Mycological Progress

, Volume 16, Issue 4, pp 403–417 | Cite as

Four new species of Tubeufia (Tubeufiaceae, Tubeufiales) from Thailand

  • Yong-Zhong Lu
  • Saranyaphat Boonmee
  • Dong-Qin Dai
  • Jian-Kui Liu
  • Kevin D. Hyde
  • D. Jayarama Bhat
  • Hiran Ariyawansa
  • Ji-Chuan Kang
Original Article

Abstract

Tubeufia was named for a sexual morph taxon. However, several asexual morph species have been accommodated in this genus as well. In our study, four new species of Tubeufia, viz. T. filiformis, T. latispora, T. laxispora and T. mackenziei, are described and illustrated. The phylogenetic placement of the new species is confirmed by analysis of combined ITS, LSU and TEF1α sequence data. A key to Tubeufia species is provided and the new species are compared with similar fungal taxa.

Keywords

Freshwater Helicosporous Phylogeny Taxonomy Woody substrates 

Introduction

The genus Tubeufia was introduced by Penzig and Saccardo (1897) to accommodate three species from Java, i.e. T. anceps, T. coronata and T. javanica, and was characterised by white, cream-pink to brownish, vertically oblong to ovoid ascomata, cylindrical asci and cylindrical, fusiform, vermiform, multi-septate ascospores (Barr 1980; Boonmee et al. 2011, 2014; Dai et al. 2017; Hyde et al. 2016). The genus has been relatively well studied, with data showing their wide distribution in both tropical and temperate regions (Scheuer 1991; Crane et al. 1998; Hsieh et al. 1998; Kodsueb et al. 2004, 2006; Lee et al. 2004; Tsui et al. 2006, 2007; Sánchez and Bianchinotti 2010; Boonmee et al. 2011, 2014; Dai et al. 2017; Doilom et al. 2017). There have been several recent introductions of new Tubeufia species, for example, Dai et al. (2017) described T. longiseta from a bamboo culm and Doilom et al. (2017) introduced T. tectonae, which formed an asexual morph on the decaying inner surface of the bark of Tectona grandis and morphologically resembled Helicomyces.

The type species T. javanica was described from Indonesia, but Boonmee et al. (2014) designated an epitype based on a collection on bamboo in Thailand. All of the described Tubeufia species are saprobes on decorticated or decaying woody substrates, often associated with other fungi, in terrestrial habitats or submerged in freshwater (Rossman 1977, 1979; Kodsueb et al. 2004; Boonmee et al. 2014; Hyde et al. 2016). The sexual morphs have ascomata that are superficially seated on a subiculum, with or without setae; with fissitunicate, saccate or cylindric-clavate asci and elongate, cylindric to subfusiform, or broadly fusiform, hyaline to pale brown ascospores with more than five septa, and that are fasciculate in the ascus. Their hyphomycetous asexual morphs have helicoid conidia, which are common morphological features in Helicoma, Helicomyces and Helicosporium species (Goos 1985, 1989; Zhao et al. 2007; Boonmee et al. 2011, 2014; Doilom et al. 2017; Hyde et al. 2016).

This paper introduces four novel species of Tubeufia with descriptions, illustrations and phylogenetic evidence. The data extend our knowledge on the genus.

Materials and methods

Sample collection and specimen examination

Decaying wood samples were randomly collected from sites in forests or in streams in Thailand. The procedures followed here have been described previously (Boonmee et al. 2014). Micromorphological structures were photographed using a Nikon Eclipse 80i compound microscope fitted with a Canon EOS 600D digital camera and measurements were made using the Tarosoft® Image FrameWork program. Figures were processed with Adobe Photoshop CS6 Extended version 10.0 software (Adobe Systems, USA).

Single spore isolations were obtained using the method described by Chomnunti et al. (2014). Germinating spores were aseptically transferred to fresh malt extract agar (MEA) plates and incubated at 25–30 °C. Cultures were grown for 1–2 months and morphological characters, such as colour, colony shape and texture, were recorded. The cultures were checked for asexual morphs after 30–60 days of growth. Type materials are deposited at the Herbarium of Mae Fah Luang University (Herb. MFLU), Chiang Rai, Thailand and the Guizhou Academy of Agriculture Sciences (Herb. GZAAS), Guiyang, China. Ex-type living cultures are deposited at Mae Fah Luang University Culture Collection (MFLUCC) and Guizhou Culture Collection (GZCC). Facesoffungi and MycoBank numbers are provided (Jayasiri et al. 2015).

DNA extraction, PCR amplification and sequencing

Genomic DNA was extracted from fungal mycelium grown on MEA at 28 °C for 60 days. Three genes were amplified with universal primers, namely the internal transcribed spacer region of ribosomal DNA (ITS: ITS5/ITS4) (White et al. 1990), large subunit nuclear ribosomal DNA (LSU: LROR/LR5) (Vilgalys and Hester 1990) and the translation elongation factor 1-alpha gene (TEF1α: EF1-983 F/EF1-2218R) (Rehner and Buckley 2005). The polymerase chain reaction (PCR) products were purified and sequenced with the same primers. The amplification reactions were carried out with the following protocol: the final volume of the PCR reaction was 50 μL, which contained 2 μL of DNA template, 2 μL of each forward and reverse primers, 25 μL of 2× Bench Top™ Taq Master Mix (mixture of Taq DNA Polymerase, dNTPs and MgCl2; Solarbio life sciences, Beijing, P.R. China) and 19 μL of distilled-deionised water. The following thermo-cycling parameters were used for the ITS region: initially 95 °C for 3 min, followed by 34 cycles of denaturation at 95 °C for 30 s, annealing at 51 °C for 1 min, elongation at 72 °C for 45 s and final extension at 72 °C for 10 min. The following thermo-cycling parameters were used for the LSU region: initially 95 °C for 3 min, followed by 30 cycles of denaturation at 94 °C for 30 s, annealing at 51 °C for 50 s, elongation at 72 °C for 1 min and a final extension at 72 °C for 7 min. The following thermo-cycling parameters were used for the TEF1α region: initially 95 °C for 3 min, followed by 40 cycles of denaturation at 94 °C for 30 s, annealing at 55 °C for 50 s, elongation at 72 °C for 1 min and a final extension at 72 °C for 7 min. The quality of PCR products was checked on 1% agarose gel electrophoresis stained with ethidium bromide. The PCR products were sent for sequencing at Sangon Biotech, Shanghai, China.

