Biodiversity Data Journal : Taxonomy & Inventories
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Taxonomy & Inventories
Expanding geographic distribution knowledge of Galerina marginata (Batsch) Kühner (Agaricales, Hymenogastraceae) with a novel Antarctic record
expand article infoFernando Augusto Bertazzo-Silva‡, Jair Putzke‡, Cassiane Furlan-Lopes‡, Maricia Fantinel D'ávila§, Alice Lemos Costa‡, Evelise Leis Carvalho‡, Ana Flavia Zorzi‡, Carlos Ernesto Gonçalves Reynaud Schaefer|
‡ Laboratório de Taxonomia de Fungos, Universidade Federal do Pampa (UNIPAMPA), São Gabriel, RS, Brazil
§ Universidade Federal do Pampa (UNIPAMPA), São Gabriel, RS, Brazil
| Universidade Federal de Viçosa, Departamento de Solos, Viçosa, MG, Brazil
Corresponding author: Fernando Augusto Bertazzo-Silva (fernandobertazzo@gmail.com)
Academic editor: Renan Barbosa
Received: 18 Apr 2024 | Accepted: 15 Jun 2024 | Published: 21 Jun 2024
© 2024 Fernando Augusto Bertazzo-Silva, Jair Putzke, Cassiane Furlan-Lopes, Maricia D'ávila, Alice Costa, Evelise Carvalho, Ana Zorzi, Carlos Schaefer
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Bertazzo-Silva FA, Putzke J, Furlan-Lopes C, D`ávila M, Costa A, Carvalho E, Zorzi A, Schaefer CGR (2024) Expanding geographic distribution knowledge of Galerina marginata (Batsch) Kühner (Agaricales, Hymenogastraceae) with a novel Antarctic record. Biodiversity Data Journal 12: e125727. https://doi.org/10.3897/BDJ.12.e125727
 Open Access

Abstract

Background

The investigation of Agaricales diversity in the Antarctica is limited, with only seven genera reported for the region. Galerina stands out as the genus with the highest species diversity, including 12 species in Antarctica. This research reports the presence of G. marginata in the region, providing the first complete morphological description for the specimen developing in Antarctica. Sampling was conducted during the Austral summer of 2022/2023 as part of the XLI Brazilian Antarctic Operation in Point Smellie, Byers Peninsula, Livingston Island, South Shetland Archipelago, Antarctica. Phylogenetic relationships reconstructed by Maximum Likelihood demonstrate that G. marginata forms a monophyletic clade with over 60% bootstrap support in most branches. The isolate in this study was found to be internal to the main cluster. Evolutionary reconstructions using the Maximum Likelihood method indicate that the branches correspond to the Antarctic isolate being an internal clade within the marginata group. Recording fungal populations in polar regions offers information about their adaptation and survival in inhospitable environments. Understanding the species' distribution in Antarctica encourages future investigations into its ecology and interactions with other organisms. Here, data are presented to establish an initial foundation for monitoring the G. marginata population in Antarctica and assessing the potential impacts of climate change on its development and survival in the forthcoming years.

New information

We report the third occurrence of Galerina marginata (Batsch) Kühner in Antarctica and provide, for the first time, a comprehensive morphological description of an individual of the species for the Antarctic continent, accompanied by phylogenetic analyses and comprehensive discussions regarding its diversity and global distribution.

Introduction

The Antarctic continent is known as one of the most inhospitable places on the Planet due to its meteorological conditions and geographical isolation (Lecordier et al. 2023). It is divided into two primary sectors: Continental Antarctica, which includes ice-free regions such as the McMurdo Dry Valleys, Windmill Islands and inland nunataks; and Maritime Antarctica, which extends along the western coast of the Antarctic Peninsula and the archipelagos of the Scotia Arc, reaching northwards to South Georgia, which is designated as part of the sub-Antarctic region (Colesie et al. 2023).

The Antarctic Peninsula and adjacent islands in Maritime Antarctica experience distinct seasons influenced by the Southern Ocean. Summers are brief, with temperatures above freezing and extended daylight hours, significantly impacting annual precipitation. Conversely, winters are characterised by temperatures ranging from -10°C to -12°C, prolonged nights and the formation of sea ice (Yu et al. 2024). In Polar Regions, physical environmental conditions often exert a more pronounced influence than biological factors (Peck et al. 2006). This suggests that climate, soil, ice and other physical factors play a substantial role, often overriding biological conditions in determining the life and adaptation of organisms in these regions.

