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The oldest fossil mushroom

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June 2017
12(6)

DOI:10.1371/journal.pone.0178327

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Authors:

Andrew N Miller

University of Illinois, Urbana-Champaign

Jared Thomas

University of Illinois, Urbana-Champaign

Show all 8 authorsHide

A new fossil mushroom is described and illustrated from the Lower Cretaceous Crato Formation of northeast Brazil. Gondwanagaricites magnificus gen. et sp. nov. is remarkable for its exceptional preservation as a mineralized replacement in laminated limestone, as all other fossil mushrooms are known from amber inclusions. Gondwanagaricites represents the oldest fossil mushroom to date and the first fossil mushroom from Gondwana.

Gondwanagaricites magnificus gen. et sp. nov (A) Photomicrograph of holotype (URM 88000) showing general habitus. (B) Interpretive drawing of (A) with major morphological features indicated. The red box indicates the position of gills shown in Fig 2.

…

Scanning electron micrographs of the gills of Gondwanagaricites magnificus gen. et sp. nov (A) Section of preserved gills (location indicated by red box on Fig 1B). (B) close-up view of (A) showing detailed structure.

…

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RESEARCH ARTICLE

The oldest fossil mushroom

Sam W. Heads

*, Andrew N. Miller

, J. Leland Crane

, M. Jared Thomas

, Danielle

M. Ruffatto

, Andrew S. Methven

, Daniel B. Raudabaugh

1,3

, Yinan Wang

1Illinois Natural History Survey, Prairie Research Institute, University of Illinois at Urbana-Champaign,

Champaign, Illinois, United States of America, 2Department of Biology, Savannah State University,

Savannah, Georgia, United States of America, 3Department of Plant Biology, University of Illinois at Urbana-

Champaign, Urbana, Illinois, United States of America, 4Independent Researcher, Arlington, Virginia, United

States of America

*swheads@illinois.edu

Abstract

A new fossil mushroom is described and illustrated from the Lower Cretaceous Crato For-

mation of northeast Brazil. Gondwanagaricites magnificus gen. et sp. nov. is remarkable for

its exceptional preservation as a mineralized replacement in laminated limestone, as all

other fossil mushrooms are known from amber inclusions. Gondwanagaricites represents

the oldest fossil mushroom to date and the first fossil mushroom from Gondwana.

Introduction

Exceptionally preserved fossils can shed important and unprecedented light on the history of

life. Particularly remarkable deposits, known as Lagersta¨tten, yield fossils characterized by

preservation of soft tissues that decay rapidly and which are not normally preserved. In many

cases, large and important groups of soft-bodied organisms would be missing entirely from

the fossil record if not for their exceptional preservation in Lagersta¨tten. Mushrooms, an

ecologically important group of fungi in the order Agaricales, produce fleshy, gilled fruiting

bodies (called basidiomes) that are rarely fossilized [1]. While certainly ancient, they have an

extremely depauperate fossil record with only ten fossil mushrooms reported to date, all

unique amber inclusions ranging from mid-Cretaceous to Early Miocene in age [2–8]. Here

we report the discovery of a new fossil mushroom that is unique in its preservation as a miner-

alized replacement, and the oldest yet encountered. The specimen comes from the laminated

limestones of the Crato Formation, which outcrop on the northern flanks of the Chapada do

Araripe in Ceara

´, Brazil; a Lagersta¨tte famous for the exceptional preservation of its diverse

Lower Cretaceous paleobiota [9–11].

Material and methods

The specimen comprises a single, nearly complete mushroom preserved as a primarily goethi-

tic replacement on a small slab (approximately 50 ×60 mm) of typical, buff-colored, millime-

trically-laminated limestone from the Nova Olinda Member; the lowermost unit of the

Crato Formation. It is housed in the URM Herbarium at the Universidade Federal de Pernam-

buco in Recife, Brazil, having been repatriated from the Illinois Natural History Survey

PLOS ONE | https://doi.org/10.1371/journal.pone.0178327 June 7, 2017 1 / 6

a1111111111

OPEN ACCESS

Citation: Heads SW, Miller AN, Crane JL, Thomas

MJ, Ruffatto DM, Methven AS, et al. (2017) The

oldest fossil mushroom. PLoS ONE 12(6):

e0178327. https://doi.org/10.1371/journal.

pone.0178327

Editor: William Oki Wong, Institute of Botany,

CHINA

Received: March 26, 2017

Accepted: May 10, 2017

Published: June 7, 2017

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.