Phylogenetic analysis

BLAST searches of new sequences were performed to verify the identities of species in the GenBank database (Kodsueb et al. 2004; Tsui and Berbee 2006; Tsui et al. 2006; Promputtha and Miller 2010; Boonmee et al. 2014). The combined alignments of ITS, LSU and TEF1α sequence data from the closest relatives in Tubeufiaceae were used to generate phylogenetic trees (Boonmee et al. 2014; Hyde et al. 2016). Botryosphaeria dothidea (strain CBS 115476) in the closely related family Botryosphaeriaceae was selected as the outgroup taxon. The sequence accession numbers in the analysis are provided in Table 1. The sequence data were aligned using the MAFFT v.7.110 online program (http://mafft.cbrc.jp/alignment/server/) (Katoh and Standley 2013) and manually adjusted via BioEdit 7.2.3 (Hall 1999). Phylogenetic analyses were performed by using PAUP v.4.0b10 (Swofford 2002) for maximum parsimony (MP) and MrBayes v.3.2.2 (Ronquist et al. 2012) for Bayesian analyses.
Table 1

Taxa used in this study and their GenBank accession numbers for ITS, LSU and TEF1α DNA sequence data

Taxa

Culture accession no.b

GenBank accession no.

References

ITS

LSU

TEF1α

Acanthohelicospora pinicola

MFLUCC 10-0116

KF301526

KF301534

KF301555

Boonmee et al. (2014)

Acanthostigma perpusillum

UAMH 7237

AY916492

AY856892

a

Tsui et al. (2006)

Acanthostigma chiangmaiensis

MFLUCC 10-0125

JN865209

JN865197

KF301560

Boonmee et al. (2014)

Acanthostigmina multiseptatum

ANM 475

GQ856145

GQ850492

Promputtha and Miller (2010)

Acanthostigmina multiseptatum

ANM 665

GQ856144

GQ850493

Promputtha and Miller (2010)

Aquaphila albicans

MFLUCC 16-0010

KX454165

KX454166

KY117034

Hyde et al. (2016); this study

Aquaphila albicans

BCC 3543

DQ341096

DQ341101

Tsui et al. (2007)

Boerlagiomyces macrospora

MFLUCC 12-0388

KU144927

KU764712

KU872750

Doilom et al. (2017)

Botryosphaeria dothidea

CBS 115476

KF766151

DQ678051

DQ767637

Schoch et al. (2006); Slippers et al. (2013)

Chlamydotubeufia huaikangplaensis

MFLUCC 10-0926

JN865210

JN865198

Boonmee et al. (2011)

Chlamydotubeufia chlamydosporum

CBS 160.69

AY916466

AY856875

Tsui et al. (2006)

Chlamydotubeufia helicospora

MFLUCC 16-0213

KX454169

KX454170

KY117035

Hyde et al. (2016); this study

Helicangiospora lignicola

MFLUCC 11-0378

KF301523

KF301531

KF301552

Boonmee et al. (2014)

Helicoma muelleri

CBS 964.69

AY916453

AY856877

Tsui et al. (2006)

Helicoma khunkornensis

MFLUCC 10-0119

JN865203

JN865191

KF301559

Boonmee et al. (2011)

Helicoma chiangraiense

MFLUCC 10-0115

JN865200

JN865188

Boonmee et al. (2011)

Helicomyces roseus

CBS 283.51

AY916464

AY856881

Tsui et al. (2006)

Helicomyces indicum

CBS 374.93

AY916477

AY856885

Tsui et al. (2006)

Helicomyces paludosa

CBS 120503/AR 4206

DQ341095

DQ341103

Tsui et al. (2007)

Helicosporium vegetum

CBS 941.72

AY916488

AY856883

Tsui et al. (2006)

Helicosporium cereum

CBS 254.75

DQ470982

DQ471105

Spatafora et al. (2006)

Manoharachariella tectonae

MFLUCC 12-0170

KF301529

KF301537

KU872762

Boonmee et al. (2014)

Neoacanthostigma fusiforme

MFLUCC 11-0510

KF301529

KF301537

Boonmee et al. (2014)

Neoacanthostigma septoconstrictum

ANM 536.1

GQ856143

GQ850491

Promputtha and Miller (2010)

Tamhinispora indica

NFCCI 2924

KC469282

KC469283

Rajeshkumar and Sharma (2013)

Thaxteriellopsis lignicola

MFLUCC 10-0124

JN865208

JN865196

KF301561

Boonmee et al. (2011)

Thaxteriellopsis lignicola

MFLUCC 15-0898

KU144926

KU764711

KU872749

Doilom et al. (2017)

Tubeufia chiangmaiensis

MFLUCC 11-0514

KF301530

KF301538

KF301557

Boonmee et al. (2014)

Tubeufia cylindrothecia

BCC 3559

AY849965

Kodsueb et al. (2006)

