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Research Article
Four new species of Tremella (Tremellales, Basidiomycota) based on morphology and DNA sequence data
expand article infoYing Zhao, Xin-zhan Liu§, Feng-yan Bai§
‡ 1 State Key Laboratory for Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, PR China 2 Key Laboratory of Microbiology Diversity Research and Application of Hebei Province, College of Life Sciences, Hebei University, Baoding 071002, PR China, Beijing, China
§ 1 State Key Laboratory for Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, PR China, Beijing, China
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Abstract

In the present study, a total of 33 Tremella specimens in China were collected and examined using molecular phylogenetic analysis based on a combined sequence dataset of the nuc rDNA internal transcribed spacer (ITS) region and nuc 28S rDNA D1/D2 domain in conjunction with the morphological characters. Four new species, namely Tremella basidiomaticola, T. cheejenii, T. erythrina, and T. salmonea, are newly described based on their distinct phylogenetic relationships and the comparison of morphological characters with known Tremella species. Our results indicate a high species diversity of Tremella waiting to be discovered.

Keywords

Basidiomycota , morphology, phylogeny, taxonomy, Tremella

Introduction

Tremella Pers. has been traditionally considered to be the largest and most polyphyletic genus in Tremellaceae (Fell et al. 2000; Scorzetti et al. 2002; Sampaio et al. 2004; Boekhout et al. 2011; Millanes et al. 2011; Weiss et al. 2014; Liu et al. 2015a). The members of Tremella sensu lato are dimorphic fungi that contain both a haploid unicellular yeast stage and a dikaryotic filamentous stage. This genus is characterized by its mycoparasitic lifestyle and comprises species growing on the hymenium of Corticiales, Polyporales, Rhytismatales, and Russulales, on the mycelium of Russulales such as Peniophora and Stereum, in the basidiomata of Dacrymycetales, Polyporales, Russulales, and Trechisporales, on the perithecia of Diaporthales, Pleosporales, and Xylariales, as well as on lichens (Bandoni 1961; Reid 1970; Brough 1974; Zugmaier et al. 1994; Bandoni 1995; Roberts 1995, 1999, 2001, 2007; Roberts and deMeijer 1997; Diederich 1996; Torkelsen 1997; Chen 1998; Hauerslev 1999; Van Ryckegem et al. 2002; Pippola and Kotiranta 2008; Zamora 2009).

Tremella sensu lato includes approximately 90 species, more than half of which are known to exclusively parasitize specific lichenized fungal hosts (Diederich and Marson 1988; Diederich and Christiansen 1994; Diederich 1996, 2003, 2007, Sérusiaux et al. 2003; Kirk et al. 2008; Zamora 2009, Zamora et al. 2011, 2016; Millanes et al. 2012, 2014, 2015, 2016; Diederich et al. 2014; Kout et al. 2015; Lindgren et al. 2015; Westberg et al. 2015; Spirin et al. 2017). This genus splits into eight monophyletic groups in combination with several isolated species in Tremellales. Four clades have been emended, namely Tremella sensu stricto, Carcinomyces, Naematelia, and Phaeotremella, and one proposed as new genus, namely Pseudotremella. The other three clades consist of lichenicolous species that were defined as Tremella clade I, II, and III (Millanes et al. 2011; Liu et al. 2015a, b). Their taxonomy remains be determined until more robust phylogeny is resolved and further morphological characters are found. The basidiomata colour and shape of species belonging to Tremella s. l. are generally variable between different clades. Non-lichenicolous species mainly exhibit jelly-like basidiomata with cerebriform, folise, lobe, or pulvinate macromorphology and white, yellow, orange, or brown colour. In addition, some species are intrahymenial parasites that occur within the hymenia of dacrymycetaceous or corticoid species. Their basidiomata are not macroscopically visible. Lichenicolous species usually produce inconspicuous gall deformations on the thallus of lichens, at least in early stages of growth, where as some species can induce the formation of large galls up to 15 mm in diameter (Diederich 1996, 2007). Some species can produce gelatinous basidiomata instead of gall formation (Diederich 1996; Lindgren et al. 2015; Millanes et al. 2015; Zamora et al. 2017). Moreover, some species grow intrahymenially without any external symptoms (Diederich 1996, 2007). Compared to the increasing knowledge of the diversity of lichenicolous species, few studies of non-lichenicolous Tremella species are published in recent years.

Tremella s. s. is now confined to Fuciformis and Mesenterica subclades containing more than 30 species. Basidiomata of some Tremella s. s. species have long been used as food or traditional medicine in China or other Asian countries. Tremella fuciformis and T. aurantialba have been cultivated in China for more than 30 years. The diversity and distribution of Tremella are poorly known in China, as comparatively few mycologists focus on these fungi (Peng 1982; Bandoni and Zang 1990). In the present study, four new species are described and characterised based on morphological characters and phylogenetic analyses of nuc rDNA ITS region and nuc 28S rDNA D1/D2 domain.

