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Research Article
Two new species of Metacampanella (Agaricales, Marasmiaceae) from China and Mongolia
expand article infoWei-nan Hou‡, Burenbaatar Ganbaatar‡§|, Tolgor Bau‡
‡ Jilin Agricultural University, Changchun, China
§ Botanic Garden and Research Institute, Mongolian Academy of Sciences, Ulaanbaatar, Mongolia
| Mongolian University of Life Sciences, Ulaanbaatar, Mongolia

Corresponding author: Tolgor Bau ( junwusuo@126.com )

Academic editor: Thorsten Lumbsch
© 2024 Wei-nan Hou, Burenbaatar Ganbaatar, Tolgor Bau.
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: Hou W-n, Ganbaatar B, Bau T (2024) Two new species of Metacampanella (Agaricales, Marasmiaceae) from China and Mongolia. MycoKeys 108: 227-247. https://doi.org/10.3897/mycokeys.108.131983
Open Access

Abstract

Metacampanella is an important genus in the Marasmiaceae family. We collected specimens during our investigations in China and Mongolia. Through morphological and molecular phylogenetic analyses, we identified two new species of this genus: Metacampanella subtricolor and Metacampanella coprophila. In addition, we identified Metacampanella tricolor as a novel combination. Molecular systematic studies support these results. Illustrated descriptions, taxonomic discussions, and keys to the genus are provided.

Key words

Metacampanella, new combination, new species, phylogeny, taxonomy

Introduction

Metacampanella is a genus in the Marasmiaceae family. Initially, species of this genus were placed in Tetrapyrgos and Campanella based on their morphological characteristics (Horak 1986; Kirk 2008). Hennings (1895) established the genus Campanella based on gelatinized trama, smooth, hyaline and inamyloid basidiospores and a pileipellis showing Rameales-structure or asterostromelloid layer (Singer 1975, 1986). Horak (1987) established the genus Tetrapyrgos based on small basidiomes with a pileus rarely greater than 10 mm diameter, a central to eccentric, black to bluish black stipe arising from a basal pad, a cutis-type pileipellis of loosely interwoven, diverticulate hyphae, cystidia with an often bulbous apex and diverticulate central axis, and hyaline, inamyloid, tetrahedral basidiospores. However, the species of the two genera could not be clearly distinguished solely based on the morphology, and the taxonomic statuses of some species remain unclear. These species were temporarily placed in one of the two genera. With the development of molecular technologies and availability of sequences, Honan et al. (2015) constructed a phylogenetic tree of these two genera and found that Campanella subdendrophora was independent of Tetrapyrgos and Campanella, highlighting the issues with this classification (Komura et al. 2020). For a better distinction, Desjardin et al. (2017) re-described and provided the ITS and nrLSU sequences of important type species in these genera. Petersen and Hughes (2024) constructed a phylogenetic tree based on ITS and nrLSU fragments of Tetrapyrgos, Campanella and related taxa showing that C. subdendrophora and related taxa belonged to a third clade. Metacampanella was established to accommodate this clade. Metacampanella dendrophora (Singer) R.H. Petersen was identified as the type species of this genus. The species of this genus were characterized by basidiomata conchate, obcupulate to obsaucer-shaped, sessile, pseudostipitate or laterally stipitate, pileus surface matt; hymenophore usually of some radial rounded veins, usually developing few to numerous interveins, meandering or joining the major veins. Pileipellis were a thatch of slender hyphae and sometimes mixed with tetrapyrgoid pileocystidia, pleurocystidia fusiform, cheilocystidia missing, tetrapyrgoid or metuloid, with or without crystalline deposit. Fruiting on dead woody substrates, monocot, or uncommonly on dicot rotting wood.

At present, there are six species in this genus, Metacampanella caesia (Romagn.) R.H. Petersen, Metacampanella costaricensis R.H. Petersen, Metacampanella dendrophora (Singer) R.H. Petersen, Metacampanella olivaceonigra (E. Horak) R.H. Petersen, Metacampanella sinecystidia R.H. Petersen and Metacampanella subdendrophora (Redhead) R.H. Petersen.

Previously, our team had recorded and described the species of Campanella from the Changbai Mountain in Jilin Province, China (Bau and Liu 2010). Recently, we re-collected specimens from this series while conducting species diversity surveys in China and Mongolia. Through morphological observations and phylogenetic analyses, we identified two new species and a new combination of Metacampanella. This study aimed to conduct systematic macroscopic, microscopic, and molecular studies to provide a key to this genus.

Material and methods

Samplings and morphological analyses

Specimens for this study were collected from China and Mongolia. Specimens were deposited at the fungarium of Jilin Agricultural University (FJAU) as described in Cai et al. (2016) and Cui et al. (2018). The macroscopic description was based on fresh specimens in the field that were photographed, recorded and measured. The color description of basidiocarps was based on Kornerup and Wanscher (1978). The tissues of the specimens were treated with 5% KOH and 1% Congo red. Observations were made using a Carl Zeiss Primo Star optical microscope (Jena, Germany). The basidiospore measurements do not include the apiculus. They presented as length × width, ‘a–b × c–d’. ‘a–b’ and ‘c–d’ represents the minimum and maximum of 90% of the measured values. The main body (sterigmata or excrescences not included) of the basidia were presented as ‘e–f × g–h’. Cheilocystidia, caulocystidia, and pileipellis were measured (if present). A total of 40 mature spores were randomly selected from the specimens to measure the size and Q was the ratio of length divided by width. The description language and order refer to Petersen’s protocols when establishing the genus (Petersen and Hughes 2024).