Tubeufia filiformis

MFLUCC 16-1128

KY092407

KY117028

This study

Tubeufia filiformis

MFLUCC 16-1135

KY092416

KY092411

KY117032

This study

Tubeufia hyalospora

MFLUCC 15-1250

KX454179

Hyde et al. (2016)

Tubeufia intermedium

ATCC 22621

AY916463

AY856912

Tsui et al. (2006)

Tubeufia javanica

MFLUCC 12-0545

KJ880034

KJ880036

KJ880037

Boonmee et al. (2014)

Tubeufia latispora

MFLUCC 16-0027

KY092417

KY092412

KY117033

This study

Tubeufia laxispora

MFLUCC 16-0219

KY092414

KY092409

KY117030

This study

Tubeufia laxispora

MFLUCC 16-0232

KY092413

KY092408

KY117029

This study

Tubeufia lilliputeus

NBRC 32664

AY916483

AY856899

Tsui et al. (2006)

Tubeufia longiseta

MFLUCC 15-0188

KU940133

Dai et al. (2017)

Tubeufia mackenziei

MFLUCC 16-0222

KY092415

KY092410

KY117031

This study

Tubeufia roseohelicospora

MFLUCC 15-1247

KX454177

KX454178

Hyde et al. (2016)

Tubeufia roseus

BCC 8808 (SS1014)

AY916481

AY856910

Tsui et al. (2006)

Tubeufia roseus

BCC 3381

AY787932

Kodsueb et al. (2006)

Tubeufia tectonae

MFLUCC 12-0392

KU144923

KU764706

KU872763

Doilom et al. (2017)

New sequences are in bold

aNo data in GenBank

bANM A.N. Miller; ATCC American Type Culture Collection, Manassas, United States; BCC BIOTEC Culture Collection, Thailand; CBS Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands; MFLUCC Mae Fah Luang University Culture Collection, Chiang Rai, Thailand; NBRC the NITE Biological Resource Center; NFCCI the National Fungal Culture Collection of India; UAMH UAMH Centre for Global Microfungal Biodiversity, University of Toronto, Canada

The phylogeny website tool “ALTER” (Glez-Peña et al. 2010) was used to transfer the alignment fasta file for RAxML analysis. Maximum likelihood (ML) analysis was performed at the CIPRES Science Gateway v.3.3 (http://www.phylo.org/portal2/; Miller et al. 2010) using RAxML v.8.2.8 as part of the “RAxML-HPC BlackBox” tool (Stamatakis 2006; Stamatakis et al. 2008). All free model parameters were estimated by RAxML with ML estimates of 25 per site rate categories. The final ML search was conducted using the GTRGAMMA + I model. The best scoring tree was selected with a final likelihood value of −15447.971004. RAxML bootstrap support values greater than 75% are given at the branches in Fig. 1.
Fig. 1

Phylogenetic tree based on the analysis of a combined ITS, LSU and TEF1α dataset. Bayesian posterior probabilities greater than 0.95 (PP) (before the forward slash) and RAxML bootstrap support values greater than 75% (BS) (after the forward slash) are shown at the branches. The tree is rooted with Botryosphaeria dothidea CBS 115476 (Botryosphaeriaceae). The type species of each genus are in bold and new isolates in red

MP analyses were performed using the heuristic search option with 1000 random taxa addition and tree bisection and reconnection (TBR) as the branch-swapping algorithm. All characters were unordered and of equal weight, and gaps were treated as missing data. Maxtrees were unlimited, branches of zero length were collapsed and all multiple, equally parsimonious trees were saved. Clade stability was assessed using a bootstrap (BT) analysis with 1000 replicates, each with ten replicates of random stepwise addition of taxa (Hillis and Bull 1993). Bayesian analysis was carried out using MrBayes v.3.2.2 (Ronquist et al. 2012). The best-fit model of sequences evolution was estimated via MrModeltest 2.2 (Nylander 2004). Markov chain Monte Carlo (MCMC) sampling in MrBayes v.3.2.2 (Ronquist et al. 2012) was used to determine the posterior probabilities (PP) (Rannala and Yang 1996; Zhaxybayeva and Gogarten 2002). Phylogenetic trees were sampled every 100th generation (resulting in a total of 10,000 trees) in 1,000,000 generations from the running of six simultaneous Markov chains. The first 2000 trees, which contained the burn-in phase of the analyses, were discarded. The remaining 8000 trees were used to calculate the posterior probabilities in the majority rule consensus tree (Liu et al. 2011). Bayesian posterior probabilities equal to or greater than 0.95 are given at the branches in Fig. 1. Phylogenetic trees were visualised using FigTree v1.4.0 (http://tree.bio.ed.ac.uk/software/figtree/, Rambaut 2012). The sequences are deposited in GenBank (Table 1). The alignment was deposited in TreeBASE (http://www.treebase.org, submission number 20309).

Results

Phylogenetic analysis of combined ITS, LSU and TEF1α sequence data

Six tubeufiaceous isolates obtained from decaying wood were identified in Tubeufia. ITS, LSU and TEF1α sequence data and morphological characters were used to assign the species and to describe novel taxa with a comparison with similar taxa.

The combined sequence alignment comprised 44 taxa, with Botryosphaeria dothidea (CBS 115476) as the outgroup taxon. The dataset comprises 2324 characters after alignment, of which 1549 characters were constant, 201 variable characters were parsimony-uninformative and 574 characters were parsimony-informative. RAxML, MP and Bayesian analysis of the combined dataset resulted in phylogenetic reconstructions with largely similar topologies, and the Bayesian tree is shown in Fig. 1. Values of the Bayesian PP ≥0.95 from MCMC analyses and bootstrap support values of RAxML ≥75% are given at the branches in Fig. 1.