Materials and methods

Sampling and morphological examination

Specimens were collected from Guangdong, Guangxi, Heilongjiang, Jilin, Qinghai, Tibet, and Yunnan provinces in China. The specimens were air dried immediately after their collection. Macromorphological descriptions were based on field observations. Micromorphological examination followed the studies by Chen (1998) and Millanes et al. (2014). Microscopic structures, features, and measurements were observed using handmade sections stained with 1% Phloxin after pretreatment with 5% KOH and photographed with Zeiss AXIO Imager A2 coupled to an AxioCam MRc5 digital camera. Basidiospores and conidia measurements are present as follows: length range × width range, L = mean spore length (arithmetic average of all spores), W = mean spore width (arithmetic average of all spores), Q = variation in the L/W ratios and n = number of spores measured. All specimens were preserved in the XZL culture collection (personal culture collection of Xin-zhan Liu housed in the Institute of Microbiology, Chinese Academy of Sciences). Type specimens were deposited in Mycological Herbarium of the Institute of Microbiology, Chinese Academy of Sciences, Beijing, China (HMAS). The cultures were deposited in China General Microbiological Culture Collection Center (CGMCC) and the CBS yeast collection of the Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands.

DNA extraction, PCR amplification and sequencing

DNA was extracted directly from the specimens examined. A very small amount of dry tissue was soaked in sterile water for 30 min and dried with sterile filter papers. The tissue was taken into 2 ml eppendorf tube with quartz sand (1–2 mm), lyophilized using liquid nitrogen and immediately crushed with tissue grinder for 2 min using SCIENTZ-48 at 70 Hz (SCIENTZ, China). The sample was homogenized in 1 ml 5% CTAB preheated at 65 °C. The mixture was warmed up at 65 °C for 1 h and centrifuged by 15000 rpm for 15 min. The supernatant was purified with phenol:chloroform:isoamyl alcohol (25:24:1) for twice of which the second purification step without phenol. The supernatant was incubated for 30 min at 37 °C with 25 μl RNAase (20 mg/ml) and then purified again. The precipitation with 3 M sodium acetate and ethyl alcohol absolute was conducted. Finally, the DNA was washed twice with 70% (w/v) ethanol and then dissolved in 50 μl of pure water. The nuc rDNA ITS region and D1/D2 domain of nuc 28S rDNA were amplified using the protocols described previously (Liu et al. 2015a). PCR products were observed on 1% Agarose gel electrophoresis stained with ethidium bromide. Purification and sequencing of PCR products were carried out at TSINGKE Biological Technology, Beijing, China.

Phylogenetic analyses

Phylogenetic analyses were performed as described previously with modification (Millanes et al. 2011; Liu et al. 2015a, b). Vishniacozyma carnescens CBS 973T was chosen as outgroup because the genera Vishniacozyma is the sister group of Tremellaceae (Liu et al. 2015a, b). Four partitions, i.e., ITS1, 5.8S, ITS2 and D1/D2 domain, were chosen as the appropriate scheme (Millanes et al. 2011; Zamora et al. 2017). Multiple sequences were aligned using MAFFT algorithm and the G-INS-I option (Standley 2013). Major insertions and ambiguous regions were identified and eliminated with Gblocks version 0.91b (Castresana 2000) using a relaxed selection (minimum number of sequences for a conserved position = 36, minimum number of sequences for a flank position = 60, maximum number of contiguous non-conserved positions = 10, minimum length of a block = 5 and allowed gap positions = ‘with half’), following Talavera and Castresana (2007). PartitionFinder V2.1.1 (Lanfear et al. 2017) was used to determine the best-fit evolutionary model for each partition, with the following settings: the ‘all’ search algorithm, the corrected Akaike Information Criterion (AICc) for model selection and either the ‘raxml’ or ‘mrbayes’ set of models.

Dataset congruence was assessed manually by analyzing the datasets separately by maximum likelihood bootstrapping. Conflict among clades was considered significant if a significantly supported clade (bootstrap support ≥ 70%; Hillis and Bull 1993) for one marker was contradicted with significantly supported by another. Incongruence was found between topologies derived from ITS1, 5.8S, ITS2, and D1/D2 domain.

Maximum likelihood (ML) analyses of single gene were performed in RAxML-HPC V.8 (Stamatakis 2014) on the CIPRES Science Gateway (Miller et al. 2010). The GTR+G, GTR+G, GTR+I+G and GTR+I+G models were applied to each partition. The best-scoring tree was obtained using rapid bootstrap analysis by running 1000 replicates. Four single-gene trees estimated above were then used as input to infer the species tree with the coalescent-based approach implemented in the ASTRAL program v5.6.3 (Mirarab and Warnow 2015). The bootstrapping option of ASTRAL was used for 1000 replicates.