DNA extraction, PCR amplification, and sequencing

Genomic DNA was extracted by modified CTAB method (Doyle and Doyle 1987). DNA and PCR products were detected by 1% agarose gel electrophoresis (Larsson and Örstadius 2008). ITS1F(3’-CTTGGTCATTTAGAGGAAGTAA-5’) and ITS4 (5’-TCCTCCGCTTATTGATATGC-3’) was used as primers for ITS sequences amplification and sequencing (White et al. 1990). LR0R (5’ -ACCCGCTGAACTTAAGC-3’) and LR5 (5’-ATCCTGAGGGAAACTTC-3’) was used for nrLSU sequences amplification and sequencing primers (Vilgalys and Hester 1990). The polymerase chain reaction (PCR) procedures were carried out according to the protocol described by Mou and Bau (2021). Dideoxy sequencing was completed by Shenggong Bioengineering (Shanghai) Co., Ltd.

Phylogenetic analyses

BioEdit was used to read new sequences (Alzohairy 2011), and DNAMAN (Lynnon Biosoft) was used to splice ITS and LSU sequences. New sequences were uploaded to the GenBank database National Center for Biotechnology Information (nih.gov). Sequences of related representative species in GenBank database and new sequences were selected to construct the phylogenetic tree (Table 1). Under the G-INI-I model, we used MAFFT 7.110 to align the sequence matrix https://mafft.cbrc.jp/alignment/server/. The Maximum Likelihood (ML) method used RAxML v8.2.4. The Bayesian (BI) phylogenetic tree was constructed using Phylosuite v1.2.2 (Zhang et al. 2020). Trees were displayed by FigTree v1.4.4. We referred to Petersen’s research results on species of Marasmiaceae (Petersen and Hughes 2024). 167 ITS sequences and 43 nrLSU sequences were used in the matrix of phylogenetic analysis. The length of ITS sequence matrix was 801, and the length of nrLSU sequence matrix was 1037. Maximum likelihood phylogenies were inferred using IQ-TREE under the edge-linked partition model for 10000 ultrafast bootstraps and the Shimodaira–Hasegawa-like approximate likelihood-ratio test. ModelFinder was used to select the best-fit model using AIC criterion. Best-fit model according to AIC: TPM2u+F+R3. Bayesian Inference(BI) phylogenetic tree was constructed by Phylosuite v1.2.2. ModelFinder (Kalyaanamoorthy et al. 2017). The best-fit partition model (Edge-linked) used BIC criterion. Best-fit model according to BIC: HKY+F+I+G4:ITS,HKY+F+I+G4.(Kalyaanamoorthy et al. 2017). In this study, Marasmiellus rhizomorphogenus Antonín, Ryoo & H.D. Shin was selected as the outgroup.

Table 1.
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GenBank accession number of sequences used in this study.

