are usually enriched in 13C compared to their food source, reported low δ13C values (–30‰ to –33‰) for the microfossils would reject a fungal origin (Foster et al., 2002). However, considering the prominent negative δ13C excursion globally recognized in carbonates and sedimentary organic matter at the P-Tr junction (e.g., Erwin, 2006),

any conclusive comparison with the carbon isotope composition of land plants should be based on strictly age-equivalent materials.
A measured coeval 13C enrichment of 1.4‰ in Reduviasporonites (Sephton et al., 2009) does not exclude a fungal affinity. In addition, the nitrogen isotope composition (δ15N) of the microfossils is compatible with a fungal derivation (Sephton et al., 2009).

Considering the absence of sufficiently conclusive chemical criteria, clarification of the biological and ecological identity of Reduviasporonites must necessarily rely on morphological comparisons with potential counterparts among modern filamentous microorganisms.
Foster et al. (2002) documented the morphology of individual cells in great detail (see also Photomicrograph gallery of species of Reduviasporonites Wilson 1962: A joint initiative with Geoscience Australia of Stephenson and Foster at http://www.bgs.ac.uk/taxonomy/reduviasporonites/home.html; Stephenson and Foster, 2002), so in this study, we focus on a comparative analysis of filament characteristics of the Late Permian morphospecies Reduviasporonites stoschianus (for taxonomy and stratigraphic range, see footnote 1). On the basis of a rich and well-preserved palynomorph assemblage recovered from a thin marly-clay interbed (level T14; Broglio Loriga and Cassinis, 1992; for methods, see footnote 1) of the classic P-Tr transition section exposed near the village of Tesero in the Dolomite Mountains, northern Italy, we examine the attractive but so far untested hypothesis, first suggested by Elsik (1999), that the enigmatic microfossils could represent pathogenic fungi. Fungal pathogens are a main driving force of processes in terrestrial ecosystems (e.g., Gilbert, 2002), but apart from proposed disease theories of dinosaur extinction (Casadevall, 2005), their expectable ecological significance at times of major biosphere crisis has so far received little attention and is likely to be greatly underestimated.

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How would proving that the microfossils found in P-Tr transition rocks are a pathogenic fungi help the Authors hypothesis?

FILAMENTS AND AGGREGATES OF REDUVIASPRONITES

The morphospecies Reduviasporonites stoschianus makes up more than 90% of the Tesero palynomorph assemblage (Visscher et al., 1996).
The remains include single cells, fragmented filaments with as many as 24 cells, as well as multicellular aggregates. Filaments are composed of predominantly barrel-shaped cells with an observed length range between 10 and 90 μm. They characteristically produce branches at wide angles (Figs. 1C and 1D). Intertwined filaments can form loose to semicompact aggregates. These structures are usually fragmented (Fig. 1F), but occasionally one may find intact disk-like bodies completely built up by Reduviasporonites (Fig. 1G). Sometimes aggregates may partly consist of narrow cells (Fig. 1E).

The basic filament characteristics of R. stoschianus from Tesero show remarkable resemblance to those of the monilioid hyphae produced by the modern fungal form-genus Rhizoctonia and morphologically allied taxa, a broad and polyphyletic complex of asexually reproducing (anamorphic) soil-borne fungi, which are artificially grouped by general vegetative features (e.g., González García et al., 2006).
The filamentous fungi involved are mostly Basidiomycota, but some represent Ascomycota. Because representatives of this morphological complex never produce conidia, and sexual (teleomorphic) structures are very rare, clear concepts of what constitutes natural species or genera are lacking. Current segregation of phylogenetically related Rhizoctonia-like strains relies largely on experiments with vegetative fusion of hyphae (anastomosis), in combination with DNA sequence data (González García et al., 2006).

With a length:width ratio of 1:1–3:1, barrel-shaped cells of the branched monilioid hyphae of the Rhizoctonia complex (Fig. 1B) are significantly broader and shorter than ordinary extant fungal cells (e.g., Butler and Bracker, 1970). At maturity these specialized hyphae may become relatively thick walled and darkened due to accumulation of melanin. They can strongly proliferate by branching and intertwining to form loosely constructed sclerotia (Fig. 1A) ranging in size from 0.25 to >5 mm in diameter.

The loose construction of the sclerotium, typically without a distinctive rind composed of hardened outer cell layers, is a basic morphological character by which members of the Rhizoctonia complex can be distinguished from other sclerotia producing fungi (Townsend and Willetts, 1954).
The aggregated bodies of fossil Reduviasporonites filaments have an indistinguishable Rhizoctonia-type sclerotial structure.