Bayesian analyses were conducted by Markov Chain Monte Carlo (MCMC) sampling for combined nucleotide sequences using MRBAYES 3.2.2 (Ronquist et al. 2012) on the CIPRES Science Gateway (Miller et al. 2010). Likelihood models were selected for each of the four gene partitions among the 24 models implemented in MrBayes. A HKY+I+G model was selected for the ITS1, a K80+G model was selected for the 5.8S, a SYM+I+G was selected for the ITS2 and a GTR+I+G model was selected for D1/D2 domain. Two independent runs were executed, each with four chains, three of which were incrementally heated. The analysis was conducted for 5 million generations with trees sampled every 5000 generations. The first 25% trees, which represent the burn-in phase of the analysis, were discarded after checking for stability on the log-likelihood curves and the split-frequencies of the runs in Tracer v.1.7 (Rambaut et al. 2018). The remaining trees were used for calculating posterior probabilities (PP) in the majority rule consensus tree.

Branches that received bootstrap values (BP) for Maximum likelihood and Bayesian posterior probabilities (BPP) greater than or equal to 50% (BP) and 0.95 (BPP) were considered as significantly supported. The GenBank accession numbers for the sequences of the ITS region and D1/D2 domain used in this study are listed in Table 1.

Table 1.

Sequences used in molecular phylogentic analysis. Entries in bold are newly generated for this study.

Species Strain number Voucher number Country ITS D1D2
Tremella basidiomaticola CGMCC 2.5724T China, Fujian MH712820 MH712784
CGMCC 2.5725 China, Fujian MH712821 MH712785
CBS 8225 China, Fujian MH712822 MH712786
Tremella brasiliensis CBS 6966R Costa Rica AF444429 AF189864
CBS 8231 Costa Rica JN053465 JN043570
Tremella cerebriformis LE 296436 Russia KP986538 /
LE 303455 Russia KP986522 /
VLA M-11693 Russia KP986538 /
Tremella cerebriformis ZRL20170101 China, Heilongjiang MH712823 MH712787
ZRL20170269 China, Heilongjiang MH712824 MH712788
Tremella cheejenii GX20172598 China, Guangxi MH712825 MH712789
GX20172640 China, Guangxi MH712826 MH712790
Tremella dysenterica LE 303447 Russia KP986509 KP986542
VLA M-18599 Russia KP986531 /
Tremella erythrina GX20170141 (HMAS 255317) China, Guangxi MH712827 MH712791
GX20170916001 (HMAS 279591) China, Guangxi MH712828 MH712792
Tremella fibulifera LE 303445 Russia KP986518 KP986547
Tremella fibulifera GX20172028 China, Guangxi MH712829 MH712793
HMAS 52852 China, Tibet MH712830 MH712794
Tremella flava CBS 8471R Taiwan KY105681 KY105681
CCJ 907 Taiwan AF042221 AF042403
CCJ 928 Taiwan AF042223 AF042405
Tremella flava ZRL20180289 China, Yunnan MH712834 MH712798
ZRL20180156 China, Yunnan MH712835 MH712799
KM20170128 China, Yunnan MH712836 MH712800
YN135 China, Yunnan MH712837 MH712801
ZRL20180167 China, Yunnan MH712838 MH712802
ZRL20180164 China, Yunnan MH712839 MH712803
ZRL20180166 China, Yunnan MH712840 MH712804
ZRL20180348 China, Yunnan MH712841 MH712805
ZRL20180349 China, Yunnan MH712842 MH712806
23 China, Yunnan MH712843 MH712807
24 China, Yunnan MH712844 MH712808
YN177 China, Yunnan MH712845 MH712809
YN180 China, Yunnan MH712846 MH712810
Tremella fuciformis CBS 6970R Taiwan KY105683 AF075476
CCJ 1072 Taiwan AF042227 AF042409
CCJ 1531 Taiwan AF042254 AF042436
Tremella fuciformis GX20170212 China, Guangxi MH712831 MH712795
GX20172644 China, Guangxi MH712832 MH712796
HMAS 0274334 China, Tibet MH712833 MH712797
Tremella fuciformis CBS 6971 USA KY105682 KY109896
Tremella globispora CBS 6972R Canada AF444432 AF189869
UBC 586 Canada AF042425 AF042243
Tremella laurisilvae Koschatzky s.n. Portugal JN053467 JN043572
Tremella lloydiae-candidae VLA M-11702 Russia KP986536 KP986559
VLA M-11703 Russia KP986537 KP986560
Tremella mesenterica CBS 6973R Canada AF444433 AF075518
Ryman 9146 Sweden JN053463 JN043568
CCJ 1040 Taiwan AF042408 AF042226
FO 24610 German AF042447 AF042265
Tremella mesenterica HMAS 270832 China, Guangdong MH712847 MH712811
HMAS 88438 China, Jilin MH712848 MH712812
HMAS 96841 China, Qinghai MH712849 MH712813
GX20170708 China, Guangxi MH712850 MH712814
Tremella resupinata CCJ 1458 Taiwan AF042421 AF042239
Tremella salmonea GX20172637 China, Guangxi MH712851 MH712815
Tremella samoensis LE 262897 Russia KP986511 /
VLA M-18603 Russia KP986532 KP986555
Tremella samoensis GX20172371 China, Guangxi MH712852 MH712816
GX20170536 China, Guangxi MH712853 MH712817
Tremella taiwanensis CCJ 1151 Taiwan AF042412 AF042230
CCJ 1153 Taiwan AF042413 AF042231
Tremella taiwanensis GX20170625 China, Guangxi MH712854 MH712818
GX20170629 China, Guangxi MH712855 MH712819
Tremella tropica CBS 8483R Taiwan KY105697 KY109908
CBS 8486 Taiwan KY105697 KY109909
CCJ 1355 Taiwan AF042433 AF042251
Tremella yokohamensis JCM 16989T Japan HM222926 HM222927
VLA M-11700 Russia KP986529 /
Outgroup
Cryptococcus depauperatus CBS 7841T FJ534881 FJ534911