Taxon Country Collection GenBank No. Reference
ITS nLSU
Campanella aff. Buettneri China TENN-F-050841ss3 OQ171234 OQ171234 Petersen and Hughes 2024
C. aff. pustulata Australia QMS0008 JX444165 — —
C. alba Unknown ZMXR3 MT446108 — —
C. buettneri China WEI17–513 MW527101 — Wei et al. 2021
C. buettneri San Tome and Principe DED 8276 (SFSU) epitype MF075136 MF075138 Desjardin et al. 2017
C. buettneri China SWFU 001873 MK809426 — Guan and Zhao 2021
C. buettneri Unknown SFSU:AHH85 KT270852 — Honan et al. 2015
C. buettneri Unknown SFSU:AHH14 KT270850 — Honan et al. 2015
C. buettneri Unknown SFSU:AHH83 EF175518 — Honan et al. 2015
C. buettneri Unknown SFSU:AHH72 EF175520 — Honan et al. 2015
C. buettneri Thailand SFSU:AHH74 KT270851 — Honan et al. 2015
C. buettneri Thailand SFSU:AHH42 EF175519 — Honan et al. 2015
C. buettneri China TENN-F-051974 OQ171237 — Petersen and Hughes 2024
C. burkei São Tomé and Príncipe SFSU:BAP 632 MF100970 — Desjardin et al. 2017
C. candida Cook Islands PDD:102184 OQ282823 — —
C. keralensis India AF 342 MW462889 — —
C. pustulata Australia AQ793972 JX444168 — —
C. pustulata Australia SMF2382 JX444164 — —
C. pustulata Australia FBT2220 MW192636 —
C. simulans India AF129 MW506836 — —
C. sp. Costa Rica TENN-F-053828 OQ171240 OQ171240 Petersen and Hughes 2024
C. sp. India Strain JZ31 MG719288 — —
C. sp. India JZ44 MG719301 — —
C. sp. USA TENN-F-050996h1 OQ171235 — Petersen and Hughes 2024
C. sp. USA TENN-F-050996h2 OQ171236 — Petersen and Hughes 2024
C. sp. Guyana MCA1689 AY916670 AY916668 Aime and Phillips-Mora 2005
C. sp. USA MCA3234 MG717365 MG717352 Koch et al. 2018
C. sp. New Zealand PDD:96255 OQ282788 OQ282744 —
C. sp. New Zealand PDD:111968 OQ282827 OQ282774 —
C. sp. New Zealand PDD:112459 OQ282810 — —
C. sp. New Zealand PDD:96318 OQ282789 OQ282789 —
C. sp. Australia HO:570075 OQ282798 OQ282753 —
C. sp. Cook Islands PDD:106889 OQ282807 OQ282760 —
C. sp. Guyana MCA2235 AY916676 AY916674 Aime and Phillips-Mora 2005
C. sp. New Zealand PDD:106900 OQ282809 — —
C. sp. New Zealand PDD:106952 OQ282805 OQ282758 —
C. sp. Polynesia biocode 09–475 MZ997207 — Osmundson et al. 2022
C. tristis New Zealand JAC9980 OQ282781 OQ282741 —
C. tristis New Zealand PDD:96329 OQ282790 OQ282746 —
C. tristis New Zealand PDD:104678 OQ282826 — —
C. tristis Australia Clone Gs2A FJ857922 — Dearnaley and Bougoure 2010
C. tristis Australia Clone GS4A FJ857925 — Dearnaley and Bougoure 2010
C. tristis Australia Clone Gs3B FJ857924 — Dearnaley and Bougoure 2010
Marasmiellus candidus USA AHH157 (SFSU) EF175513 — Honan et al. 2015
Ma. candidus Canada UBC:F19683 HM240532 HM240532 —
Ma. candidus Canada UBC:F33072 MF908473 — —
Ma. candidus Canada TENN-F-052592 OQ171238 OQ171238 Petersen and Hughes 2024
Ma. candidus USA TENN-F-068189 OQ171253 OQ171253 Petersen and Hughes 2024
Ma. candidus USA TENN-F-069193 OQ171256 OQ171256 Petersen and Hughes 2024
Ma. candidus France MICH175508 MN173348 — —
Ma. candidus Unknown CBS252.39 MH856003 — Vu et al. 2019
Ma. candidus New Zealand PDD:86918 OQ282779 — —
Ma. candidus New Zealand PDD:112971 OQ282815 OQ282765 —
Ma. candidus New Zealand PDD:86983 OQ282780 OQ282740 —
Ma. candidus India KUBOT-KRMK-2020-72 MW485122 MW485123 Kantharaja and Krishnappa 2020
Ma. candidus USA BHI-F446d MF161268 — Haelewaters et al. 2018
Ma. celebanticus SPAIN TO HG2281 TYPE NR_154152 — Perez-de Gregorio et al. 2011
Ma. rhizomorphogenus USA RA705-27 MK234196 — Alanbagi et al. 2019
Metacampanella caesia Mexico Clone O7c81H GQ924042 — Herrera et al. 2010
Me. caesia USA Clone 8WE1cf02 GU910308 — Herrera et al. 2010
Me. caesia USA Clone 8WE1cf06 GU910311 — Herrera et al. 2010
Me. caesia USA Clone 8WE1cg01 GU910317 — Herrera et al. 2010
Me. caesia Kenya Isolate F41 MW995635 — Petersen and Hughes 2024
Me. caesia USA 8WE3ch07 GU910438 — Herrera et al. 2011
Me. caesia Spain T24 MH633918 — Pereira,E. et al. 2019
Me. caesia Kenya CSB F175 KU680416 — 2024
Me. caesia USA Clone 8WE1cd05 GU910299 — Herrera et al. 2010
Me. caesia USA Clone 8WE6cc07 GU910546 — Herrera et al. 2010
Me. caesia USA Clone 8WE1cg12 GU910324 — Herrera et al. 2010
Me. caesia USA Clone 8WE6ca04 GU910532 — Herrera et al. 2010
Me. caesia USA Clone 8WE6cg02 GU910572 — Herrera et al. 2010
Me. caesia USA Clone 8WE1cf11 GU910315 — Herrera et al. 2010
Me. caesia India BROP8 KU168340 — —
Me. coprophila Mongolia FJAU69316 PP973101 PP973108 This study
Me. coprophila Mongolia FJAU69317 PP973102 PP973107 This study
Me. costaricensis Costa Rica TFB9908ss13 OQ171249 OQ171249 Petersen and Hughes 2024
Me. costaricensis Costa Rica TENN-F-056536 Isotype OQ171247 OQ171247 Petersen and Hughes 2024
Me costaricensis Costa Rica TENN-F-056536ss1 OQ171248 OQ171248 Petersen and Hughes 2024
Me. dendrophora Argentina TENN-F-055003ss4 OQ171243 OQ171243 Petersen and Hughes 2024
Me. dendrophora Argentina TENN-F-055002ss11 OQ171242 OQ171242 Petersen and Hughes 2024
Me. olivaceonigra New Zealand PDD:112550 OQ282811 OQ282761 —
Me. olivaceonigra New Zealand PDD:87486 OQ282784 — —
Me. olivaceonigra Australia MEL2220682 EF175541 — Honan et al. 2015
Me. sinecystidia USA C402M KT203169 — David et al. 2016
Me. sinecystidia USA AHH120 (SFSU) EF175521 — Honan et al. 2015
Me. subdendrophora USA iNAT-99991981 ON979424 — —
Me. subdendrophora USA AHH79 (SFSU) EF175523 — Honan et al. 2015