Data Availability Statement: All relevant data are

within the paper.

Funding: This work was partly supported by US

National Science Foundation grant EF-1304622 (to

SWH) and EF-1205935 and EF-1502735 (to ANM).

Competing interests: The authors have declared

that no competing interests exist.

Paleontological Collection. It was studied using a Zeiss SteREO Discovery.V20 zoom stereomi-

croscope with a Plan-Apochromat S 0.63x f/ Reo WD = 81 mm objective. Photographs were

taken using a Canon 5D Mark III and MP-E 65 mm macro lens mounted to a Cognisys Stack-

shot motor rail on a copy stand. Multiple high-resolution images were then stacked using Heli-

conSoft’s Helicon Focus 6 and subsequently stitched together as a mosaic using Photoshop

CC. Scanning electron micrographs were produced using a JEOL JSM-6060LV SEM.

Nomenclature

The electronic version of this article in Portable Document Format (PDF) in a work with an

ISSN or ISBN will represent a published work according to the International Code of Nomen-

clature for algae, fungi, and plants, and hence the new names contained in the electronic publi-

cation of a PLOS ONE article are effectively published under that Code from the electronic

edition alone, so there is no longer any need to provide printed copies. In addition, new names

contained in this work have been submitted to MycoBank from where they will be made avail-

able to the Global Names Index. The unique MycoBank number can be resolved and the asso-

ciated information viewed through any standard web browser by appending the MycoBank

number contained in this publication to the prefix http://mycobank.org/MB/. The online ver-

sion of this work is archived and available from the following digital repositories: PubMed

Central, LOCKSS.

Results

Systematic paleontology

Kingdom Fungi (L.) Moore, 1980; Phylum Basidiomycota Moore, 1980; Class Agaricomycetes

Doweld, 2001; Order Agaricales Underwood, 1899; Family incertae sedis

Gondwanagaricites magnificus Heads, A.N. Mill. et J.L. Crane, gen. et sp. nov. (Figs 1

and 2)

[urn:lsid:mycobank.org:names:MB821206]

Holotype. Brazil: Ceara

´: Chapada do Araripe; Crato Formation: Nova Olinda Member

(Lower Cretaceous: Upper Aptian, 113–120 Ma); URM-88000. While precise locality details

are unknown, the lithology of the matrix is consistent with the specimen having been col-

lected in one of the extensive quarry complexes near the town of Nova Olinda (7.0939˚S,

39.6796˚W).

Etymology. The genus name is a combination of Gondwana, the ancient supercontinent,

the Greek word agarikon, “a mushroom,” and the Greek suffix -ites, denoting a fossil. The spe-

cific epithet is the Latin adjective magnificus, meaning “magnificent” or “splendid” in reference

to the remarkable preservation of the holotype.

Description. Basidiome color unknown (preserved as orange-brown goethitic replace-

ment). Pileus 10.0 mm diameter, 7.5 mm high at widest point; apparently circular, convex;

probably glabrous and striate; margin slightly incurved; veil absent; context 3.0 mm thick.

Lamellae (gills) 4.5 mm broad at widest point, broadly attached to stipe apex; edge entire, up to

50μm wide. Stipe 34.0 mm long, 6.5 mm wide, straight, cylindrical, with longitudinal stria-

tions, annulus absent, base slightly bulbous. Basidiospores not observed.