Due to the extreme conditions in Antarctica, research on its biodiversity is crucial for understanding the distribution and adaptive capabilities of extremophile organisms. Although more than 70 genera of Agaricales have been reported for the continent in biodiversity databases (GBIF.org 2024b), the diversity and distribution of Agaricales in Antarctica in scientific literature remain understudied. Reports indicate only seven genera in the region: Arrhenia Fr. (= Leptoglossum P. Karst.), Galerina Earle, Lichenomphalia Redhead, Lutzoni, Moncalvo and Vilgalys (= Owingsia I. Saar, Voitk and Thorn), Omphalina Quél., Pholiota (Fr.) P. Kumm., Rimbachia Pat. and Simocybe P. Karsten (Putzke et al. 2012, Palfner et al. 2020, MycoBank Database 2024). Amongst these, Galerina stands out as the genus with the highest species diversity, with 12 species thriving in the Antarctic Region, as indicated by Garrido-Benavent et al. (2023).

The genus Galerina comprises approximately 300 species and typically produces basidiomata commonly associated with living bryophytes, functioning as saprophytes or being confined to woody material and other plant remnants (Horak 1994, Gulden et al. 2005). Recent studies have shown that lethal mushrooms of the genus colonised Antarctica as early as the Pleistocene, concurrent with the estimated colonisation of plants such as the grass Deschampsia antarctica Desv., mosses and some amphitropical lichens on the continent (Garrido-Benavent et al. 2023). Despite their presence on the Antarctic continent for thousands of years, studies related to the genus Galerina are still in their early stages, highlighting the need for more comprehensive research on their diversity in Antarctica to clarify distribution issues and provide consistent information on the impacts of climate change on Galerina spp. populations.

This study presents a novel finding of Galerina marginata (Batsch) Kühner in Antarctica through the collection of Agaricales fungi in the South Shetland Islands. The primary contribution of this research lies in providing new insights into the morphology, phylogeny and distribution of G. marginata on the Antarctic Continent, offering novel and relevant information on the bionomy and ecology of this species in the region. This research aims to report, for the first time in scientific literature, the presence of G. marginata on the Byers Peninsula (Livingston Island, Antarctica), providing morphological and phylogenetic data on the species.

Materials and methods

Study site

The samplings were carried out in the austral summer of 2022/2023 as part of the XLI Brazilian Antarctic Operation at Point Smellie, Byers Peninsula, Livingston Island, South Shetland Archipelago, Antarctica (62°39'12.6"S, 61°08'44.6"W) (Fig. 1). The specimens were photographed and collected using tweezers, along with detailed documentation of the mushrooms' morphology, the geographical coordinates of their location and the substrate on which they were discovered. Subsequently, a fraction of the specimens underwent desiccation in a 40°C oven, while the remaining portion was preserved fresh for molecular analysis. All samples were transported to Brazil and stored frozen at -20°C.

Figure 1.  

Location map of the collection area. Antarctica, Antarctic Peninsula, Livingston Island, Byers Peninsula, Point Smellie. Created in QGIS 3.32.0 software and designed in PhotoFiltre Studio X 10.12.1 software.

Morphological characterisation and classification

The morphological characterisation and examination of organism structures were initially conducted in the field in Antarctica and subsequently continued at the Laboratório de Taxonomia de Fungos (LATAF) at Universidade Federal do Pampa (UNIPAMPA), São Gabriel, Rio Grande do Sul State, Brazil. Microscope slides were prepared using a 3% potassium hydroxide (KOH) solution and observed under the Axio Scope A1 Binocular Microscope. The microscopic characterisation involved measuring 25 specimens of each microscopic structure, with means followed by standard deviations presented and the maximum and minimum sizes of each structure included in parentheses. Following the analyses, samples of the material were dehydrated in an oven at 40°C and subsequently deposited in the Bruno Edgar Irgang Herbarium (HBEI 127).

For the verification of the current taxonomic classification and synonyms of Galerina marginata, the Catalogue of Life and Index Fungorum platforms were employed. To analyse the worldwide geographical distribution of the species, specialised bibliographies, the Global Biodiversity Information Facility and Barcode of Life Data System platforms were consulted.