Me. subdendrophora Canada ATCC 42449 AY445121 AY445115 Vinnere et al. 2005
Me. subdendrophora Canada ATCC 42449 NR_171206 NG_075153 Vinnere et al. 2005
Me. subdendrophora USA MushroomObserver.org/
443698		 MW433846 — —
Me. subdendrophora Mexico TENN-F-055280 OQ171244 OQ171244 Petersen and Hughes 2024
Me. subdendrophora USA TENN-F-078187 OQ171257 — Petersen and Hughes 2024
Me. subdendrophora USA DED7338 (SFSU) EF175529 — Honan et al. 2015
Me. subdendrophora USA AHH148 (SFSU) EF175522 — Honan et al. 2015
Me. subdendrophora Canada CCCM:UBC 5060-extype OQ171258 OQ171258 Petersen and Hughes 2024
Me. subdendrophora USA TENN-F-059502 OQ171251 — Petersen and Hughes 2024
Me. subtricolor China FJAU69309 PP973106 PP973112 This study
Me. subtricolor China FJAU69310 PP973105 PP973111 This study
Me. tricolor China FJAU69313 PP973104 PP973110 This study
Me. tricolor China FJAU69314 PP973103 PP973109 This study
Me. tricolor Unknown NN055704 JN943601 JN941149 Schoch et al. 2012
Me. subdendrophora USA UBC-F-33841b OQ171259 — Petersen and Hughes 2024
Root associated fungus Australia EP57 AY627833 — Bougoure and Cairney 2005
T. aff. nigripes Australia MEL:2382866 KP012740 — —
T. aff. nigripes Australia MEL:2382974 KP012833 — —
T. atrocyanea Brazil INPA259598 KT287094 — Komura et al. 2020
T. atrocyanea Brazil INPA259611 KT287095 — Komura et al. 2020
T. atrocyanea Brazil INPA259597 KT287096 — Komura et al. 2020
T. atrocyanea India KUBOT-KRMK-2020-80 MW555782 — Kantharaja and Krishnappa 2022
T. atrocyanea USA TENN-F-055739 OQ171245 — Petersen and Hughes 2024
T. atrocyanea USA FLAS-F-61224 MH211826 — —
T. atrocyanea Puerto Rico TJB7935 (SFSU) EF175544 — Honan et al. 2015
T. atrocyanea Bolivia REHalling6376 (SFSU) EF175533 — Honan et al. 2015
T. atrocyanea Costa Rica REHalling8396 (SFSU) EF175545 — Honan et al. 2015
T. atrocyanea Brazil INPA259596 KT287093 — Schoch et al. 2012
T. atrocyanea epitype Madagascar JES 216 (SFSU) NR_169666 — Desjardin et al. 2017
T. brevicystidiata Brazil DLK1065 KT287087 — Komura et al. 2020
T. brevicystidiata Brazil INPA259604 KT287088 — Komura et al. 2020
T. cerebrata Brazil INPA259594 KT287090 — Komura et al. 2020
T. cerebrata Brazil INPA259601 KT287089 — Komura et al. 2020
T. crassicystidiata Brazil INPA259607 KT287091 — Komura et al. 2020
T. crassicystidiata Brazil INPA259606 KT287092 — Komura et al. 2020
T. griseibrunnea Brazil INPA259610 KT287098 — Komura et al. 2020
T. griseibrunnea Brazil INPA259608 KT287097 — Komura et al. 2020
T. griseibrunnea Brazil INPA259609 KT287099 — Komura et al. 2020
T. nigripes Unknown TOR89 (SFSU) EF175540 — Honan et al. 2015
T. nigripes USA TENN-F-060065 DQ449941 — Lickey et al. 2003
T. nigripes USA TENN-F-060781 DQ449942 — Lickey et al. 2003
T. nigripes USA TENN-F-060065 KT270853 Honan et al. 2015
T. nigripes USA MCA6925 MG717370 MG717355 Koch et al. 2018
T. nigripes Not indicated Wong888 (SFSU) EF175535 — Honan et al. 2015
Tetrapyrgos novinigripes Brazil INPA259605 KT287082 — Komura et al. 2020
T. novinigripes Brazil INPA259603 KT287083 — Komura et al. 2020
T. parvispora Thailand AHH66 EF175536 — Honan et al. 2015
T. parvispora Thailand AHH122 (SFSU) EF175551 — Honan et al. 2015
T. parvispora Thailand AHH26 (SFSU) EF175546 — Honan et al. 2015
T. parvispora Thailand AHH27 (SFSU) EF175547 — Honan et al. 2015
T. parvispora Not indicated DED7603 (SFSU) KT270855 — Honan et al. 2015
T. similinigripes Brazil INPA259600 KT287084 — Komura et al. 2020
T. similinigripes Brazil INPA265162 KT287085 — Komura et al. 2020
T. similinigripes Brazil INPA265320 KT287086 — Komura et al. 2020
T. sp. Costa Rica TENN-F-056741 OQ171250 OQ171250 Petersen and Hughes 2024
T. sp. Brazil INPA265272 KT287100 — Komura et al. 2020
T. sp. Costa Rica REHalling7542 (SFSU) EF175531 — Honan et al. 2015
T. sp. USA TENN-F-068199 OQ171255 OQ171255 Petersen and Hughes 2024
T. sp. USA TENN-F-068191 OQ171254 OQ171254 Petersen and Hughes 2024
T. sp. Puerto Rico TJB7902 (SFSU) EF175542 — Honan et al. 2015
T. sp. Brazil DLK1970 KT287101 — Komura et al. 2020
T. sp. Costa Rica ZT12386 (SFSU) EF175543 Honan et al. 2015
T. sp. Australia TENN-F-053779 OQ171239 — Petersen and Hughes 2024
T. sp. Costa Rica TENN-F-056390 OQ171246 — Petersen and Hughes 2024
T. subcinerea Malaysia KUM60047 EF175549 — Honan et al. 2015
T. subcinerea Malaysia AHH84 (SFSU) EF175524 — Honan et al. 2015
T. subcinerea USA DED 6178 (SFSU) EF175528 — Honan et al. 2015
T. subcinerea Thailand AHH71 (SFSU) EF175534 — Honan et al. 2015
T. subcinerea Indonesia AR 019 (SFSU) EF175548 — Honan et al. 2015
T. subcinerea Malaysia KUM60047 (SFSU) EF175549 — Honan et al. 2015
T. subcinerea Thailand DED 7448 (SFSU) EF175553 — Honan et al. 2015
T. subcinerea Indonesia AR 505 (SFSU) EF175530 — Honan et al. 2015
T. subcinerea Malaysia DED 7517 (SFSU) EF175532 — Honan et al. 2015
T. subcinerea Malaysia AHH86 (SFSU) EF175537 — Honan et al. 2015
T. subcinerea Indonesia AHH115 (SFSU) EF175550 — Honan et al. 2015
T. subcinerea Indonesia AHH109 (SFSU) EF175555 — Honan et al. 2015
T. subcinerea Malaysia AHH90 (SFSU) EF175552 — Honan et al. 2015
T. subcinerea Malaysia RW832 (SFSU) EF175539 — Honan et al. 2015
T. subcinerea Malaysia KUM60051 (SFSU) EF175527 — Honan et al. 2015
T. subcinerea Indonesia AR 138 (SFSU) EF175554 — Honan et al. 2015
Uncultured Marasmiaceae clone Unknown OTU26 MH005865 — Xing et al. 2019