Comments. While Gondwanagaricites is without doubt a gilled mushroom in the Agari-

cales, familial placement is presently impossible since no evidence of basidiospores was found

during SEM examination of the specimen. The general habitus of Gondwanagaricites is remi-

niscent of mushrooms in the family Strophariaceae and placement in this family would be sup-

ported by the small size and robust shape of the overall basidiome, the thick context of the

pileus, the putative complete attachment of the gills to the central stipe, and the apparent

The oldest fossil mushroom

PLOS ONE | https://doi.org/10.1371/journal.pone.0178327 June 7, 2017 2 / 6

absence of a universal and partial veil. However, a number of other mushroom families present

similar basidiome morphology (e.g., Agaricaceae, Tricholomataceae, Bolbitiaceae, etc.) and

can only be separated by detailed studies of basidiospore shape, ornamentation, and colora-

tion. Thus, since the spores of Gondwanagaricites were not observed, we refrain from assigning

the new genus to a family.

Discussion

Fungi are ecologically diverse, geographically widespread, speciose organisms that account for

the second largest group of eukaryotes [12]. Despite their global distribution and evolutionary

history extending some 1,430 Ma [13], the fossil record for fungal structures other than spores

is exceedingly scant with reports of mostly sexual [14–18] and asexual stages [19–23] of asco-

mycetes from mid-Cretaceous to Miocene ambers. The Basidiomycota contains over 30,000

extant species [24], but their fossil record—especially in the case of gilled mushrooms—is

nearly non-existent due to their ephemeral nature and a strong preservational bias against

their fleshy basidiomes [1–8]. The earliest report of a member of the Basidiomycota is from

hyphae with diagnostic clamp connections dating c. 330 Ma from the Upper Visean (Mississip-

pian) of France [25]. Only ten fossils resembling modern-day gilled mushrooms have been

recorded to date, all from amber. The hitherto oldest fossil mushroom, Palaeoagaricites

Fig 1. Gondwanagaricites magnificus gen. et sp. nov. (A) Photomicrograph of holotype (URM 88000) showing general habitus. (B) Interpretive

drawing of (A) with major morphological features indicated. The red box indicates the position of gills shown in Fig 2.

https://doi.org/10.1371/journal.pone.0178327.g001

The oldest fossil mushroom

PLOS ONE | https://doi.org/10.1371/journal.pone.0178327 June 7, 2017 3 / 6

antiquus, was reported from mid-Cretaceous Burmese amber (c. 99 Ma) [6]. More recently,

four unnamed mushrooms placed in the Agaricales have also been reported from Burmese

amber [8]. Archaeomarasmius leggetti was recorded from Cretaceous amber (c. 90–94 Ma)

from New Jersey, USA [3,4]. Most recently, Gerontomyces lepidotus was reported from Eocene

Baltic amber (c. 45–55 Ma) from the Samland Peninsula of Russia [7]. Three other mush-

rooms, Aureofungus yaniguaensis [5], Coprinites dominicana [2], and Protomycena electra [3,4]

have all been recorded from Early Miocene amber (Burdigalian, c. 16–18 Ma) from the

Dominican Republic.

Gondwanagaricites magnificus represents the oldest fossil record of a gilled mushroom and

is the only fossil mushroom known from a mineralized replacement. The unique specimen

extends the geological range of gilled mushrooms back by approximately 14–21 million years

and confirms their presence in Gondwana during the Early Cretaceous. Molecular clock esti-

mates suggest the divergence of the Basidiomycota around 500 Ma to 1.2 billion years [26] and

Fig 2. Scanning electron micrographs of the gills of Gondwanagaricites magnificus gen. et sp. nov.

(A) Section of preserved gills (location indicated by red box on Fig 1B). (B) close-up view of (A) showing

detailed structure.

https://doi.org/10.1371/journal.pone.0178327.g002

The oldest fossil mushroom

PLOS ONE | https://doi.org/10.1371/journal.pone.0178327 June 7, 2017 4 / 6

G.magnificus establishes the earliest calibration point so far for the Agaricales, with a new min-

imum age of 113–120 Ma.

Acknowledgments

We thank Dra. Leonor Costa Maia of the URM Herbarium for providing a URM accession

number and for assistance repatriating the specimen to Brazil. SEM work was carried out in

the Frederick Seitz Materials Research Laboratory Central Research Facilities at the University

of Illinois. This work was partly supported by NSF grant EF-1304622 (to SWH) and EF-

1205935 and EF-1502735 (to ANM).