DNA extraction, PCR amplification and sequencing

Fungal DNA extraction utilised desiccated frozen tissue obtained from G. marginata. These extractions were performed using an E.Z.N.A.® Fungal DNA Mini Kit, Omega Bio-tek. DNA sequences of the ITS region (ITS1–5.8S–ITS2) were obtained by primers ITS1 (5’-CTTGGTCATTTAGAGGAAGTAA-3’) and ITS4 (5’-TCCTCCGCTTATTGATATGC-3’) (Sappington and Taylor 1990, White et al. 1990). PCR was performed for a final volume of 25 μl containing: 25 ng of genomic DNA (1 μl), 20 mM of each primer (0.25 μl) 10 mM of dNTP mix (2 μl), 50 mM of MgCl2 (0.75 μl) 10 × PCR buffer (2.5 μl), Taq polymerase at 5 U/μl (0.25 μl) (Ludwig Biotecnologia) and Milli-Q water to complete the reaction. The PCR reaction was performed following White et al. (1990) adapted conditions: 94°C for 2 min, followed by 35 cycles at 94°C for 30 s, 55°C for 40 s and 72°C for 1 min and a final extension of 72°C for 1 min. The PCR product was purified using a column PCR Product Purification Kit (Ludwig Biotecnologia) and sequenced automatically in a sequencer (ABI 3500 XL Applied Biosystems).

Phylogenetic analysis

For the phylogenetic analysis, the BLAST search was performed at the National Center for Biotechnology Information (NCBI) and closely related sequences were downloaded from GenBank. Evolutionary analysis using the Maximum Likelihood method was conducted to reconstruct the evolutionary history of G. marginata. The Tamura 3-parameter model (Tamura and Nei 1993) was employed within the Maximum Likelihood framework. A bootstrap consensus tree was inferred from 10,000 replicates (Kumar et al. 2018). Branches in partitions reproduced in fewer than 50% of bootstrap replicates were collapsed (Felsenstein 1985). The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (10,000 replicates) is shown next to the branches. Initial trees for the heuristic search were automatically obtained by applying the Neighbour-Joining and BioNJ algorithms to a matrix of pairwise distances estimated using the Maximum Composite Likelihood (MCL) approach, then selecting the topology with the highest log likelihood value. A discrete Gamma distribution was utilised to model evolutionary rate differences amongst sites (1,000 categories; G parameter = 0.2683). The analysis involved 51 taxa (nucleotide sequences), with 47 in the in-group and four in the out-group. (Table 1). There were a total of 1,303 positions included (1st + 2nd + 3rd + non-coding) in the final dataset. Evolutionary analyses were conducted using RAxML v.8 (Stamatakis 2016).

Table 1.
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Species and GenBank accession numbers of sequences used in this study (newly-generated sequence are indicated in bold).

Species

Strain/Voucher

Location

GenBank Accession No.