Results

Molecular phylogeny

The results of molecular phylogenetic analysis showed that ML and BI have the same topological structure. The ML tree was shown in Fig. 1, and the self-reported values (MLbs ≥ 80%) and posterior probability values (PP ≥ 0.8) of ML tree and BI tree were marked on each branch. This phylogenetic tree was basically consistent with the tree of previous studies by J.J.S. Oliveira (Oliveira et al. 2020), Vladimír Antonín (Antonín et al. 2023) and Ronald H. Petersen (Petersen and Hughes 2024). The proposed new species Metacampanella subtricolor T. Bau & W.N. Hou (PP = 1, MLbs = 100%) and Metacampanella coprophila Burenbaatar Ganbaatar & T. Bau (PP = 1, MLbs = 100%) were both independent branches with high support and were sister groups to each other. A related taxon, the so-called Marasmiellus tricolor (Alb. & Schwein.) Singer clustered in Metacampanella with high support (PP = 1, MLbs = 99%), so it should be treated as a member of Metacampanella.

Figure 1. 

The phylogenetic relationships of Tetrapyrgos, Campanella, and Metacampanella based on nrITS plus LSU sequences. Nodes with PP (posterior probabilities) values ≥0.9 and ML bootstrap support values ≥80% are indicated in the phylogenetic tree. Sequences newly generated in this study are highlighted in different colored fonts. This ML tree generated by RAxML v8.2.4.

Taxonomy

Metacampanella coprophila Burenbaatar Ganbaatar & T. Bau, sp. nov.

MycoBank No: 854569
Figs 2A, B, 3

Type material

Holotype. Mongolia • Dornod, Menengiin tal, 8 August 2023, 47°40'28"N, 116°50'21"E, alt. 600 m, Tolgor Bau & Burenbaatar Ganbaatar, BH34(FJAU69317).

Figure 2. 

Basidiomata A, B Metacampanella coprophila C, D Metacampanella subtricolor E, F Metacampanella tricolor. Scale bars: 5 mm.

Etymology

“coprophila” refers to the growth on dung.

Figure 3. 

Metacampanella coprophila A basidiomata B basidiospores C basidia D basidioles E cheilocystidia F pileipellis G stipitipellis. Scale bars: 1 mm (A); 5 µm (B); 15 µm (C–G).

Diagnosis

The pileus is white. The surface is frosted. The stipe is finely scaly, and the base is dark yellowish brown. Basidiospores are ellipsoid. Cheilocystidia two types: tetrapyrgoid, mostly ten pin-shaped. Caulocystidia is long clavate, irregularly curved, smooth.

Description

Pileus 2–4 mm, bell-shaped when young, then applanate, central protuberance, the surface uneven like a grid pattern after drying, edge slightly involuted, membranous. The surface of the cap is milky white, creamy or beige, rough, frosted scales, the edge complete, wavy, without stripes. The flesh is white and thin. Lamellae white to creamy, distant (L = 12–14, I = 1–2), decurrent. Stipe 4–5 × 0.5–1 mm, cylindrical, upper and lower equal thick, hollow, fibrous, milky white at the top, yellowish white to yellowish brown in the middle, dark yellowish brown, brown to dark brown at the base, and white powdery frosty fine scales on the surface.