Author Contributions

Conceptualization: SWH.

Investigation: SWH ANM JLC MJT DMR ASM DBR.

Resources: YW.

Visualization: MJT DMR.

Writing – original draft: SWH ANM JLC MJT DMR ASM.

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Jun 2023

Mimoune Souna

The higher fungi constitute a precious wealth for humanity, some of which have a nutritional quality and an interest in human health as sources of natural biomolecules, also a utility both ecological and economic. The present study aims to present the fungal biodiversity of the wilaya of Tlemcen as well as the selection of seven mushrooms in order to chemically characterize their extracts and evaluate their biological activities. For this, mycological surveys were conducted on the 15 study sites from autumn 2018 to spring 2022. The recognition of macromycetes is based on morphological identification. The results of the mycological inventory indicate a very remarkable fungal biodiversity across the region of Tlemcen, a set of 56 species of mushrooms have been listed, classified into 40 genera and 28 families belonging to 11 orders. Five mushrooms are recorded in Algeria for the first time. The myco-chemical study carried out on the different extracts prepared (hydro-methanolic, hexane, dichloromethane and AEEM mixture) is performed, by myco-chemical screening, spectrophotometric assays of total polyphenols, flavonoids, condensed tannins, flavonols, saponins and triterpenoids as well as the determination of β-carotene and lycopene. Furthermore, GC-MS analyses were performed for the selected extracts. First, in order to determine the toxicity of the different extracts, the hemolysis test was performed in vitro against human red blood cells. The total antioxidant capacity, DPPH● , ABTS●+ radical scavenging and iron reducing power (FRAP) tests were used to evaluate the in vitro antioxidant capacity of the extracts. The anti-inflammatory activity of the extracts was monitored in vitro by the heat denaturation protein inhibition method and also by the erythrocyte membrane stabilization method which includes heat-induced hemolysis. Determination of antihemolytic activity and investigation of the α-amylase inhibitory effect of the extracts were performed. hydro-methanolic, hexane, dichloromethane and AEEM mixture It is necessary to mention the considerable toxicity levels of the extracts of dichloromethane of Tricholoma pseudonictitans, the hydro-methanolic of Boletus satanas and the hexane of Suillus collinitus towards human erythrocytes with rates respectively (38.35 ± 2.64%; 28.07 ± 1.41% and 26.03 ± 0.56%). The level of hemolysis in other extracts still meets safety standards. The hydro-methanolic extract of Melanogaster broomeianus reported the highest contents of total and reducing sugars (494.70 ± 7.95 and 406.46 ± 16.80 µg EG/mg Ext-S respectively). The different results acquired revealed the richness of the tested extracts in secondary metabolites. The (IC 50 ) of ABTS test of the mixture extract of (AEEM) of Pleurotus eryngii var. ferulae, the mixture extract (AEEM) of M. broomeianus, the hexane and the dichloromethane extract of S. collinitus, the dichloromethane extract of B. satanas and the hydro-methanolic extract of Suillus mediterrneensis were higher than the standard. The (EC 50 ) of FRAP test of the dichloromethane extract of S. collinitus was higher than that of ascorbic acid. The dichloromethane extract of P. eryngii var ferulae, the hydro-methanolic extract and the mixture extract (AEEM) of M. broomeianus and the hydro-methanolic extract of Terfezia claveryi showed a very interesting protective activity against protein denaturation. T. claveryi, P. eryngii var. ferulae, M. broomeianus species showed protective ability against heat-induced hemolysis. M. broomeianus and P. eryngii var. ferulae species showed more potent anti-hemolytic protection than the standard.