Results

Phylogenetic analyses

The combined dataset consisted of ITS1 region (44 bp), 5.8S region (156 bp), ITS2 region (168 bp), and D1/D2 domain (532 bp) (a total of 900 bp) for 57 specimens and 13 strains in genus Tremella with Vishniacozyma carnescens CBS 973T as the outgroup. Two methods for phylogenetic tree construction resulted in a similar topology. Therefore, only the best scoring RAxML tree is shown with BP and BPP values simultaneously in Figure 1. All the Tremella specimens and strains in this study separated into 19 clades, representing 15 known and four new species. The four new species clustered into distinct clades supported with high bootstrap values.

Figure 1. 

The maximum likelihood tree of the novel species and related taxa in Tremella sensu stricto based on the combined sequences of the nuc rDNA ITS region and nuc 28S rDNA D1/D2 domain. Bootstrap supports (BP) (> 50%) of maximum likelihood method and Bayesian posterior probability (BPP) values (> 0.9) are shown at each node. Note: ns, not supported (BP < 50% or PP < 0.9); nm, not monophyletic.

Taxonomy

Tremella basidiomaticola X.Z. Liu & F.Y. Bai, sp. nov.

MycoBank No: MycoBank: MB827184
Figure 2

Type

CHINA, Fujian Province, Ningde city, Gutian county, on the basidioma of Tremella fuciformis, July 2017, X.Z. Liu (holotype strain: CGMCC 2.5724T, ex-holotype strain: CBS 15261T).

Etymology

Basidiomaticola refers to the species isolated from the basidioma of T. fuciformis.

Description

Asexual morph: colonies yellowish, smooth, shiny, and slimy, with an entire margin. Pseudohyphae and hyphae are not formed on corn meal agar. Conidia hyaline, smooth, globose to subglobose, 3.0–6.0 × 2.5–5.0 μm, L = 4.8 ± 0.9 μm, W = 3.9 ± 0.8 μm, Q = 1.0–1.7 (n = 30). Ballistoconidia, globose to subglobose on CMA agar, 5.0–7.0 × 3.5–6.0 μm, L = 6.0 ± 0.6 μm, W = 5.1 ± 0. 6 μm (n = 30). The comparison of physiological properties between this new species and its related taxa were listed in Suppl. material 1. Sexual morph: undetermined.

Figure 2. 

Tremella basidiomaticolaCGMCC 2.5724TA Vegetative cells grown in YM agar for 7 days at 17 °C B Ballistoconidia produced on CMA agar for 7 days at 17 °C. Scale bars: 5 μm.

Additional isolate examined

CHINA, Fujian Province, on the basidioma of Tremella fuciformis, July 2017, X.Z. Liu, CGMCC 2.5725 = CBS 15262; Japan, isolated from Mori Ind. Co., Ltd, 1968, T. Suda, NBRC 8990 = CBS 8225.

Notes

Three strains representing T. basidiomaticola clustered in a well-supported clade that closely related to T. yokohamensis, T. flava, and T. fuciformis. Tremella basidiomaticolaCGMCC 2.5724T differed from T. yokohamensis, T. flava, and T. fuciformis by 97.4%, 94.4%–95.1%, and 97.8%–98.1% sequence identities in D1/D2 domain and 96.3%–96.6%, 94.4%–95.7%, and 96.6%–97.5% sequence identities in ITS region. Physiologically, the ability to assimilate lactose, melibiose, raffinose, inulin, soluble starch, L-rhamnose, ethanol, glycerol, DL-lactic acid, and inositol were different between T. basidiomaticola and closely related taxa (Suppl. material 1: Table S1). Moreover, the novel species can grow in vitamin-free medium but not for its sister species.

Tremella cheejenii X.Z. Liu & F.Y. Bai, sp. nov.

MycoBank No: MycoBank: MB827187
Figures 3, 4

Type

CHINA. Guangxi Province, Hechi city, Luocheng county, Pingying village, Jiuwan Mountain National Nature Reserve, 108°48'E, 25°19'N, G.J. Li, H.S. Ma, Z.L. Lin & M.Z. Zhang, 7 August 2017, GX20172598 (HMAS 279589).

Etymology

Cheejenii was named in honor of Chee-Jen Chen for his contributions to systematics of tremellalean fungi.