Basidiospores 7.8–10.5 × 5–7 μm, Q = 1.5, ellipsoid, the front non-protruding, colorless, smooth, transparent, thin-walled, non-amyloid. Basidia 26–37 × 6–8 μm, clavate, 4-spored, sometimes 2-spored, thin-walled, colorless, transparent, clamp connections present at base. Basidioles 25–37 × 4–6.8 μm, rod-shaped or spindle-shaped, thin-walled. Trama hyphae of lamellae irregularity, 3.2–4.6 μm in width, with clamp connections, thick-walled. Cheilocystidia two types: a. tetrapyrgoid, colorless, transparent, thick-walled, 16–21 × 5.7–6.3 µm, clavate or fusiform, an axis beset with numerous diverticula, a swollen obovate apex, smooth, rare; b. mostly ten pin-shaped, phialide or clavate, apex bifurcated or mid-divergent, smooth. Pleurocystidia absent. Terminal cellular elements of pileipellis two types: a. diverticulate repent hypha, 21–30 × 4.7–6.3 µm, light yellow, thick-walled. b. minority tetrapyrgoid, 20–27 × 6.7–7.4 µm, thick-walled. Pileipellis composed of extremely tightly interwoven hyphae, 4–6.9 µm in width, pale yellow, transparent, thick-walled. Caulocystidia 19–30 × 4.8–8 µm, phialide or clavate, irregularly curved, yellow, thick-walled, smooth. Stipitipellis cylindrical, 4.2–5.9 µm in width, parallel, yellow, thick-walled. Trama hyphae of stipe cylindrical, 6–8 µm in width, parallel, colorless, transparent, thick-walled. Clamp connections present in all tissues.

Habitat and distribution

Summer-growing, in sheep dung. Currently only known from Mongolia.

Additional specimens examined

Mongolia • Dornod, Menengiin tal, 8 August 2023, 47°40'28"N, 116°50'20"E, Tolgor Bau, Haiying Bao and Burenbaatar Ganbaatar, B34(FJAU69316).

Notes

This species is similar to Metacampanella subtricolor in terms of morphological characteristics. However, cheilocystidia of Metacampanella coprophila is two types: a. tetrapyrgoid, b. mostly ten pin-shaped and caulocystidia only phialide or clavate. Nevertheless cheilocystidia of Metacampanella subtricolor is only tetrapyrgoid and caulocystidia two types: a. tetrapyrgoid, b. individual arboreal dermatocystidia. At the same time, the habitat of Metacampanella coprophila is special for sheep dung.

Metacampanella subtricolor T. Bau & W. N. Hou, sp. nov.

MycoBank No: 854571
Figs 2C, D, 4

Type material

Holotype. China • Inner Mongolia, Tongliao City, Daqinggou national nature reserve, 16 July 2023, 42°49′20″N, 122°15′42″E, alt. 313 m, Weinan Hou, H2307120(FJAU69309)

Figure 4. 

Metacampanella subtricolor A basidiomata B basidiospores C basidia D basidioles E cheilocystidia F pileipellis G stipitipellis. Scale bars: 1 mm (A); 5 µm (B); 15 µm (C–G).

Etymology

“subtricolor” refers that this species is similar to Metacampanella tricolor.

Diagnosis

Pileus is milky white, with furrowed edges and frosted surface. The stipe is finely scaly and black at base. Basidiospores are ellipsoid. Cheilocystidia tetrapyrgoid. Caulocystidia two types: a. tetrapyrgoid, b. individual arboreal dermatocystidia.

Description

Pileus 3–6 mm, bell-shaped to hemispherical when young, and then gradually flattened, with a slight uplift in the center and wavy edges. The surface of the cap is densely covered with white powder frost, membranous, milky white to light yellow when young, light yellowish brown to brown in the center when mature, white to light yellow on the edge, with shallow grooves, membranous. Context milky white, thin. Lamellae cream to light yellowish brown, distant (L = 10–12, I = 1–2), decurrent. Stipe 4–6 × 1–2 mm thick, cylindrical, equal thick or tapering downward. The top of the stipe milky white to light yellow brown, the middle is brown, slightly transparent, and the base dark brown to black and the surface white fine scales, fibrous, hollow.

Basidiospores 7.7–10 × 4.5–6 µm, Q = 1.7, ellipsoid, colorless, transparent, thin-walled, non-amyloid. Basidia 24–30 × 8–11 µm, clavate, 4(2)-spored, colorless, transparent, thin-walled, base with clamp connections. Basidioles 20–23 × 5–8 µm, clavate or subfusiform, thin-walled. Trama hyphae of lamellae irregularity, 3–4.9 µm in width, with clamp connections and thick-walled. Cheilocystidia tetrapyrgoid, 18–27 × 5–8 µm, cylindrical, apex with or without a swollen obovate, base irregularly branched, surface protrusions, colorless, transparent, thick-walled. Pleurocystidia absent. Terminal cellular elements of pileipellis tetrapyrgoid, 20–36 × 4–7 µm, colorless, thick-walled. Pileipellis interwoven hyphae, 3.4–5.6 µm in width, pale yellow, transparent, verrucous surface, thick-walled. Caulocystidia two types: a. tetrapyrgoid, 11–22 × 4–7 µm, pale yellow, thick-walled, cylindrical, with spherical or ellipsoid cells at the top and protrusions on the surface; b. individual arboreal dermatocystidia. Stipitipellis composed of cylindrical hyphae, 2.9–4.7 µm, parallel, yellowish brown, thick-walled. Trama hyphae of stipe composed of cylindrical hyphae, 6.2–8 µm in width, parallel, colorless, transparent, thick-walled. Clamp connections present in all tissues.

Habitat and distribution

Summer-growing, on the residues of Artemisia halodendron Turcz.ex Bess. Currently only known from northeast China.

Additional specimens examined

China • Inner Mongolia, Tongliao City, Naiman Banner, Xinglongnuma Forest Farm, 12 July 2022; 43°23′31″N, 122°12′20″E, alt. 329 m, Tolgor Bau, Fang Guo, gf2234 (FJAU67070). China • Inner Mongolia, Tongliao City, horqin left back banner, Nugustai Town, 14 July 2022, 43°23′48″N, 122°24′53″E, alt. 311 m, Tolgor Bau, Weinan Hou, H220752 (FJAU67068). China • Inner Mongolia, Daqinggou national nature reserve, 16 July 2023, 42°49′18″N, 122°15′31″E, alt. 312 m, Tolgor Bau, Weinan Hou, H2411102 (FJAU69310).