Galerina allospora

O 73460

United Kingdom

AJ585452.1

Galerina arctica

O 50535

Norway

AJ585441.1

Galerina atkinsoniana

O 73459

United Kingdom

AJ585479.1

Galerina calyptrata

O 73449

Germany

AJ585465.1

Galerina cephalotricha

O 154146

Norway

AJ585462.1

Galerina chionophila

O 73463

Switzerland

AJ585506.1

Galerina clavata

O 72166

Denmark

AJ585436.1

Galerina fallax

O 154355

Norway

AJ585451.1

Galerina fibrillosa

MICH 40850

USA

AJ585473.1

Galerina harrisonii

O 50711

Norway

AJ585463.1

Galerina hybrida

O 73458-2

Germany

AJ585445.1

Galerina hypnorum

MICH 46302

USA

AJ585470.1

Galerina jaapii

O 154387

Finland

AJ585505.1

Galerina laevis

O 70903

Norway

AJ585439.1

Galerina lubrica

O 154034

Norway

AJ585471.1

Galerina luteolosperma

O 154076

Norway

AJ585453.1

Galerina marginata

O 72427

USA

AJ585500.1

Galerina marginata

O 300011

USA

AJ585497.1

Galerina marginata

O 72507

USA

AJ585496.1

Galerina marginata

UBC F32027

Canada

KX236118.1

Galerina marginata

LFGM 2401

Antarctica

PP346498.1

Galerina marginata

ARIOS_GalMar

Antarctica

OQ569484.1

Galerina marginata

SAT-21-248-01

USA

ON787723.1

Galerina marginata

Amsler-2012

Antarctica

OP795715.1

Galerina marginata

ZR4

Iran

OR504254.1

Galerina marginata

UBC F32036

Canada

KX236132.1

Galerina marginata

191

Finland

PP152355.1

Galerina marginata

LE-BIN 2479

Russia

KY327296.1

Galerina minima

O 154480

Norway

AJ585486.1

Galerina mniophila

O 60574

Norway

AJ585459.1

Galerina nana

O 153723

Norway

AJ585490.1

Galerina paludosa

O 73462

Estonia

AJ585447.1

Galerina pruinatipes

O 73438

France

AJ585510.1

Galerina pseudobadipes

O 154252

Norway

AJ585474.1

Galerina pseudocamerina

O 73471

Germany

AJ585507.1

Galerina pseudocerina

O 153998

Norway

AJ585431.1

Galerina pseudomycenopsis

O 50526

Norway

AJ585501.1

Galerina pumila

O 73440

Germany

AJ585477.1

Galerina salicicola

K 99448

United Kingdom

AJ585493.1

Galerina sphagnicola

O 73441

Estonia

AJ585464.1

Galerina sphagnorum

O 70913

Norway

AJ585454.1

Galerina stordalii

O 154169

Norway

AJ585435.1

Galerina stylifera

UBC F-25666

Canada

MF954881.1

Galerina tibiicystis

O 72930

Norway

AJ585443.1

Galerina triscopa

O 73453

France

AJ585491.1

Galerina vittiformis

O 154565

Norway

AJ585487.1

Hebeloma mesophaeum NYS:NYS-F-001411 USA MN006662.2
Hebeloma smithii MICH:MICH 10730 USA MK280985.1
Psathyloma leucocarpum JAC12071 New Zealand KT591551.1
Psathyloma leucocarpum K. Soop KS-BR185 New Zealand KT591553.1

Taxon treatment

Galerina marginata (Batsch) Kühner

Nomenclature

= Agaricus autumnalis Peck, Ann. Rep. Reg. N.Y. St. Mus. 23: 92 (1872) [1870]

= Agaricus caudicinus var. denudatus Pers., Syn. meth. fung. (Göttingen) 2: 272 (1801)

= Agaricus marginatus Batsch, Elench. fung., cont. sec. (Halle): 207 (1789)

= Agaricus mutabilis var. marginatus (Batsch) Fr., Hymenomyc. eur. (Upsaliae): 225 (1874)

= Agaricus unicolor Vahl, Fl. Danic. 6: 7 (1792)

= Dryophila marginata (Batsch) Quél., Enchir. fung. (Paris): 69 (1886)

= Dryophila unicolor (Vahl) Quél., Enchir. fung. (Paris): 69 (1886)

= Flammula marginata (Batsch) Fayod, Annls Sci. Nat., Bot., sér. 7 9: 361 (1889)

= Galera marginata (Batsch) P. Kumm., Führ. Pilzk. (Zerbst): 74 (1871)

= Galera unicolor (Vahl) Ricken, Die Blätterpilze: Pl. 56, figs 4, 7 (1912)

= Galerina autumnalis (Peck) A.H. Sm. and Singer, Monogr. Galerina: 246 (1964)

= Galerina autumnalis f. robusta Thiers, Mycologia 51(4): 534 (1960) [1959]

= Galerina autumnalis var. angusticystis A.H. Sm., Monogr. Galerina: 249 (1964)

= Galerina autumnalis var. robusta Thiers, Beitr. Naturk. Forsch. Südwestdeutschl.: 249 (1964)

= Galerina unicolor (Vahl) Singer, Beih. Botan. Centralbl., Abt. 2 56: 170 (1936)

= Galerina unicolor f. fibrillosa Arnolds, Biblthca Mycol. 90: 379 (1982)

= Galerina unicolor f. paucicystidiata Arnolds, Biblthca Mycol. 90: 378 (1982)

= Galerula marginata (Batsch) Kühner, Bull. trimest. Soc. mycol. Fr. 50: 78 (1934)

= Galerula unicolor (Vahl) Kühner, Bull. trimest. Soc. mycol. Fr. 50: 78 (1934)

= Gymnopilus autumnalis (Peck) Murrill, N. Amer. Fl. (New York) 10(3): 200 (1917)

= Naucoria autumnalis (Peck) Sacc., Syll. fung. (Abellini) 5: 834 (1887)

= Pholiota autumnalis (Peck) Peck, Bull. N.Y. St. Mus. 122: 156 (1908)

= Pholiota marginata (Batsch) Quél., Mém. Soc. Émul. Montbéliard, Sér. 2 5: 127 (1872)

= Pholiota marginata subsp. mustelina (Quél.) P. Karst., Bidr. Känn. Finl. Nat. Folk 32: 305 (1879)

= Pholiota marginata var. tremulae Pilát, Stud. Bot. Čechoslov. 11: 166 (1950)

= Pholiota unicolor (Vahl) Gillet, Hyménomycètes (Alençon): 436 (1876) [1878]

= Ryssospora marginata (Batsch) Fayod, Annls Sci. Nat., Bot., sér. 7 9: 361 (1889)