Representatives of the sequenced genera (with molecular data) of Tubeufiaceae (Kodsueb et al. 2006; Spatafora et al. 2006; Tsui et al. 2006, 2007; Promputtha and Miller 2010; Boonmee et al. 2011, 2014; Rajeshkumar and Sharma 2013; Dai et al. 2017; Doilom et al. 2017; Hyde et al. 2016) are included in our phylogenetic analysis (Fig. 1). Fifteen genera are represented by at least one species in Tubeufiaceae. Our six isolates were included in the analysis of combined ITS, LSU and TEF1α sequence data. They were identified as T. filiformis, T. latispora, T. laxispora and T. mackenziei spp. nov. based on morphology and phylogenetic analysis.

Taxonomy

Tubeufia filiformis Y.Z. Lu, Boonmee & K.D. Hyde, sp. nov. Figs. 2 and 3
Fig. 2

Tubeufia filiformis (MFLU 16-2659, holotype). a, b Superficial ascomata on substrate. Note shiny appearance under the light microscope. c Ascoma. d Peridium. e Pseudoparaphyses. f Asci with pseudoparaphyses. gi Asci. jm Ascospores. Scale bars: a, b = 200 μm, c = 200 μm, d, f, g = 100 μm, e = 20 μm, hm = 50 μm

Fig. 3

Tubeufia filiformis (asexual morph, MFLU 16-2660, paratype). a Colony on wood. b Conidiogenous cell with conidiophores. ce Conidia. f Germinating conidium. g, h Colony on MEA from above and below. Scale bars: a = 500 μm, b = 20 μm, cf = 50 μm, g, h = 40 mm

MycoBank: MB 818986; Facesoffungi number: FoF 02692

Holotype: MFLU 16-2659

Etymology: ‘filiformis’ referring to elongate filiform ascospores.

Saprobic on decaying wood in a stream. Sexual morph:Ascomata 273–327 μm high × 160–174 μm diam., superficial, seated on a subiculum, solitary, sometimes gregarious, oblong, subclavate to obclavate, cream-white to yellowish when young, brownish to brown when mature, apex rounded, base narrow, brown to dark brown, collapsing when dry, compressed subiculum hyphae, 3.5–5.5 μm wide, partially branched, septate, dark brown and irregular. Peridium 21–33 μm wide, comprising light brown cells of textura angularis, and inwardly small, subhyaline cells of textura prismatica. Hamathecium comprising numerous, 1.5–3 μm wide, filiform, septate, branched, hyaline pseudoparaphyses. Asci 138–181 × 15–17 μm (\( \overline{x} \) = 153 × 16 μm, n = 20), 8-spored, bitunicate, fissitunicate, cylindrical, short pedicellate, apically rounded, with an ocular chamber. Ascospores 94–157 × 3.5–4.5 μm (\( \overline{x} \) = 124 × 4 μm, n = 50), fasciculate, broadly filiform, cylindrical to long subfusiform, elongate, ends rounded, 13–16-septate, not constricted at septa, hyaline to pale yellow or brown, smooth-walled. Asexual morph: Conidiophores pale brown, macronematous, erect, short, smooth-walled. Conidiogenous cells monoblastic, holoblastic, integrated, each with a single conidium. Conidia 54.5–75 μm diam. and conidial filament 4.5–5.5 μm wide (\( \overline{x} \) = 65 × 5 μm, n = 20), 331–392 μm long, loosely coiled 1–2.5 times, rounded at the tip, multi-septate, slightly constricted at septa, hyaline, smooth-walled.

Culture characteristics: Conidia germinating on water agar (WA) within 36 h and germ tubes produced from ascospores. Colonies growing on malt extract agar (MEA), circular, umbonate, edge entire, reaching 11 mm in 2 weeks at 28 °C, brown to dark brown in MEA medium. Mycelium superficial and partially immersed, branched, septate, hyaline to pale brown, smooth.

Materials examined: THAILAND, Krabi, Plai Praya, Khao To, Ban Bang Thao Mae, on decaying wood in a freshwater stream, 17 December 2015, Saranyaphat Boonmee, BTM01-5 (MFLU 16-2659, holotype; GZAAS 16-0141, isotype); ex-type living culture, MFLUCC 16-1128 = GZCC 16-0104; Krabi, Muang, Khao Khram, Ban Nong Jig, Tha Pom Klong Song Nam, on decaying wood in freshwater stream, 16 December 2015, Saranyaphat Boonmee, TP01-4 (MFLU 16-2660, paratype; GZAAS 16-0142); living culture, MFLUCC 16-1135 = GZCC 16-0105.

Notes: The sexual morph of Tubeufia filiformis has elongated, curved, filiform ascospores which are 94–157 μm long. Phylogenetically, T. filiformis forms a sister clade to T. roseohelicospora, T. tectonae and T. hyalospora with high support (Fig. 1). Tubeufia filiformis formed a sexual morph on the natural substrate, morphologically similar to that of T. javanica (Boonmee et al. 2014). The ascomata of T. filiformis (273–327 × 160–174 μm) are smaller than T. javanica (376–505 × 224–260 μm) and its asci (138–181 × 14.9–17.1 μm) are shorter than T. javanica (164–221 × 14–18 μm) as well. The ascospores of T. filiformis are, however, longer than that of T. javanica (100.5–117 × 4–5 μm). Both the asexual and sexual morphs were found on the woody substrates.