Notes

This species is similar to Metacampanella subtricolor with respect to morphological characteristics. Caulocystidia of Metacampanella subtricolor comprise two types: a. tetrapyrgoid, b. individual arboreal dermatocystidia, but caulocystidia of Metacampanella tricolor is composed of three types: a. long cylindrical or long clavate, b. U-shape, c. a few short clavate, base with irregular protrusion.

Metacampanella tricolor (Alb. & Schwein.) T. Bau & W. N. Hou, comb. nov.

MycoBank No: 854570
Figs 2E, F, 5

Agaricus tricolor Alb. & Schwein., Consp. fung. (Leipzig): 224 (1805) Basionym.

Marasmiellus tricolor (Alb. & Schwein.) Singer, Pap. Mich. Acad. Sci. 32: 128 (1948)[1946] Synonym.

Type material

Holotype. China • Inner Mongolia, Tongliao City, horqin left back banner, Udantara Forest Farm, 15 July 2023, 43°1′17″N, 122°44′47″E, alt. 345 m, Weinan Hou, H230754(FJAU69314).

Figure 5. 

Metacampanella tricolor A basidiomata B basidiospores C basidia D basidioles E cheilocystidia F pileipellis G stipitipellis. Scale bars: 2 mm (A); 5 µm (B); 15 µm (C–G).

Description

Pileus 4–10 mm, convex when young, applanate after maturity, slightly concave at the center, and shallow grooves on the edge. The surface of the pileus white, creamy, center light yellow, with pink tone, rough, white powder frosty fine scale, membranous. Context white, thin. Lamellae rice white to cream color, distant(L = 8–10, I = 1–2), decurrent. Stipe 6–24 × 1–2 mm, cylindrical, slightly thinner at the base, white at the top of the stipe, light yellow in the middle, brown to grayish brown at the base, densely white fine scale on the surface, fibrous, hollow.

Basidiospores 8.6–11.8 × 4.8–6.3 µm, Q = 1.9, long ellipsoid, not protuberant on the front, slightly sharp at base, colorless, transparent, thin-walled, non-amyloid. Basidia 22–32 × 7.4–11 µm, clavate, 4(2)-spored, colorless, transparent, thin-walled, base with clamp connections. Basidioles 20–30 × 5–10 µm, clavate or subfusiform, thin-walled. Trama hyphae of lamellae irregularity, 3.8–5.7 µm in width, with clamp connections, thick-walled. Cheilocystidia tetrapyrgoid, 18–27 × 5–8 µm, the main body cylindrical, irregular protrusion on the surface. Pleurocystidia absent. Terminal cellular elements of pileipellis two types: a. tetrapyrgoid, 30–47 × 6–12 µm; b. long cylindrical or long clavate, verrucous base, colorless, 37–49 × 4.4–6 µm, thick-walled. Caulocystidia three types: a. long cylindrical or long clavate, thick-walled, smooth, 23–59 × 3.7–6.6 µm; b. U-shaped, smooth, 16–28 × 3.3–6.7 µm; c. a few short clavate, base with irregular protrusion, 16–29 × 3–6.8 µm. Stipitipellis composed of cylindrical hyphae, 3.3–5.6 µm in width, parallel, pale yellow, thick-walled. Stipitipellis composed of cylindrical hyphae, 4–6 µm in width, parallel, colorless, transparent, thick-walled. Trama hyphae of stipe composed of cylindrical hyphae, 3.3–5.6 µm in width, parallel, transparent, colorless, thick-walled. Clamp connections present in all tissues.

Habitat and distribution

Summer-growing, on the residues of herbaceous plants. Known from south, northwest and northeast China.

Additional specimens examined

China • Inner Mongolia, Tongliao City, Liaohe Park, 19 July 2023, 43°39′10″N, 122°16′57″E, alt. 179 m, Tolgor Bau and Weinan Hou, H2307216(FJAU69318). China • Inner Mongolia, Tongliao City, horqin left back banner, Udantara Forest Farm, 15 July 2023, 43°1′17″N, 122°44′47″E, alt. 345 m, Weinan Hou, H230759(FJAU69313). China • Heilongjian, Yichun City, Beishan Park, 25 July 2023, 47°44′13″N, 128°53′18″E, alt. 318 m, Weinan Hou, H2307334(FJAU69315). China • Liaoning, Zhuanghe City, Xishan Park, 6 July 2024, 39°37′51″N, 121°59′51″E, alt. 70 m, Weinan Hou, H2470619(FJAU69319). China • Liaoning, Dalian City, Heping Park, 9 July 2024, 38°47′22″N, 121°8′57″E, Hong Cheng, C24070901(FJAU69320).

Notes

Because the macroscopic morphological characteristics of Metacampanella tricolor are very close to species of Marasmiellus, Singer classified this species into Marasmiellus in the early stage (Singer 1948). However, now it was observed that the microstructure characteristics of pileipellis and cheilocystidia were more in line with the definition of Metacampanella (Petersen and Hughes 2024).