Material   Download as CSV 
  1. taxonomicStatus:
    accepted
    ; scientificNameID:
    Galerina marginata
    ; kingdom:
    Fungi
    ; phylum:
    Basidiomycota
    ; class:
    Agaricomycetes
    ; order:
    Agaricales
    ; family:
    Hymenogastraceae
    ; genus:
    Galerina
    ; specificEpithet:
    marginata
    ; scientificNameAuthorship:
    (Batsch) Kühner
    ; continent:
    Antarctica
    ; islandGroup:
    South Shetland Islands
    ; island:
    Livingston Island
    ; locality:
    Byers Peninsula, Point Smellie.
    ; verbatimLatitude:
    62°39'12.6"S
    ; verbatimLongitude:
    61°08'44.6"W
    ; decimalLatitude:
    -62.653500
    ; decimalLongitude:
    -61.145723
    ; year:
    2023
    ; month:
    01
    ; day:
    24
    ; habitat:
    Growing in a coastal moss field.
    ; fieldNotes:
    Basidiomata are scattered in an area with vegetation predominantly composed of Sanionia uncinata (Hedw.) Loeske
    ; associatedSequences:
    GenBank: PP346498.1
    ; identificationID:
    Galerina marginata
    ; identifiedBy:
    Fernando Augusto Bertazzo-Silva, Jair Putzke
    ; dateIdentified:
    2024
    ; institutionCode:
    HBEI127
    ; collectionCode:
    Fungi
    ; basisOfRecord:
    PreservedSpecimen
    ; occurrenceID:
    7209E6AB-A5FE-5819-A500-5CE116BBC10D

Description

Pileus 7–31 mm diameter, initially campanulate to hemispherical and then flat-convex to convex (Fig. 2A). Margin involute to revolute as the basidiome develops. Hymenophore with lamellae adnate to slightly emarginate. Stipe 2–8 x 4–17 mm, central, cylindrical. Basal mycelium is absent. Spore print not obtained (Fig. 2A). Basidiospores (9.3) 11.4 ± 1.4 (13.3) x (5.5) 6.4 ± 0.4 (7.2) µm, Q = (1.29) 1.78 (2.42), ellipsoid to amygdaliform, moderately rugulose to verrucose, heavily pigmented (Fig. 2B). Basidia (24.0) 29,3 ± 2.6 (34.3) x (6.9) 9.3 ± 1.6 (12.82) x (3.6) 5.8 ± 1.2 (8.47) µm, clavate, hyaline, four-spored (Fig. 2C). Pleurocystidia (18.4) 34.3 ± 9 (48.8) x (7.6) 10.0 ± 2.1 (14.1) x (3.6) 6.1 ± 1.9 (9.4), utriform to slightly lageniform, hyaline (Fig. 2D). Cheilocystidia (29.0) 37.8 ± 12.6 (57.79) x (7.7) 10.5 ± 1.9 (12.2) x (4.8) 5.1 ± 0.2 (5.3) x (5.2) 5.8 ± 0.4 (6.3) µm, lageniform to ventricose-fusoid and slightly fusiform, hyaline (Fig. 2E, F). Caulocystidia (59) 63.9 ± 7.9 (78.1) x (11.2) 12.7 ± 0.7 (13), hyphoid to utriform, hyaline to slightly pigmented (Fig. 2G). Pileocystidia were not observed. Regular lamellar context. Pileipellis is composed of prostrate to periclinal hyphae, encrusted with pigments (Fig. 2I, J). Clamp connections were not observed.

Figure 2.  

Galerina marginata. A Basidiome in Laboratory; B Spores; C Basidia; D Pleurocystidia; E, F Cheilocystidia; G Caulocystidia; H Lamellar trama; I, J Pileipellis. Scale bar in B, C, D, E, F, G, H and J - 10 μm. In I - 100 μm.

Ecology

Growing in a coastal moss field. Basidiomata are scattered in an area with vegetation predominantly composed of Sanionia uncinata (Hedw.) Loeske.

Analysis

Phylogenetic analysis

Phylogenetic relationships reconstructed by Maximum Likelihood demonstrate that Galerina marginata forms a monophyletic clade with over 60% bootstrap support in most branches (Fig. 3). The isolate in this study was found to be internal to the main cluster. Evolutionary reconstructions using the Maximum Likelihood method indicate that the branches correspond to the Antarctic isolate being an internal clade within the marginata group. The same species, OQ569484.1, found in Antarctica (South Shetland Islands, Livingston Island, Punta Hannah) and OP795715.1, also in Antarctica (Norsel Point, Amsler Island), exhibited behaviour as a sister clade with over 60% bootstrap support (Fig. 3).

Figure 3.  