Mycophagous rove beetles highlight diverse mushrooms in the Cretaceous

Article

Full-text available

Apr 2017

Agaricomycetes, or mushrooms, are familiar, conspicuous and morphologically diverse Fungi. Most Agaricomycete fruiting bodies are ephemeral, and their fossil record is limited. Here we report diverse gilled mushrooms (Agaricales) and mycophagous rove beetles (Staphylinidae) from mid-Cretaceous Burmese amber, the latter belonging to Oxyporinae, modern members of which exhibit an obligate association with soft-textured mushrooms. The discovery of four mushroom forms, most with a complete intact cap containing distinct gills and a stalk, suggests evolutionary stasis of body form for B99 Myr and highlights the palaeodiversity of Agaricomycetes. The mouthparts of early oxyporines, including enlarged mandibles and greatly enlarged apical labial palpomeres with dense specialized sensory organs, match those of modern taxa and suggest that they had a mushroom feeding biology. Diverse and morphologically specialized oxyporines from the Early Cretaceous suggests the existence of diverse Agaricomycetes and a specialized trophic interaction and ecological community structure by this early date.

A fossil Aspergillus from Eocene Dominican amber

Article

Full-text available

Jan 1988

A sporulating Aspergillus is described from a piece of Eocene amber originating from the Dominican Republic. The Aspergillus most closely resembles a form of the white spored phase of Aspergillus janus Raper and Thom. This is the first report of a fossil species of Aspergillus. -Authors

Another fossil agaric from Dominican amber

Article

Jul 2003

We report the discovery of a fossil agaricoid homobasidiomycete from Dominican amber (ca 15–20 Ma). Aureofungus yaniguaensis appears to be a member of the euagarics clade, but its precise taxonomic placement is obscure. This is the fourth known fossil agaric and the third from Dominican amber.

Perithecial ascomycetes from the 400 million year old Rhynie chert: an example of ancestral polymorphism

Article

Mar 2005

We describe a perithecial, pleomorphic ascomycetous fungus from the Early Devonian (400 mya) Rhynie chert; the fungus occurs in the cortex just beneath the epidermis of aerial stems and rhizomes of the vascular plant Asteroxylon. Perithecia are nearly spherical with a short, ostiolate neck that extends into a substomatal chamber of the host plant; periphyses line the inner surface of the ostiole. The ascocarp wall is multilayered and formed of septate hyphae; extending from the inner surface are elongate asci interspersed with delicate paraphyses. Asci appear to be unitunicate and contain up to 16 smooth, uniseriate-biseriate ascospores. The method of ascospore liberation is unknown; however, the tip of the ascus is characterized by a narrow, slightly elevated circular collar. Ascospores appear 1–5 celled, and germination is from one end of the spore. Also present along the stems and interspersed among the perithecia are acervuli of conidiophores that are interpreted as the anamorph of the fungus. Conidiogenesis is thallic, basipetal and probably of the holoarthric-type; arthrospores are cube-shaped. Some perithecia contain mycoparasites in the form of hyphae and thick-walled spores of various sizes. The structure and morphology of the fossil fungus is compared with modern ascomycetes that produce perithecial ascocarps, and characters that define the fungus are considered in the context of ascomycete phylogeny.

A gilled mushroom, Gerontomyces lepidotus gen. et sp. nov. (Basidiomycota: Agaricales), in Baltic amber

Article

Jun 2016

George Poinar

A densely scaled small mushroom in Baltic amber is described as Gerontomyces lepidotus gen. et sp. nov. and is characterized by a convex pileus 1.0 mm in diameter, distant to subdistant lamellae with smooth margins and a centrally inserted cylindrical, solid stipe. Its taxonomic placement is uncertain. This is the first mushroom described from Baltic amber.

The Crato Fossil Beds of Brazil: Window into an Ancient World

Book

Jan 2007

This beautifully illustrated 2007 volume describes the entire flora and fauna of the famous Lower Cretaceous Crato Formation of Brazil - one of the world's most important fossil deposits, exhibiting exceptional preservation. A wide range of invertebrates and vertebrates are covered, including extended sections on pterosaurs and insects. Two chapters are devoted to plants. Many of the chapters include descriptions of new species and re-descriptions and appraisals of taxa published in obscure places, rendering them available to a wider audience. Fossil descriptions are supported by detailed explanations of the geological history of the deposit and its tectonic setting. Drawing on expertise from around the world and specimens from the most important museum collections, this book forms an essential reference for researchers and enthusiasts with an interest in Mesozoic fossils.

Fossils of the Santana and Crato formations

Article