Key to the species of Metacampanella

1 hymenophore usually of some radial rounded veins, usually developing few to numerous interveins, meandering or joining the major veins 2
– hymenophore lamellae, none radial rounded vein 8
2 sessile, pseudostipitate, laterally stipitate (<1 mm 3
– well-developed stipe(≥1 mm 6
3 surface of pileus gelatinous Me. dendrophora
– surface of pileus non-gelatinous 4
4 basidiospores triangular or round triangular, with abaxial bulg-e Me. subdendrophora
– basidiospores ellipsoid, without abaxial bulge 5
5 cheilocystidia missing Me. caesia
– cheilocystidia ten pin-shaped, tetrapyrgoid or gymnopoi-d Me. dendrophora f. washingtonensis
6 surface of pileus uniform dark green, not white Me. costaricensis
– surface of pileus white, with suffused greenish 7
7 pileipellis hyphae Rameales-structure Me. sinecystidia
– pileipellis hyphae not Rameales-structure Me. olivaceonigra
8 grow in sheep dung Me. coprophila
– grow on branches of trees or dead grass 9
9 Caulocystidia three types: a. long cylindrical or long clavate, b. U-shaped, c. a few short clavate, base with irregular protrusion Me. tricolor
– Caulocystidia two types: a. tetrapyrgoid b. individual arboreal dermatocystidi-a Me. subtricolor

Discussion

Peterson’s phylogenetic framework combined with sample sequences from China and Mongolia was used to reconstruct a phylogenetic tree based on the ITS and nrLSU datasets. The new species, i.e., Metacampanella coprophila, identified in this study formed an independent evolutionary branch in the phylogenetic tree and a sister group with Metacampanella subtricolor. However, there are some differences in their habitats. The former was isolated from sheep dung and the latter from herbaceous plant residues. Metacampanella tricolor was originally placed in Marasmiellus (Singer 1948). In the present study, morphological observations and phylogenetic analysis showed that this species belongs to the genus Metacampanella, with high phylogenetic support - (PP = 0.99, MLbs = 97%). It is a sister group of Metacampanella subtricolor and Metacampanella coprophila. This species was widely distributed in Asia, and also distributed in south, northwest and northeast China (Song et al. 2009; Luo 2021).

In the phylogenetic tree of this study, there were two major branches Clade A and Clade B. The main difference between these clades was that the hymenia of Clade A had some radial rounded veins, and the hymenia of Clade B had real lamellae. Our samples belonged to Clade B, which was located at the base of Metacampanella. Their stipe length was ≥ 1 mm, which was similar to Me. costaricensis, Me. olivaceonigra, and Me. sinecystidia in Clade A. Basidiospores were ellipsoid, with no protuberant on the front, similar to Me. caesia in Clade A. In addition, the recognition characteristics of basidiospore ellipsoid in this branch species were also similar to Campanella. The basidiophore was umbellate, the pileus was convex, not conchate or obcupulate-to-obsaucer in shape, and the hymenium was lamellar. These characteristics are similar to those of Tetrapyrgos. However, the basidiospores of Tetrapyrgos were quadrilateral, and the species in Clade B did not meet the definition of Tetrapyrgos. In addition, we speculate that the differentiation of the basidiospore morphology of these genera occurred earlier than that of other characteristics. Clade B reflects the different genetic characteristics of these genera and plays a vital role in the classification of these species. This provides key clues for determining the species boundary of Metacampanella and Tetrapyrgos, and the multilineage problem of Campanella.

The original identifying characteristics of Metacampanella have changed, because Clade B has broadened and increased the species range of Metacampanella. We attempted to supplement and revise the definition of species characteristics in Metacampanella. After revision, the characteristics of the genus were basidiophore conchate or obcupulate to obsaucer-shaped or umbellate, white to suffused greenish or yellowish (rarely pale pink), membrane, sometimes gelatinous, hymenium some radial rounded veins or lamellae, sessile, pseudostipitate, laterally stipitate or well-developed stipe, finely scales on the surface, necropigment at the base, basidiospores generally triangular, round triangular or ellipsoid, sometimes with or without abaxial bulge, cheilocystidia missing, ten pin-shaped, tetrapyrgoid, gymnopoid or metuloid, with or without crystalline deposit, pileipellis a thatch of slender hyphae, often encrusted with annular thickenings, pileocystidia tetrapyrgoid, long cylindric or missing, caulocystidia long cylindrical or long clavate, U-shaped, short clavate with irregular protrusion at base, tetrapyrgoid, individual arboreal dermatocystidia. Growing on dead woody substrates, dead grass, a few on dung.

This study provides specimens and their corresponding sequences from three species of Metacampanella from China and Mongolia. Because we only referred to the results of the species at the time of establishment of the genus, we did not modify the level of the subgenus. We have only provided key information and compiled a key for the species of this genus.

Acknowledgments

We are grateful for the useful tools (BioEdit, DNAMAN, MAFFT, RAxML, Phylosuite, FigTree) used in this study. We extend our thanks to Liang-peng Sun, Han-bing Song, Li-yang Zhu, Hong Cheng and Xianyan Zhou for their kinds of help in studies. We would also like to thank Engineering Research Center of Edible and Medicinal Fungi (Ministry of Education, Jilin Agricultural University, China) for their support throughout the project.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

Key Laboratory of Edible Fungal Resources and Utilization (North), Ministry of Agriculture and Rural Affairs, Jilin Agricultural University, Changchun 130118, China.

Author contributions

All authors have contributed equally.

Author ORCIDs

Wei-nan Hou https://orcid.org/0000-0002-9838-3489

Burenbaatar Ganbaatar https://orcid.org/0000-0003-0720-2441

Tolgor Bau https://orcid.org/0000-0003-2461-9345

Data availability

All of the data that support the findings of this study are available in the main text.

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