Maximum Likelihood phylogenetic tree, based on 1,303 nucleotide positions within the ITS1-5.8S-ITS2 region. The specimen isolated in this study is highlighted in bold. Antarctic specimens are highlighted in a red box. The yellow box highlights the out-group and the grey box represents the in-group. The Galerina lineages are divided by colours according to Guldem et al (2005): Naucoriopsis: black. Galerina: green. Mycenopsis: brown. Tubariopsis: blue. Values alongside the branches indicate bootstrap support greater than 60%. The scale bar at the bottom of the topology indicates substitutions per site, with a value of 0.05.

Discussion

The findings presented in this study mark the third documented occurrence of Galerina marginata in Antarctica and, notably, it represents the first comprehensive morphological description of an individual of this species developing on the Antarctic Continent. Previously, Arenz et al. (2014) reported the presence of G. marginata on Amsler Island, while Garrido-Benavent et al. (2023) conducted a phylogenetic study focusing on specimens collected in Punta Hannah, Livingston Island, to understand the evolution of this species.

The morphological characteristics, particularly the size and shape of the pileus, as well as the size and form of the spores described by Garrido-Benavent et al. (2023), closely correspond to those observed in this study, indicating similarity amongst individuals of the species found on the Antarctic Continent. However, the absence of descriptions of other structures of G. marginata limits more comprehensive comparisons.

In comparison with collections worldwide, the specimen collected in Antarctica and detailed in this study exhibits variations and similarities in its macroscopic characteristics (Table 2). The size of the pileus in the described specimen ranged from 7 to 31 mm, while other individuals had pilei ranging from 5 to 45 mm. Across all samples, the pileus shapes displayed remarkable similarity, with the majority of individuals initially possessing campanulate to hemispherical pilei that later became convex as the fungus developed. Nevertheless, other forms such as umbonate, depressed, flattened and bell-shaped were also documented. The attachment of the lamellae to the stem varied from adnate, subdecurrent or adnexed to slightly emarginate or decurrent. Notably, our sample was the only one displaying an emarginate shape during its development. Moreover, our specimen stands out as the individual with the smallest stipe. While stipe sizes ranged from 20 to 60 mm in other specimens, our sample exhibited a size ranging from 4 to 17 mm (Cho et al. 2016, Gulden and Hallgrimsson 2000, Akata et al. 2020, Prydiuk 2020). The aforementioned differences may be influenced by the development substrate and possible extreme climate conditions that could impact the species' growth process. However, more comprehensive studies focused on the bionomics and distribution of the species on the continent are needed for more robust confirmations (Table 2).

Table 2.
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Morphological characterisation of Galerina marginata.

This study

Gulden and Hallgrimsson (2000)

Cho et al. (2016)

Prydiuk (2020)

Akata et al. (2020)

Antartica

Iceland

Korea

Ukraine

Turkey

Pileus

7–31 mm, initially campanulate to hemispherical and then flat-convex to convex

10-40 mm, conic, ± umbonate or even papillate, becoming convex to plane, sometimes also slightly depressed, moist ± sticky to viscid

15–35 mm, convex or conical when young, then expanded, piano-convex or flattened when mature

5-30 mm, initially hemispherical, bell-shaped or convex, later convex-spreading to spreading, often with a low bump in the centre

20–45 mm, broad, hemispherical at first and then became convex to plano-convex with an obtuse umbo

Lamellae

Adnate to slightly emarginate

Adnate to slightly decurrent

Subdecurrent

Adnate

Adnexed to slightly decurrent

Stipe

4–17 x 2–8 mm

20–60 x 2–5 mm

20–40 × 4–8 mm

20–55 mm x 2–5 mm

22–40 mm × 2–5 mm

Spore

(9.3) 11.4 (13.3) x (5.5) 6.4 (7.2) µm, Q = (1.29) 1.78 (2.42), ellipsoid to amygdaliform, moderately rugulose to verrucose

(8.5-)9–10.5 x 5.5–6.5 μm, Av (40/4) = 9.7 x 5.9 μm, Q = 1.5-1.8, Q./30) = 1.6, amygdaliform to ellipsoid, rugulose-verruculose

(9.4) 9.7 (10.2) × (5.6) 6.1 (6.7) μm, Q = (1.47) 1.60 (1.72), ellipsoidal to oval

(7,5–)8,0–9.5(–11.0) × 5.0–6.5 μm, Q = 1,36– 1.83; av. L = 8.9 ± 0.71 μm, av. B = 5.7 ± 0.37 μm, av. Q = 1.57 ± 0.09, rugulose to verrucose