Tubeufia latispora Y.Z. Lu, Boonmee & K.D. Hyde, sp. nov. Fig. 4
Fig. 4

Tubeufia latispora (MFLU 16-2658, holotype). a Superficial ascomata on substrate. Note ascomata surrounded by dark brown setae. b Ascoma. c Peridium. d Seta. e Hamathecium. fh Asci. i Germinating ascospore. jl Ascospores. Scale bars: a = 500 μm, b = 100 μm, cd, fi = 50 μm, e, jl = 20 μm

MycoBank: MB 818985; Facesoffungi number: FoF 02691

Holotype: MFLU 16-2658

Etymology: ‘latispora’ referring to wide ascospores.

Saprobic on decaying wood in a stream. Sexual morph: Ascomata 267–331 μm high × 166–215 μm diam. (\( \overline{x} \) = 287 × 185 μm, n = 20), superficial, gregarious, ellipsoidal, globose to subglobose, dark brown. Setae (99–) 135–317 × 3–6.5 μm (\( \overline{x} \) = 229 × 4.5 μm, n = 30), dense, flexuous, covering the whole ascoma, unbranched, rounded at apical end, septate, dark brown. Peridium 24–44 μm wide, composed cells of textura angularis, dark, with innermost part comprising thin layers of hyaline to pale brown cells of textura subprismatica. Hamathecium comprising numerous filiform, septate, branched, hyaline pseudoparaphyses. Asci 137–235 × 20–30 μm (\( \overline{x} \) = 181 × 24 μm, n = 30), 8-spored, bitunicate, cylindrical, rounded at the apex, with an ocular chamber, thick-walled, sessile. Ascospores 68–105 × 7–10 μm (\( \overline{x} \) = 83 × 8.5 μm, n = 50), fasciculate, broad fusiform, cylindrical to long subfusiform, elongate, slightly curved, tapering towards the rounded ends, 16–21-septate, hyaline, smooth-walled. Asexual morph: Undetermined.

Culture characteristics: Ascospores germinating in water agar (WA) within 24 h and germ tubes produced from a lower cell of ascospores. Colonies growing slowly on malt extract agar (MEA), irregular, with rough surface, edge undulate, reaching 10 mm in 2 weeks at 28 °C, initially brown and becoming dark brown when aged. Mycelium superficial and partly immersed, branched, septate, hyaline to pale brown, smooth-walled.

Material examined: THAILAND, Chiang Rai, Muang, Ban Nang Lae Nai, on decaying wood in a freshwater stream, 28 November 2015, Saranyaphat Boonmee and Yong-Zhong Lu, TUB06 (MFLU 16-2658, holotype; GZAAS 16-0140, isotype); ex-type living culture, MFLUCC 16-0027 = GZCC 16-0103.

Notes: Tubeufia latispora is introduced here as a novel species based on its distinct morphological and phylogenetic placement. The phylogenetic analysis (Fig. 1) recognises T. latispora belonging to the genus Tubeufia, where it is sister to T. longiseta with high support (100% BS and 1.00 PP). Tubeufia latispora formed a sexual morph on the natural substrate, which is morphologically quite similar to T. longiseta (Dai et al. 2017). Although both species have similar coloured and sized ascomata and are covered by dense, flexuous setae, T. latispora differs from T. longiseta in the sizes of asci and ascospores. The asci (137–235 × 20–30 μm) of T. latispora are longer and wider than T. longiseta (90–140 × 14.5–18 μm) and ascospores (68–105 × 7–10 μm) are longer and wider than T. longiseta (38.5–55.5 × 4.5–6 μm) as well. Therefore, we introduced it as a novel species.

Tubeufia laxispora Y.Z. Lu, Boonmee & K.D. Hyde, sp. nov. Fig. 5
Fig. 5

Tubeufia laxispora (MFLU 16-2663, holotype). a Colony on wood. b Conidiogenous cells with conidiophores and conidium. cf Conidia. g Germinating conidium. h, i Colonies on MEA from above and below. Scale bars: a = 200 μm, b = 50 μm, ce, g = 20 μm, f = 10 μm, h, i = 20 mm

MycoBank: MB 818987; Facesoffungi number: FoF 02694

Holotype: MFLU 16-2663

Etymology: ‘laxispora’ referring to loosely coiled helicospores.

Saprobic on submerged wood in a stream. Mycelium partly immersed, partly superficial, pale brown, septate, sparsely branched hyphae, with masses of crowded conidia. Sexual morph: Undetermined. Asexual morph: Conidiophores 30.5–73 μm long, 3.5–5 μm wide, pale brown at the base, gradually paler upwards, becoming hyaline, macronematous, erect, short, smooth-walled. Conidiogenous cells monoblastic, holoblastic, integrated, each with single conidium. Conidia 17.5–40 μm diam. and conidial filament 2–4 μm wide (\( \overline{x} \) = 26.5 × 3 μm, n = 20), with 111–182 μm long, loosely coiled 1–3.5 times, rounded at the apical end, multi-septate, slightly constricted at septa, hyaline, smooth-walled.

Culture characteristics: Conidia germinating on water agar (WA) within 12 h and germ tubes produced from conidia. Colonies growing on malt extract agar (MEA), circular, edge entire, reaching 12 mm in 2 weeks at 28 °C, brown to dark brown in MEA medium. Mycelium superficial and partially immersed, branched, septate, hyaline to pale brown, smooth-walled.

Materials examined: THAILAND, Krabi, Plai Praya, Khao To, Ban Bang Thao Mae, on decaying wood in a freshwater stream, 17 December 2015, Saranyaphat Boonmee, BTM06-1 (MFLU 16-2663, holotype; GZAAS 16-0145, isotype); ex-type living culture, MFLUCC 16-0232 = GZCC 16-0108; Krabi, Muang, Nongtalay, Khao Hang Nak, on decaying wood in a freshwater stream, 16 December 2015, Saranyaphat Boonmee, HN02-2 (MFLU 16-2662; GZAAS 16-0144); living culture, MFLUCC 16-0219 = GZCC 16-0107.