Description

Basidiomata sessile, cerebriform, up to 1.0–3.0 cm in diameter, broadly attached to substratum, soft gelatinous, pale white when fresh and pale brown in dry condition. Hyphae smooth, thick-walled, slender, 2.0–4.5 μm in diameter, often anastomosing, clamp connections abundant, loop-like forming a large hollow. Haustoria rare, small, subglobose, ca 2.0 μm in diameter, with a single hypha. Hyphidia abundant, smooth, thin-walled, 2.5–4.0 μm in diameter, branched, hyphidia and basidia derived from the same hypha. Probasidial initials subglobose, ovoid or pyriform. Mature basidia subglobose, broadly ellipsoid or ovoid, mostly two-celled, and occasionally four-celled, with apical protuberance, often longitudinally septate or occasionally oblique or cruciate-septate, thin-walled, 12.0–17.0 μm × 13.0–18.0 μm, stalked, 2.0–4.0 μm long, with sterigmata up to 70 μm, not swollen at apex. Basidiospores hyaline, smooth, thin-walled, subglobose to broadly ellipsoid, apiculate, 5.0–10.0 μm × 4.5–8.0 μm, L = 8.6 ± 1.1 μm, W = 6.6 ± 0.8 μm, Q = 1.1–1.8 (n = 40). Basidiospores forming secondary ballistoconidia by the formation of a sterigma. Conidia ellipsoid, smooth, hyaline, thin-walled, 2.2–4.0 μm × 1.8–3.0 μm, L = 3.1 ± 0.6 μm, W = 2.2 ± 0.3 μm, Q = 1.0–2.0 (n = 40), monokaryotic, budding from apex of sterigmata.

Figure 3. 

Macromorphology of Tremella basidiomata. A T. cheejenii B T. erythrina C T. salmonea. Scale bars: 1 cm.

Figure 4. 

Microscopic structure of Tremella cheejenii (HMAS 279589). A Section through hymenium B Hyphidia from context C Hyphae from context D Probasidia E–H Mature basidia I Mature basidia and conidia produced from the sterigmata J–K Basidiospres and its germination with short sterigma. Scale bars: 10 μm (A–D), 5 μm (E–J).

Habitat

On wood of deciduous tree, in forest dominated by Fagaceae, Lauraceae, Theaceae, Magnoliaceae, and Hamamelidaceae.

Additional specimens examined

CHINA. Guangxi Province, Hechi city, Luocheng county, Pingying village, Jiuwan Mountain National Nature Reserve, 108°48'E, 25°19'N, G.J. Li, H.S. Ma, Z.L. Lin & M.Z. Zhang, 7 August 2017, GX20172640 (HMAS 279590).

Notes

Two specimens form the sister group to T. fibulifera, T. lloydiae-candidae, and T. resupinata and represent a new species, T. cheejenii. The sequence identities between T. cheejenii and T. fibulifera are 95.7%–95.9% and 92.5%–93.2% in the D1/D2 domain and ITS region, respectively. Similarly, T. cheejenii and T. lloydiae-candidae showed 96.1%–96.2% and 92.1% sequence identities in the D1/D2 domain and ITS region, respectively. Tremella cheejenii and T. resupinata showed 90.4% and 89.9% sequence identities in the D1/D2 domain and ITS region, respectively. Tremella cheejenii is distinct from T. fibulifera in its bigger basidia (12.0–17.0 μm × 13.0–18.0 μm in T. cheejenii vs 14–16 μm × 10–13 μm in T. fibulifera). However, the basidia of T. cheejenii are smaller than that of T. resupinata (12.0–17.0 μm × 13.0–18.0 μm in T. cheejenii vs 27.0–40.0 μm × 22.0–31.0 μm in T. resupinata) (Chen 1998; Malysheva et al. 2015). Moreover, conidia are produced from the sterigmata in T. cheejenii compared to the absence of conidia in T. fibulifera, T. lloydiae-candidae, and T. resupinata.

Tremella erythrina X.Z. Liu & F.Y. Bai, sp. nov.

MycoBank No: MycoBank: MB827186
Figures 3, 5

Type

CHINA. Guangxi Province, Chongzuo city, Longzhou county, Qiang village, Nonggang National Nature Reserve, 106°54'E, 22°27'N, R.L. Zhao, M.Q. He, G.F. Mou, J.L. Qin, H.J. Wang & X.Y. Zhu, 30 July 2017, GX20170141 (HMAS 255317).

Etymology

Erythrina refers to the colour of the basidioma.

Description

Basidiomata sessile, cerebriform to foliose, with undulate broad lobes, lobes hollow, firm gelatinous, up to 1.3–1.8 cm in diameter, broadly attached to substrate, red and brownish orange when fresh and brownish orange when dry. Hyphae smooth, thin- or thick-walled, slender, hyaline, 1.0–3.0 μm, with clamp connections, branched with frequent anastomoses. Haustoria rare, small, subglobose, 1.5–2.0 μm in diameter, with single hyphae. Hyphidia present, smooth, thin-walled, 2.0–4.0 μm, branched. Probasidia mostly broadly ellipsoid. Mature basidia, globose to subglobose or broadly ellipsoid to ovoid, 12.0–18.0 μm × 13.0–19.0 μm, mostly four-celled, occasionally two-celled, without stalks, frenquently longitudianllly cruciate-septate. Basidiospores, smooth, thin-walled, ellipsoid to ovoid, apiculate, 7.0–10.0 μm × 5.0–7.0 μm, L = 8.2 ± 0.8 μm, W = 6.1 ± 0.6 μm, Q = 1.1–1.7 (n = 40).