Why would it be important to distinguish members of the Rhizoctonia complex from other sclerotia producing fungi?

SOIL EROSION

Monilioid hyphae and sclerotia are storage structures that accumulate large amounts of energy-rich compounds, particularly lipids and poly-saccharides (Coley-Smith and Cooke, 1971). In the absence of suitable hosts or under environmental conditions inhibiting fungal growth, the structures remain dormant in the soil. Due to high resistance to chemical and biological degradation this quiescent state can persist for several years. After cell viability is lost, the melanized walls of the resting structures may remain structurally preserved in soils (Watanabe et al., 2007). Therefore,

the common occurrence of soil-borne resting hyphae and sclerotia in waterlain latest Permian sediments provides unmistakable evidence for significant loss of topsoil.

Increased soil erosion at the P-Tr junction is consistent with the presence of degraded soil-derived organic debris in marine sediments (Sephton et al., 2005b) and, at the molecular level, elevated levels of aromatic hydrocarbons, which confirm an intensified burial flux of soil- derived precursor materials (Sephton et al., 2005a; Wang and Visscher, 2007; Nabbefeld et al., 2010).
Strongly increased river discharge and erosion rates are also substantiated by a wealth of sedimentological information from P-Tr fluvial systems (e.g., Newell et al., 2010) and shelf deposits (e.g., Algeo and Twitchett, 2010).

Massive P-Tr soil erosion is generally attributed to worldwide demise of protective deep-rooted plant cover. Paleobotanical and palynological studies corroborate that

tree mortality was a critical element of the end- Permian biosphere crisis.
Unstable Late Permian terrestrial ecosystems underwent preferential loss of arboreal vegetation, while in many parts of the world surviving shrubby and herbaceous plant species played a pioneering role in repopulating deforested terrain (e.g., Looy et al., 2001; Grauvogel-Stamm and Ash, 2005).

How is an increase in soil erosion connected to fungal virulence?

FUNGAL VIRULENCE

The soil-borne origin of Reduviasporonites stoschianus does not support earlier concepts that these fungal resting structures would represent subaerial saprotrophic mycobiota taking advantage of excessive abundances of dead wood (e.g., Visscher et al., 1996). Modern fungi of the Rhizoctonia complex that generate similar large-celled monilioid hyphae and sclerotia are mostly facultative pathogens that can thrive in both dead and living plant materials. Their virulence is normally held in check by the immune system of healthy host organisms, but can accelerate when plants are physiologically weakened, causing root, stem, and foliar diseases of many herbaceous and woody plant species.

In general there is a positive correlation between the concentration of sclerotia of pathogenic Rhizoctonia in soil and disease incidence (Naiki and Ui, 1977).

In the fossil record, direct proof of fungal virulence can only be obtained from structurally preserved plant fossils showing traces of fungal attack.

Permian and Triassic records are very rare, but silicified wood has provided strong evidence that pathogenic wood-rotting fungi could have been well established at the time of the Late Permian biosphere crisis, while patterns of wood decay were similar to those found today (Stubble-field and Taylor, 1986; Creber and Ash, 1990).
So far, infection by soil-borne Rhizoctonia-like pathogens has only been recognized in silicified rhizomes of Eocene plants (Lepage et al., 1994). Indirectly, however, one may consider an essentially facultative-pathogenic lifestyle for the Late Permian Rhizoctonia-like fungi that have produced the Reduviasporonites hyphal and sclerotial structures.

Considering a pathogenic potential for the soil fungi, proliferation of Reduviasporonites would be in harmony with patterns of present-day forest mortality.
Forest decline must be understood as a complex cascade of causes and effects that may lead to a strongly increased susceptibility of trees to fungal disease (e.g., Manion, 1991). Initially, trees can become predisposed to mortality when they are weakened by periodic or chronic environmental stress factors such as drought, excessive temperatures, insect infestation, acidifying and toxic air and soil pollutants, and ionizing and ultraviolet radiation. Increasing propensity to disease then triggers lethal attacks by pests and opportunistic pathogens that successfully invade and colonize stress-weakened trees.

At present, the leading hypothesis explaining the end-Permian ecological crisis is the excessive emission of volcanogenic gases and aerosols accompanying the emplacement of the Siberian Traps igneous province (e.g., Visscher et al., 2004; Erwin, 2006; Svensen et al., 2009). It is increasingly realized that in modern forested ecosystems, drought accompanied by warmer temperatures resulting from greenhouse forcing may lead to increased tree mortality rates worldwide (e.g., Allen et al., 2010).