Notes: Tubeufia laxispora formed an asexual morph on the natural substrate and is morphologically similar to T. tectonae and T. hyalospora. Their colonies on natural substrates are hyaline to white and conidiophores are pale brown at the base; however, these taxa differ in conidia size. The conidia (17.5–40 μm diam.) of T. laxispora are distinctly smaller than T. tectonae (32–55 μm diam.), slightly larger than T. hyalospora (16–33 μm diam.), but the conidial filament is similar in size (Table 2). Furthermore, T. laxispora shares similar characters to Helicomyces denticulatus in the conidia shape and size. However, the conidiophores of H. denticulatus (5–13 × 3–4.5 μm) are distinctly shorter than T. laxispora (30.5–73 × 3.5–5 μm) and the conidia of H. denticulatus coiled 3.5–3.75 times (Zhao et al. 2007) differs from T. laxispora (conidia coiled 1–3.5 times). Phylogenetically, T. laxispora formed a single clade with high support (91% BS, 1.00 PP) within Tubeufia. Therefore, we introduced it as a novel species.
Table 2

Synopsis of Tubeufia asexual species

Species

Colonies on natural substrates

Conidiophores

Diameter of conidia (μm)

Number of coils in conidia (times)

Width of conidial filament (μm)

References

Tubeufia filiformis

Hyaline to white

Pale brown

54.5–75

1–2.5

4.5–5.5

This study

T. hyalospora

Hyaline to white

Pale brown

16–33

2.5–3.5

3–5

Hyde et al. (2016)

T. intermedium

Yellowish brown to reddish brown

Brown to dark brown

21–26

2–2.75

5.5–7

Zhao et al. (2007)

T. laxispora

Hyaline to white

Pale brown at base, gradually paler upwards becoming hyaline

17.5–40

1–3.5

2–4

This study

T. lilliputeus

Hyaline to pale yellow

Hyaline

12.5–20

2–3.25

1.5–2.5

Moore (1957); Zhao et al. (2007)

T. mackenziei

Hyaline to white

Pale brown

26.5–32.5

2.5–3.5

4.5–6.5

This study

T. roseohelicospora

Light pink

Pale brown

36–48

2.5–3.5

5–7

Hyde et al. (2016)

T. tectonae

Subhyaline to white

Pale brown at base, gradually paler upwards becoming subhyaline to pale yellow

32–55

2–3.5

2–5

Doilom et al. (2017)

In T. roseus, data are lacking

Tubeufia mackenziei Y.Z. Lu, Boonmee & K.D. Hyde, sp. nov. Fig. 6
Fig. 6

Tubeufia mackenziei (MFLU 16-2661, holotype). a Colony on wood substrate. b, c Conidiophores with apical conidium. d Conidiogenous cell with conidiophores. ei Conidia. j Germinating conidium. k, l Colony on MEA from above and below. Scale bars: a = 200 μm, b, c = 50 μm, dj = 20 μm, k, l = 10 mm

MycoBank: MB 818988; Facesoffungi number: FoF 02693

Holotype: MFLU 16-2661

Etymology: Named in honour of Professor Eric H. C. McKenzie for his outstanding contributions to mycology.

Saprobic on decaying wood in a stream. Mycelium partly immersed, partly superficial, pale brown, septate, with sparsely branched hyphae, with masses of crowded conidia. Sexual morph: Undetermined. Asexual morph: Conidiophores 60–102.5 μm long, 4.5–6 μm wide, pale brown, macronematous, erect, short, smooth-walled. Conidiogenous cells monoblastic, holoblastic, integrated, denticulate. Conidia 26.5–32.5 μm diam. and conidial filament 4.5–6.5 μm wide (\( \overline{x} \) = 28.5 × 5.5 μm, n = 20) with (99–) 116–141 μm long, tightly coiled 2.5–3.5 times, rounded at apical end, multi-septate, up to 23–septate, slightly constricted at septa, hyaline, smooth-walled.

Culture characteristics: Conidia germinating on water agar (WA) within 12 h. Colonies growing slowly on malt extract agar (MEA), irregular, surface rough, edge undulate, reaching 11 mm in 2 weeks at 28 °C, brown to dark brown in MEA medium. Mycelium superficial and partially immersed, branched, septate, hyaline to pale brown, smooth-walled.

Material examined: THAILAND, Krabi, Muang, Nongtalay, Khao Hang Nak, on decaying wood in a freshwater stream, 16 December 2015, Saranyaphat Boonmee, HN05-1 (MFLU 16-2661, holotype; GZAAS 16-0143, isotype); ex-type living culture, MFLUCC 16-0222 = GZCC 16-0106.

Notes: Phylogenetic analysis places the newly described T. mackenziei within the Tubeufia clade, where it occurs as a sister species to T. lilliputeus. Tubeufia mackenziei formed an asexual morph on the natural substrate and is morphologically similar to T. lilliputeus and Helicoma morganii (Linder 1929; Moore 1957; Zhao et al. 2007). However, T. mackenziei differs from T. lilliputeus in conidia size and shape. The conidia of T. mackenziei (26.5–32.5 μm diam.) are distinctly larger than T. lilliputeus (12.5–20 μm diam.) and its conidial filaments (4.5–6.5 μm) are also distinctly wider than those of T. lilliputeus (1.5–2.5 μm). Tubeufia mackenziei differs from H. morganii in sizes of conidiophores and conidia. The conidiophores of T. mackenziei (60–102.5 × 4.5–6 μm) are shorter than those of H. morganii (up to 250 μm long, 3.2–7 μm wide). The conidia of T. mackenziei (26.5–32.5 × 4.5–6.5 μm) are larger than those of H. morganii (17–27 × 3–4.5 μm). Thus, we introduced T. mackenziei as a novel species.