Figure 5. 

Microscopic structure of Tremella erythrina (HMAS 255317). A Section through hymenium B Hyphae from context C Hyphidia with basidia of different developmental stages D–H Mature basidia I–K Basidiospres. Scale bars: 10 μm (A–C), 5 μm (D–K).

Habitat

On decaying wood of deciduous tree, in forest dominated by Anacardiaceae, Palmae, Hypericaceae, and Sterculiaceae.

Additional specimens examined

CHINA. Guangxi Province, Chongzuo city, Longzhou county, Nonggang village, Nonggang National Nature Reserve, 106°56'E, 22°28'N, H.S. Ma, 16 September 2017, GX20170916001 (HMAS 279591).

Notes

Two specimens representing T. erythrina clustered in a well-supported clade and were closely related to T. samoensis. These two species showed 97.6%–97.8% and 93.7%–96.0% sequence identities in the D1/D2 domain and ITS region, respectively. Basidia in T. erythrina are larger than those of T. samoensis (12.0–18.0 μm × 13.0–19.0 μm in T. erythrina vs 12.0–18.0 μm × 8.0–12.0 μm in T. samoensis) (Chen 1998; Malysheva et al. 2015). Moreover, hyphidia are present and located in the hymenial structure and derived from the same generative hyphae with basidia in T. erythrina, whereas hyphidia are lacking in T. samoensis (Chen 1998; Malysheva et al. 2015).

Tremella salmonea X.Z. Liu & F.Y. Bai, sp. nov.

MycoBank No: MycoBank: MB827188
Figures 3, 6

Type

CHINA. Guangxi Province, Hechi city, Luocheng county, Jiuwan Mountain National Nature Reserve, 108°48'E, 25°19'N, G.J. Li, H.S. Ma, Z.L. Lin & M.Z. Zhang, 7 August 2017, GX20172637 (HMAS 279588).

Etymology

Salmonea refers to the colour of the basidioma.

Description

Basidiomata small, gyrose to cerebriform, 0.6–1.0 cm in diameter, firm gelatinous and thick, pale orange when fresh, yellow orange when dry, flat on the substrate. Hyphae smooth, thin-walled, slender, 2.0–3.5 μm in diameter, often with clamp connections. Haustoria rare, small, globose or subglobose, 2.0–4.0 μm in diameter, with single hyphae. Hyphidia rare, smooth, thin-walled, 2.0–4.0 μm, branched. Probasidial initials mostly subglobose to globose, sometimes broadly ellipsoid. Basidia, when mature, subglobose to globose, four-celled, occasionally two-celled, thin-walled, 31.0–38.0 μm × 29.0–37.0 μm, with longitudinally cruciate-septate, without stalk-like base; sterigmata up to 110.0 μm long, not swollen at apex. Basidiospores globose to subglobose, 16.0–22.0 μm × 15–20.0 μm, L = 18.3 ± 1.3 μm, W = 17.8 ± 1.4 μm, Q = 0.9–1.3 (n = 25), with a distinct apiculus. Conidia present, ellipsoid, fusiform to cylindrical, 8.0–17.0 μm × 2.0–5.0 μm, L = 10.7 ± 2.2 μm, W = 3.5 ± 0.5 μm, Q = 2–5.8 (n = 40), hyaline, clamped, arranged in cluster. Terminally and laterally swollen cells appearing abundant in the subhymenium, citriniform, pyriform or broadly ellipsoid, 9.0–20.0 μm × 5.6–13.0 μm, L = 14.2 ± 2.8 μm, W = 8.8 ± 1.8 μm, Q = 1.1–2.8 (n = 40).

Figure 6. 

Microscopic structure of Tremella salmonea (HMAS 279588). A Section through hymenium B Hyphae from context C Swollen cells D Conidia in cluster E–G Mature basidia H–M Basidiospres. Scale bars: 10 μm (A–M).

Habitat

On wood of deciduous tree, in forest dominated by Rosaceae, Moraceae, Lauraceae, and Theaceae.

Notes

Only one specimen representing T. salmonea formed a distinct clade closely related to T. taiwanensis with 96.8%–98.3% sequence identities in D1/D2 domain and 95.4%–96.6% in ITS region, respectively. The affinity of T. salmonea to T. taiwanensislacked high support by the coalescent-based method (Fig. 1). Tremella salmonea differs from T. taiwanensis in its larger basidia (31.0–38.0 μm × 29.0–37.0 μm in T. salmonea vs 23.0–29.0 μm × 22.0–27.0 μm in T. taiwanensis) and basidiospores (16.0–22.0 μm × 15.0–20.0 μm in T. salmonea vs 14.0–18.0 μm ×14.0–20.0 μm in T. taiwanensis). In addition, hyphae-like conidiogenous cells and dikaryotic conidia were observed in T. salmonea compared to monokaryotic conidia produced from apex of sterigmata (Chen 1998). Swollen cells were located in the hymenium in T. salmonea whereas they were absent in T. taiwanensis (Chen 1998).