8–10 × 5–6 μm, elliptical to amygdaliform, moderately verrucose

Basidia

(24.0) 29.3 (34.3) x (6.9) 9.3 (12.82) x (3.6) 5.8 (8.47), clavate, four-spored

22.5–32 x 7.5–8 μm, constricted, four-spored

27.7–35.3 × 7.8–10.4 μm, clavate, four-spored

17.0–25.0 × 7.0–8.5 μm, club-shaped, two- and four-spored

25–30 × 7–8 μm, cylindrical to clavate, hyaline, four-spored

Cheilocystidia

(29.0) 37.8 (57.79) x (7.7) 10.5 (12.2) x (4.8) 5.1 (5.3) x (5.2) 5.8 (6.3) µm, lageniform to ventricose-fusoid

40–65 x 9–14.5 x 3–5 x 3–7 μm, ventricose- (sub)capitate, head often ellipsoid to spearhead-shaped, rarely tip not inflated

51.3–62.2 × 8.2–9.1 μm, fusiform-ventricose to obclavate, abundant

35.0–50.0 × 7.0–14.5 μm, spindle-shaped, apex rounded or slightly thickened

35–55 × 10–15 μm, lageniform to fusiform

Pleurocystidia

(18.4) 34.3 (48.8) x (7.6) 10.0 (14.1) x (3.6) 6.1 (9.4), Utriform to slightly lageniform

Scattered, often few, similar to cheilocystidia

52.4–77.2 × 11.4–13.9 μm, fusiform-ventricose to obclavate

40.0–75.0 × 13.0–17.0 μm, spindle-shaped, apex rounded or slightly thickened

Similar to cheilocystidia

Caulocystidia

(59) 63.9 (78.1) x (11.2) 12.7 (13), hyphoid to utriform, hyaline to slightly pigmented

Rather few, similar to the cheilocystidia

-

Two types: a) 50.0–85.0 × 9.5–17.0 μm, spindle-shaped, apex rounded or slightly thickened; b)20.0–31.0 × 6.5–8.0 μm, club-shaped

-

Pileipellis

Prostrate to periclinal hyphae, encrusted with pigments

-

-

Hyphae 2.5–6.0 μm thick, somewhat mucilaginous in the upper layers, with a light granular pigment encrustation

Periclinal hyphae, hyaline to light brownish, 3–5 broad and had some septa with clamps

The microscopic morphology of the specimen examined in this study reveals both similarities and differences compared to other samples described in various countries (Table 2). Our sample exhibits spores that are relatively larger than those found in other individuals, although the ellipsoidal to amygdaliform shape is consistent across all specimens. Basidia sizes vary, ranging from 17 µm to 35.3 µm (Cho et al. 2016, Prydiuk 2020), with the basidia of our specimen falling within the average size range. Notably, basidia containing two spores were not observed in our sample, despite reports of bisporic and tetrasporic basidia found in this species (Prydiuk 2020). The cheilocystidia in our sample are similar in size to the structures described by Prydiuk (2020) and Akata et al. (2020), albeit smaller compared to the maximum sizes described, which can reach up to 65 µm (Gulden and Hallgrimsson 2000). Similarly, the pleurocystidia also demonstrate smaller sizes, differing from the maximum values described in literature, which can reach up to 77.2 µm (Cho et al. 2016) (Table 2).

Another notable characteristic observed in the individual under study is also evident in other specimens of the species collected in Antarctica (Garrido-Benavent et al. 2023). While individuals from other continents display pileus colours ranging from ochre to reddish-brown (Akata et al. 2020, Prydiuk 2020), G. marginata developing in Antarctica exhibits pileus colours leaning towards dark red, with rare yellow tones in its composition. These data corroborate the findings of Krah et al. (2019), who observed that mushroom assemblages in colder areas, based on the assessment of mushrooms in Europe, tend to be significantly darker. The dark colouration of G. marginata in the Antarctic Continent may play a determining role in its growth and development, as it can regulate temperature and, thus, contribute to its survival. Furthermore, pigmented fungi tolerate high UV radiation better than non-pigmented fungi due to their melanised cell wall, which serves as a radiation shield, aiding their survival in extreme conditions (Pulschen et al. 2015, Venil et al. 2020, Kreusch and Duarte 2021, Cavalcante et al. 2023).

In the phylogenetic reconstructions with G. marginata (isolate PP346498.1), a relationship within the monophyletic clade of the genus was observed and it behaved as a sister clade to other G. marginata found in gelid regions. Additionally, G. marginata showed the behaviour of a most derived clade, compared to the other internal clades of Galerina analysed. In other studies involving isolates of species collected in alpine regions of North America, close relationships were presented (Garrido-Benavent et al. 2023). For the Antarctic isolates, this grouping phenomenon is curiously repeated. However, the behaviour of isolates from the Polar Regions, which diversified relationships in this reconstruction, does not show a clearly defined internal unique clade. This suggests that the ancestry of G. marginata in this region occurred through more than one demographic expansion event during the Pleistocene. (Garrido-Benavent et al. 2023). This fact converges with our findings, as the isolate in this study, despite belonging to the marginata clade, did not form a monophyletic internal clade with the other G. marginata from Antarctica, with its branches collapsing only as sister clades.