Discussion

In this study, we introduced four new Tubeufia species, T. filiformis, T. latispora, T. laxispora and T. mackenziei, based on both morphology and phylogeny analyses. A key to the species accepted in Tubeufia, in which their placement is confirmed with molecular analysis, is provided.

We compared all asexual morph species of Tubeufia except T. roseus (Table 2) because of the unavailability of its voucher material. We introduced three new asexual morph species into Tubeufia, namely T. filiformis, T. laxispora and T. mackenziei.

The genus Tubeufia now comprises 27 species (Table 3), 14 species whose placement is confirmed with molecular analysis. Nine species are reported from fresh water, including those newly described, viz. T. claspisphaeria, T. filiformis, T. hyalospora, T. latispora, T. laxispora, T. mackenziei, T. paludosa, T. roseohelicospora and T. roseus. One sexual morph species, T. filiformis, has been linked to its asexual morph. Tubeufia species are characterised by white, cream-pink to brownish, black, vertical oblong to ovoid ascomata and cylindrical, fusiform, vermiform, multi-septate ascospores, asexual morphs commonly found as helicoid conidia.
Table 3

Checklist of Tubeufia species

No.

Name of species

Hosts

Location

References

1

Tubeufia acaciae

On dead bark of Acacia catechu

India

Tilak and Kale (1969)

2

T. aciculospora

On mycelium of Perisporiopsis quinqueseptata on Syzygium buxifolium

Japan

Katsumoto and Harada (1979)

3

T. aurantiella

On well-rotted wood

Java

Rossman (1979)

4

T. brevispina

On stromata of Hypoxylon deustum

New York

Barr and Rogerson (1983); Crane et al. (1998)

5

T. claspisphaeria

Wood submerged in stream

Hong Kong

Kodsueb et al. (2004)

6

T. cylindrothecia

On old corn stalks

Ohio

Seaver (1909)

7

T. dactylariae

On decayed twig

Taiwan

Chang (2003)

8

T. eriodermatis

On Erioderma sorediatum

Colombia

Etayo (2002)

9

T. eugeniae

On dead twigs of Syzygium cumini

Madhya Pradesh

Pande (2008)

10

T. filiformis

On decaying wood in a freshwater stream

Thailand

This study

11

T. garugae

On bark of Garuga pinnata

Maharashtra

Pande (2008)

12

T. helicomyces

In Graminaceis emortuis

Austria

Saccardo (1913); Rossman (1977)

13

T. heterodermiae

On dead wood

Belgium, Luxembourg, northern France

van den Boom and van den Boom (2006)

14

T. hyalospora

On decaying wood in flowing freshwater stream

Thailand

Hyde et al. (2016)

15

T. javanica

On dead culms or sheaths of bamboo

Tjibodas, Thailand

Boonmee et al. (2014)

16

T. latispora

On decaying wood in a freshwater stream

Thailand

This study

17

T. laxispora

On decaying wood in a freshwater stream

Thailand

This study

18

T. longiseta

On dead culms of bamboo

Thailand

Dai et al. (2017)

19

T. mackenziei

On decaying wood in a freshwater stream

Thailand

This study

20

T. pachythrix

On well-rotted wood

Brazil

Rossman (1979)

21

T. paludosa

On decaying wood; on wood partially submerged

Bermuda, Canada, England, Japan, Hong Kong

Rossman (1977); Kodsueb et al. (2004)

22

T. pannariae

On thallus of Pannaria rubiginosa

Colombia

Etayo (2002)

23

T. parvula

On dead inflorescences of Ammophila arenaria

Great Britain

Dennis (1975)

24

T. roseohelicospora

On decaying wood in flowing freshwater stream

Thailand

Hyde et al. (2016)

25

T. roseus

Submerged wood in a river

Thailand

Tsui et al. (2006); Boonmee et al. (2014)

26

T. silentvalleyensis

On dead wood

Kerala

Pande (2008)

27

T. tectonae

On decaying inner surface of bark of Tectona grandis

Thailand

Doilom et al. (2017)

The most similar genera that can be confused with Tubeufia species are Helicoma, Helicomyces and Helicosporium. (1) Helicoma and Tubeufia species share similar features in their sexual morphs, but they can be distinguished in their asexual morphs. The Helicoma asexual morph is characterised by relatively short, erect, thick, dark brown conidiophores, holoblastic conidiogenous cells, denticulate conidiophores and helicoid, hyaline to pigmented, broad conidia. (2) There is only one sexual morph species known in Helicomyces, which is H. paludosa (= Tubeufia paludosa, BPI 871087, CBS 120503), renamed by Boonmee et al. (2014) based on phylogenetic analysis. We compared Helicomyces paludosa with other Tubeufia species and they are morphologically rather similar in all characters. However, Tubeufia species have short pedicellate or apedicellate asci, while Helicomyces paludosa have long pedicellate asci (Boonmee et al. 2014). The asexual morphs share similar characters (Tsui and Berbee 2006). Tsui et al. (2006, 2007) indicated that species referred to as Helicomyces are polyphyletic and linked to the sexual genera Acanthostigma and Tubeufia. Therefore, they cannot be well separated based on morphology, but phylogenetic analysis can resolve their taxonomic placement. (3) In Helicosporium, conidiophores are fertile in the centre and sterile and tapering towards the narrow subacute apex (Goos 1989; Zhao et al. 2007; Boonmee et al. 2014), but Tubeufia species differ.
  • Key to species of Tubeufia (confirmed with molecular data)