Since field observations and experimental studies confirm a predisposition of trees to fungal infection by drought stress (e.g., Desprez-Loustau et al., 2006), the spread of probably pathogenic Reduviasporonites is in line with end-Permian crisis scenarios of terrestrial community and ecosystem turnover as a consequence of massive CO2 and/or CH4 release into the atmosphere. However, scenarios emphasizing the effects of stratospheric ozone-layer breakdown could also explain the Reduviasporonites phenomenon.
Growth experiments indicate that roots of trees whose shoots are exposed to harmful levels of UV-B radiation may become susceptible to infection by soil-borne pathogens (Klironomos and Allen, 1995).

There may have been a variety of other globally operating environmental stress factors (e.g., Erwin, 2006), but whatever sequence of events that triggered ecosystem destabilization on land, the aggressiveness of soil-borne pathogenic fungi must have been an integral factor involved in Late Permian forest decline worldwide.

Do you think there was enough information in this article to prove that pathogenic fungi played a part in the Late Permian forest decline? If so what are the major facts that the authors used to prove this?

CONCLUDING REMARKS

In Global Biodiversity Assessment, Stork and Samways (1995, p. 526) qualified soils as “the critical life-support surface on which all terrestrial biodiversity depends.” Soils represent by far the most biologically diverse compartment of the terrestrial biosphere, and nowhere are species so densely packed as in soil communities. Many soil organisms and aboveground plants have coevolved to establish complex mutualistic relationships in which they exchange metabolites and nutrients required for their growth and survival. Unfortunately, structurally preserved remains of soil organisms are extremely rare in the fossil record. In relation to global biosphere crises and associated extinction events, therefore, the study of soil biota still remains terra incognita.

Hence, despite an allochthonous and incomplete nature, the Reduviasporonites mycobiota and associated soil-derived detrital and molecular organic matter offer a unique and intriguing window into the fungal component of P-Tr soil biota.
Further morphological and organic-geochemical comparisons with modern soil- borne organisms and soil organic matter could contribute to an appreciation of the profound ecological and evolutionary consequences of global disruption of host-pathogen equilibria and mutualistic relationships in terrestrial ecosystems at the time of the end-Permian crisis.

Summary of Article "i.e. what you should be able to produce after reading"

The Journal article “Fungal virulence at the time of the end-Permian biosphere crisis?” discusses a study done by Hank Visscher, Mark A. Sephton and Cindy V. Looy which addressed the hypothesis that enigmatic microfossils, namely Reduviasporonites stoschianus, could represent pathogenic fungi and therefore have played a major part in the biosphere crisis seen in Permian–Triassic transition sections worldwide.

The problem with this hypothesis lies in the difficulty of determining exactly what types of microfossils are being seen in the Permian–Triassic rocks being studied. The Genus Reduviasporonites contains multiple types of microfossils that can occur in lacustrine, fluviatile, and marine sediments deposited in a variety of climatic zonations. When these microfossils are interpreted on a morphological basis they are labeled as two types of wood-decaying fungi, Ascomycete Conidia and Conidiophores, which would cause a die back of woody vegetation. When they are interpreted using chemical criteria they are seen as a fresh water green algae of which the Zygnemataceae are thought of as the closest living relatives. This second interpretation would indicate excessive ponding and swamping in the Permian–Triassic sections. The article states that the current accepted hypothesis for the end – Permian crisis is that of an algal Reduviasporonite but that recently the microfossils were shown to have no distinctive biomarkers of algae or fungi. This is due to multiple problems such as the poor preservation potential of the cellulosic walls of filamentous green algae as well as the inability to use Carbon 13 as a marker due to the prominent negative Carbon 13 levels that are globally recognized in carbonates and sedimentary organic matter at the late Permian–Triassic junction. Therefore a conclusive answer to question of what types of microfossils are seen in these Permian–Triassic age rocks can only be done by analyzing the filament characteristics of Reduviasporonites stoschianus.

The analysis of the filament characteristics was performed on a well-preserved palynomorph assemblage found in a thin marly–clay interbed of Permian–Triassic transition section found in the Dolomite Mountains of northern Italy. The filaments that where studied are composed of barrel-shaped cells that typically produce branches at wide angles. These branches can intertwine to form semi compact aggregates called sclerotia. These sclerotia are a basic morphological character of members of the Rhizoctonia complex, which can be used to distinguish them from other sclerotic producing fungi. The conclusion is that fungi in the soil, coupled with the weakening of trees due to massive volcanic outgases during the end Permian did in fact play a role in the die off of vegetation.