Discussion

Tremella s. s. is characterized by their tremella-like basidiomata. Many morphological characteristics have been used in taxonomic studies of Tremella, including the shape, colour, and size of basidiomata, basidia, and basidiospores, as well as other features such as length of the stalks and sterigmata, spore formation of the basidia, conidia, swollen cells, and hyphidia (Chen 1998). However, morphology-based taxonomy of Tremella species is very complicated. Almost 30 macromorphological and micromorphological characters need to be checked for identification at the species level (Chen 1998). Morphological taxonomy cannot provide enough evidence of phylogenetic relationship. Morphologically, Tremella globispora resembles species in the Indercorata group by its pyriform to capitates basidia and its spores that are broader than long (Chen 1998). Nevertheless, it is more related to species in the Fuciformis group, based on molecular data (Chen 1998; Fell et al. 2000; Scorzetti et al. 2002; Liu et al. 2015b). The application of molecular phylogenetics has significantly benefited the systematics and taxonomy of Tremella. In the present study, four new species of genus Tremella are described from China based on both morphological and molecular data.

The fruiting bodies of fungi harbour diverse microbial community including bacteria, yeasts and filamentous fungi (Buzzini et al. 2005; Barbieri et al. 2007; Pacioni et al. 2007). Microbial habitants could have roles in the development of the fruiting body, such as mycelium growth, nutrition supply, antifungal activity, and flavour formation (Sbrana et al. 2002; Barbieri et al. 2007; Antony-Babu et al. 2013; Seung-Yoon et al. 2018). There have been a new bacterial species found in the fruiting body of T. fuciformis which can cause infection (Wen et al. 2016). Tremella basidiomaticola was isolated from the fruit body of T. fuciformis and their relationship and contributions to the growth of fruiting body remain unknown.

Tremella salmonea is highly supported as belonging to the Mesenterica group. Microscopically, T. salmonea and T. mesenterica are similar in that both species share loose a hymenial structure with abundant hyphidia. However, these two species have different basidiomata colour: in T. salmonea basidiomata are salmon-orange, whereas in T. mesenterica they are yellowish. Other species in the T. mesenterica group with similar basidiomata colour include T. roseolutescens (basidia 20–27 μm × 18–27 μm) and T. tropica(basidia 19–21 μm × 15–17 μm), but these are clearly different in the shape of their basidiomata and size of their basidia (Bandoni et al. 1996; Chen 1998; Roberts 2008).

The affiliation of T. cheejenii and T. erythrina to the Fuciformis or Mesenterica groups were not ascertained phylogenetically. Tremella cheejenii are closely related to T. fibulifera, T. lloydiae-candidae, and T. resupinata in the phylogenetic analysis. Though they all have white basidiomata, there are clear differences in the shape and size of their basidiamata, length of their basidia and stalks, and length of their sterigmata (Bandoni and Oberwinkler 1983; Chen 1998; Malysheva et al. 2015). Tremella hainanensis also has whitish basidiomata, but it is distinguished from T. cheejenii by its filamentous lobes and ball-like basidiomata (Peng 1982). Tremella erythrina is closely related to T. samoensis, nevertheless, T. erythrina is distinguished by its salmon-orange cerebriform basidiomata that are larger than in T. samoensis (Chen 1998). Macroscopically, the most similar species to T. erythrina is T. armeniaca, T. elastica, T. roseolutescens, and T. tawa, all of which have orange basidiomata. Tremella roseolutescens (basidia 20–27 μm × 18–27 μm; basidiospores 11–15 μm × 9–11.5 μm) is diagnosed by its pulvinate basidiomata and larger basidia and basidiospores differing from T. erythrina (basidia 12–18 μm × 13–19 μm; basidiospores 7–10 μm × 5–7 μm) (Bandoni et al. 1996). Basidia in T. erythrina are slightly larger than those of T. elastic (10.0–15.0 μm × 6.0–9.0 μm) (Chen 1998). The presence of conidia and phialide-like conidiogenous cells in the hymenium of T. armeniaca has not been discovered in T. erythrina (Bandoni et al. 1996). Tremella tawa (basidia 20–30 μm × 13–18 μm) differs from T. erythrina in its clavate basidia and larger basidiomata and basidia (Bandoni and Buchanan 1990).