The differences observed in the described specimens may reflect both environmental reactions and the development of functional traits to ensure the survival of these organisms in extreme regions. G. marginata exhibits a cosmopolitan distribution and further studies should be conducted to assess its bionomy and provide a comprehensive morphological description of these organisms worldwide. Searching on the Global Biodiversity Information Facility (GBIF.org 2024a) yielded 22,397 occurrences of G. marginata worldwide (Fig. 4). Amongst these, 80.30% represented human observations and 17.30% were occurrences with specimens preserved in herbaria and research institutions, totalling 17,678 georeferenced records (Fig. 4). Searches on the Barcode of Life Data System (Ratnasingham and Hebert 2007) resulted in 29 records of G. marginata worldwide, distributed across Norway, the United States and Canada (Fig. 4). Despite the significant disparity in the number of records between the systems, both indicate North America and Europe as the continents with the highest distribution of G. marginata globally.

Figure 4.  

Global distribution of Galerina marginata, based on records from the Global Biodiversity Information Facility (GBIF) and the Barcode of Life Data System (BOLD Systems).

However, it is important to consider that the distribution observed in the USA and Europe (Fig. 4) may be influenced by sampling effort and could reflect a bias in the number of reports. This suggests that regions with more active recording and research efforts might show higher occurrence numbers, potentially overlooking areas with less extensive biodiversity documentation. Therefore, it is crucial to conduct research focused on documenting new species records. Such efforts are essential for providing a more comprehensive understanding of global biodiversity, identifying regions of high conservation priority and ensuring that lesser-studied areas are not neglected. Expanding our understanding of biodiversity can facilitate a more accurate and comprehensive representation of species distributions worldwide.

Conclusion

In this study, we present the third documented occurrence of Galerina marginata in Antarctica, providing the first comprehensive morphological description of an individual of this species developing on the Antarctic Continent. Our findings contribute to the understanding of the geographic distribution and morphological variability of G. marginata, exploring its adaptations to extreme environments.

The morphological characterisation revealed both similarities and differences between the Antarctic specimen and those from other regions. While certain macroscopic characteristics, such as pileus shape, show remarkable similarity across specimens globally, variations in size and attachment of lamellae were observed. Additionally, distinctive dark colouration is observed in Antarctic specimens, which may signify an adaptation to extreme conditions, potentially assisting in temperature regulation and UV protection in the harsh polar environment. Microscopically, it differs in spore size and lacks bisporic basidia. However, fundamental traits like spore shape and basidia size remain consistent. Cheilocystidia and pleurocystidia are smaller, but still adhere to the species description.

These characteristics may be attributed to a combination of environmental and genetic factors that influence the development and morphology of fungi in the Antarctic Region. However, more comprehensive studies on the bionomics and distribution of the species on the continent are needed to corroborate these observations and better understand fungal diversity in Antarctica.

Additionally, the phylogenetic relationship observed, with Antarctic isolates forming a sister clade to other specimens from cold regions, implies a shared evolutionary history amongst cold-adapted populations of G. marginata. This relationship suggests the possibility of historical demographic events during the Pleistocene that influenced the dispersal and diversification of the species.

Thus, the data presented in this study serve as an initial foundation for subsequent monitoring of the G. marginata population in Antarctica. The analysis of the individuals described in this research enables the assessment of the potential impacts of climate change on the development and survival of these organisms in the coming years. This study not only fosters, but also points towards future research dedicated to the bionomics, phylogeny and distribution of G. marginata in Antarctica.

Acknowledgements

We would like to thank Professor Dr. Andrés Delgado Canedo for generously providing his laboratory space and equipment for molecular biology tests. To the funding support provided by the BiCIKL project, Grant No 101007492. The Marinha do Brasil for its pivotal role in providing vital logistical support for the fieldwork carried out during OPERANTAR XLI (41st Brazilian Antarctic Operation). The Brazilian Antarctic Program (PROANTAR) for its support. The Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the funding. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001.

Author contributions

FABS, JP, CFL, MFD, ELC, ALC, AFZ and CEGRS designed and conducted the study. FABS and JP conducted the fieldwork. FABS, CFL, MFD, ALC and AFZ performed the laboratory work. JP and CEGRS secured funding. FABS and ALC wrote the original draft. JP supervised the study. All authors participated in revising and editing all versions of the manuscript.

References

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