  • 1. Ascomata present......................................................................................................2

  • 1. Ascomata lacking......................................................................................................7

  • 2. Ascospores with >10 septa......................................................................................................3

  • 2. Ascospores 46–53 (−55.5) × (3.5–) 4–4.5 μm, cylindric-fusiform, 7-septate......................................................................................................T. chiangmaiensis

  • 3. Ascospores shorter than 67 μm......................................................................................................4

  • 3. Ascospores longer than 67 μm......................................................................................................5

  • 4. Ascomata subglobose, obovoid, black, dense long setae covering the whole ascomata, ascospores 38.5–55.5 × 4.5–6 μm......................................................................................................T. longiseta

  • 4. Ascomata ellipsoid or cylindric, pallid or brightly pigmented, rarely short setae or without setae, ascospores 40–55 (−65) × (2.5–) 3–5 μm, elongate clavate or fusoid, (5–) 7–9 (−13)-septate......................................................................................................T. cylindrothecia

  • 5. Ascomata 267–331 × 166–215 μm, asci 137–235 × 20–30 μm, ascospores 68–105 × 7–10 μm, 16–21-septate......................................................................................................T. latispora

  • 5. Ascospores with <18 septa......................................................................................................6

  • 6. Ascomata 273–327 × 160–174 μm, asci 138–181 × 14.9–17.1 μm, ascospores 94–157 × 3.5–4.5 μm, 13–16-septate......................................................................................................T. filiformis

  • 6. Ascomata 376–505 (−550) × (200–) 224–260 μm, asci (140–) 164–221 (−230) × 14–18 (−22) μm, ascospores (95–) 100.5–117 (−120) × 4–5 μm, 14–17-septate......................................................................................................T. javanica

  • 7. Conidial filament wider than 5 μm......................................................................................................8

  • 7. Conidial filament narrower than 5 μm......................................................................................................11

  • 8. Diameter of conidia <35 μm......................................................................................................9

  • 8. Diameter of conidia >35 μm......................................................................................................10

  • 9. Colonies on natural substrates yellowish brown to reddish brown, diameter of conidia 21–26 μm, conidia coiled 2–2.75 times, conidial filament 5.5–7 μm wide......................................................................................................T. intermedium

  • 9. Colonies on natural substrates hyaline to white, diameter of conidia 26.5–32.5 μm, conidia coiled 2.5–3.5 times, conidial filament 4.5–6.5 μm wide.......................................................................................................T. mackenziei

  • 10. Colonies on natural substrates light pink, diameter of conidia 36–48 μm, conidia coiled 2.5–3.5 times, conidial filament 5–7 μm wide...............................T. roseohelicospora

  • 10. Colonies on natural substrates hyaline to white, diameter of conidia 54.5–75 μm, conidia coiled 1–2.5 times, conidial filament 4.5–5.5 μm wide.....................................................................T. filiformis

  • 11. Diameter of conidia <33 μm....................................12

  • 11. Diameter of conidia >33 μm......................................................................................................13

  • 12. Colonies on natural substrates hyaline to white, diameter of conidia 16–33 μm, conidia coiled 2.5–3.5 times, conidial filament 3–5 μm wide..........................T. hyalospora

  • 12. Colonies on natural substrates hyaline to pale yellow, diameter of conidia 12.5–20 μm, conidia coiled 2–3.25 times, conidial filament 1.5–2.5 μm wide.............................T. lilliputeus

  • 13. Colonies on natural substrates hyaline to white, diameter of conidia 17.5–40 μm, conidia coiled 1–3.5 times, conidial filament 2–4 μm wide........................T. laxispora

  • 13. Colonies on natural substrates subhyaline to white, diameter of conidia 32–55 μm, conidia coiled 2–3.5 times, conidial filament 2–5 μm wide............................T. tectonae

Notes

Acknowledgements

This work was funded by grants of the National Natural Science Foundation of China (NSFC grant nos. 31460011, 31260087 and 31460561) and the Thailand Research Fund (project no. TRG5880152). Yong-Zhong Lu thanks Dr. Shaun Pennycook, Yuan-Pin Xiao, Qing Tian, Ting-Chi Wen, Chuan-Gen Lin and Ning-Guo Liu for their help. Dong-Qin Dai would like to thank the Key Laboratory of Yunnan Province Universities of the Diversity and Ecological Adaptive Evolution for Animals and Plants on Yun Gui Plateau for the support. K.D. Hyde would like to thank the Chinese Academy of Sciences, project number 2013T2S0030, for the award of Visiting Professorship for Senior International Scientists at Kunming Institute of Botany.

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Copyright information

© German Mycological Society and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.The Engineering and Research Center for Southwest Bio-Pharmaceutical Resources of National Education Ministry of ChinaGuizhou UniversityGuiyangPeople’s Republic of China
  2. 2.Center of Excellence in Fungal ResearchMae Fah Luang UniversityChiang RaiThailand
  3. 3.School of Pharmaceutical EngineeringGuizhou Institute of TechnologyGuiyangPeople’s Republic of China
  4. 4.Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food EngineeringQujing Normal UniversityQujingPeople’s Republic of China
  5. 5.Guizhou Key Laboratory of Agricultural BiotechnologyGuizhou Academy of Agricultural SciencesGuiyangPeople’s Republic of China
  6. 6.Formerly: Department of BotanyGoa UniversityGoaIndia
  7. 7.Curca, Goa VelhaIndia

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