A total of 33 specimens of Tremella s. s. were collected from seven provinces (Guangdong, Guangxi, Heilongjiang, Jilin, Qinghai, Tibet, and Yunnan), which span a large portion of China and have different climates, humidity, and vegetation types. This implies the genus is really diverse beyond current knowledge. Tremella s. s. showed a significant deviation from the optimal range calculated for the genus rank using the phylogenetic rank boundary optimization (RPBO) analysis that indicates great genetic variation between different species in Tremella s. s. (Liu et al. 2015b). Two subclades, namely Mesenterica and Fuciformis, are included in this genus and can be featured by distinct ecological and morphological characters (Chen 1998, Liu et al. 2015b). They could probably be reclassified as two separate genera in the future. Further studies with additional fresh collections will clarify the systematic of this genus and enrich the knowledge of distribution, abundance, and ecology of Tremella species.

Key to the whitish species in Tremella s. s

1 Basidia with sterigmata shorter than 35, hyphae grow from side of hyphae 2
Basidia with sterigmata longer than 35, hyphae grow from basidial clamp 3
2 Basidiomata gyrose to cerebriform, 1–3 cm in diameter and basidia > 10 μm long T. lloydiae-candidae
Basidiomata foliose, larger than 3 cm in diameter and basidia < 10 μm long 4
3 Basidiomata filamentous lobes, conjunctive as a ball T. hainanensis
Basidiomata resupinate or gyrose to cerebriform 5
4 Basidia globose to subglobose T. fuciformis
Basidia clavate with stalks T. yokohamensis
5 Basidiospores mostly broader than long T. globispora
Basidiospores mostly longer than broad 6
6 Basidiomata resupinate, < 1 cm in diameter T. resupinata
Basidiomata gyrose to cerebriform, usually > 1 cm in diameter 7
7 Basidia size longer than 30 μm and basidiospores > 17 μm long T. cerebriformis
Basidia size smaller than 20 μm and basidiospores ≤ 10 μm in long 8
8 Basidia > 13 μm wide, with short stalk, sterigmata with inconspicuous apically swollen T. cheejenii
Basidia < 13μm wide, without stalk, sterigmata with conspicuous apically swollen T. fibulifera

Key to the yellow, orange, or red species in Tremella s. s

1 Basidiomata yellow 2
Basidiomata orange or red 11
2 Basidia mostly > 25 μm long 3
Basidia mostly < 25 μm long 4
3 Basidia < 22 μm wide and basidiospores 10–12 μm long T. philippinensis
Basidia > 26 μm wide and basidiospores > 13 μm long T. brasiliensis
4 Basidiomata pulvinate T. subrubiginosa
Basidiomata gyrose to cerebriform or foliose 5
5 Basidiomata gyrose to cerebriform 6
Basidiomata foliose 8
6 Vesicles absent, haustoria rare, and conidia monokaryotic budding from apex of sterigmata T. taiwanensis
Vesicles present, haustoria abundant, and conidia dikaryotic from hyphae-like conidiogenous cells 7
7 Basidiospores broadly ellipsoid or ovoid T. mesenterica
Basidiospores globose to subglobose T. mesenterella
8 Basidia > 17 μm long and basidiospores > 7 μm wide T. iduensis
Basidia < 17 μm long and basidiospores < 7 μm wide 9
9 Basidiomata lobes not hollow T. boninensis
Basidiomata lobes hollow 10
10 Haustoria abundant and branched, probasidia mostly growing from side of the hymenial hyphae T. flava
Haustoria rare, probasidia proliferating directly from basidial clamps T. samoensis
11 Basidiomata pulvinate T. roseolutescens
Basidiomata gyrose to cerebriform or foliose 12
12 Basidiomata foliose and flat; basidia > 30 μm long T. salmonea
Basidiomata gyrose to cerebriform; basidia < 30 μm long 13
13 Basidiomata reddish 14
Basidiomata orange 15
14 Basidia 17–21 μm long T. rubromaculata
Basidia 11–15 μm long T. flammea
15 Basidia predominantly clavate T. tawa
Basidia globose to subglobose or ellipsoid to oval 16
16 Conidia present 17
Conidia absent 18
17 Conidiogenous cells globose or subglobose to ellipsoid, basidiospore > 12 μm long T. tropica
Conidiogenous cells phialide-like, basidiospore 6–9 μm long T. armeniaca
18 Hollow lobes T. erythrina
Not having hollow lobes T. dysenterica

Acknowledgments

We sincerely thank Professor Dr Rui-lin Zhao, Dr Jin-kang Wei, Dr Guo-jie Li, Mr Hu-sheng Ma, Dr Jun-min Liang, Mr Bao-song Chen, Ms Hui-jun Wang, Mr Guang-fu Mou, Mr Mao-qiang He, Ms Zhi-lin Ling, Mr Ming-zhe Zhang, and Mr Xin-yu Zhu for their kind help with collecting specimens. This project was supported by Grant No. 31670020 from the National Natural Science Foundation of China (NSFC), P. R. China, No. 2017125 from the Youth Innovation Promotion Association of the Chinese Academy of Sciences.

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Supplementary materials

Supplementary material 1 

Table S1. Physiological properties

Ying Zhao, Xin-zhan Liu, Feng-yan Bai

Data type: measurement

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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Supplementary material 2 

Sequence alignment

Ying Zhao, Xin-zhan Liu, Feng-yan Bai

Data type: phylogenetic data

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (64.09 kb)