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Submitted 23 February 2017, Accepted 22 March 2017, Published 3 April 2017
Corresponding Author: Liu ZY－email－gzliuzuoyi@163.com
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Fungi from Asian Karst formations II. Two new species of
Occultibambusa (Occultibambusaceae, Dothideomycetes) from karst
landforms of China
Zhang JF1,2,3, Liu JK2,4, Hyde KD2,3, Yang W1 & Liu ZY2*
1Guizhou Tea Research Institute, Guizhou Academy of Agricultural Sciences, Guiyang 550006, P. R. China.
2Guizhou Key Laboratory of Agricultural Biotechnology, Guizhou Academy of Agricultural Sciences, Guiyang 550006,
P. R. China
3Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai 57100, Thailand.
4Guizhou Institute of Biotechnology, Guiyang, Guizhou 550006, P. R. China
Zhang JF, Liu JK, Hyde KD, Yang W, Liu ZY 2017 – Fungi from Asian Karst formations II. Two
new species of Occultibambusa (Occultibambusaceae, Dothideomycetes) from karst landforms of
China. Mycosphere 8(4), 550–559, Doi 10.5943/mycosphere/8/4/4
Abstract
During an investigation of saprobic ascomycetes from karst landforms in southwest China, two
new species were isolated from dead bamboo culms collected from Maolan Town in Guizhou
Province. The new taxa share similar morphological characters as known Occultibambusa species in
having immersed, papillate ascomata, broadly-cylindrical to clavate asci and fusiform, hyaline to
brown ascospores. Phylogenetic analysis of combined LSU, SSU, TEF1-α and RPB2 sequence data
also placed the new taxa within the genus Occultibambusa in the family Occultibambusaceae with
good support. The new taxa can be distinguished from other species by septation and different-sized
ascospores and the present or absence of sheaths. The new species, Occultibambusa jonesii and O.
maolanensis are introduced here, with descriptions, illustrations and molecular data.
Key words－Dothideomycetes－phylogeny－Pleosporales－taxonomy
Introduction
We are carrying out the fungal diversity survey in the Karst formations of the Asian region and
this is the second in a series of papers (Chen et al. 2017). The family of Occultibambusaceae D.Q.
Dai & K.D. Hyde was introduced by Dai et al. (2017) and assigned to the order Pleosporales. The
family is typified by Occultibambusa and characterized by immersed, solitary to gregarious
ascomata, cylindrical to clavate, bitunicate asci and fusiform, hyaline to brown, septate ascospores
and rather diverse asexual morphs. The family presently comprises four genera: Neooccultibambusa
Doilom & K.D. Hyde (Doilom et al. 2017), Occultibambusa D.Q. Dai, Seriascoma Phookamsak.,
D.Q. Dai & K.D. Hyde (Dai et al. 2017) and Versicolorisporium Sat. Hatak., Kaz. Tanaka & Y.
Harada (Hatakeyama et al. 2008).
Species in this family occur on monocotyledons and hardwood trees, and share similar
morphology with species of the genera Bambusicola, Lophiostoma and Massarina in having clavate
asci and fusiform ascospores, however they can be distinguished readily via phylogenetic analysis
Mycosphere 8(4): 550–559 (2017) www.mycosphere.org ISSN 2077 7019
Article
Doi 10.5943/mycosphere/8/4/4
Copyright © Guizhou Academy of Agricultural Sciences
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(Zhang et al. 2009, Dai et al. 2012, 2015, 2017). Dai et al. (2017) indicated that the family
Occultibambusaceae is phylogenetically close to Biatriosporaceae, but differs from members of the
latter, which usually having dark brown ascospores with hyaline, rounded, swollen ends which
release mucilage (Hyde et al. 1986, 2013, Dai et al. 2017). There is confusion surrounding
Biatriosporaceae and until Biatriospora marina is epitypified (sensu Ariyawansa et al. 2014), we
follow the classification of Wijayawardene et al. (2014).
In the course of an ongoing survey of saprobic ascomycetes from Karst landforms, two new
taxa were isolated from dead bamboo culms collected in Guizhou Province, southwest China.
Molecular analysis of combined LSU, SSU, TEF1-α and RPB2 sequence data placed the new taxa
within the family of Occultibambusaceae where they cluster with Occultibambusa species with good
support. The taxa also share similar morphological characters with existing Occultibambusa species.
Therefore, O. jonesii and O. maolanensis are introduced to accommodate the new taxa.
Materials & Methods
Collection, examination and isolation of specimens
Samples were collected from Maolan Town in Guizhou Province, and taken back to
laboratory in envelopes. Examination and vertical sections of samples were processed under a
stereomicroscope (Nikon SMZ 745) and a compound microscope (Nikon E100). Micro-
morphological characters were observed under the Nikon ECLIPSE Ni compound microscope and
captured by using the Cannon EOS 70D digital camera with DIC microscopy. The Tarosoft (R) Image
Frame Work version 0.9.7 program was used to measure micro-morphological characters, and
photographic plates were edit by using Adobe Photoshop CS6 (Adobe Systems Inc., USA).
Isolates were made from single ascospore following the method by Chomnunti et al. (2014).
The single germinated ascospore was individually transferred to potato dextrose agar (PDA; 39 g/l
distilled water, Difco potato dextrose) and incubated at 25 oC in the dark for recording growth rates
and culture characters. The holotypes are deposited at the herbarium of Guizhou Academy of
Agricultural Sciences (GZAAS), Guiyang, China and duplicated at the herbarium of Kunming
Institute of Botany, Chinese Academy of Sciences (HKAS), Kunming, China. Isolates are deposited
at Guizhou Culture Collection (GZCC), Gui Yang, China and duplicated at Kunming Culture
Collection (KUMCC), Kunming, China. Facesoffungi and Index Fungorum numbers are provided as
explained in Jayasiri et al. (2015) and Index Fungorum (2017).
DNA extraction, PCR amplification and sequencing
Genomic DNA was extracted from the fresh mycelia, and the Ezup Column Fungi Genomic
DNA Purification Kit (Sangon Biotech, Shanghai, P. R. China) was used to processed it following
the manufacturer’s instructions.
Primers of LR0R and LR5 (Vilgalys & Hester 1990), NS1 and NS4 (White et al. 1990) were
used for the amplification of large subunit rDNA (LSU) and small subunit rDNA (SSU) respectively.
Translation elongation factor 1-α gene (TEF 1-α) and RNA polymerase II second largest subunit gene
(RPB2) were amplified by the primers of EF1-983F and EF1-2218R (Rehner 2001), fRPB2-5f and
fRPB2-7cr (Liu et al. 1999) respectively.
DNA amplification procedure was performed by Polymerase Chain Reaction (PCR) in a 50
μl reaction volume, which contains 19 μl Distilled-Deionized-water, 25 μl of 2 Power Taq PCR
Master Mix (TIANGEN Co., China), 2 μl of DNA template and 2 μl of each forward and reverse
primers. The PCR thermal cycle program of LSU, SSU and TEF1-α gene amplifications were
provided as: initially 94 oC for 3 minutes, followed by 40 cycles of denaturation at 94 oC for 45
seconds, annealing at 56 oC for 50 seconds, elongation at 72 oC for 1 minute, and a final extension at
72 oC for 10 minutes. The PCR thermal cycle program for RPB2 genes was provided as: initially 95
oC for 5 minutes, followed by 40 cycles of denaturation at 95 oC for 1 minute, annealing at 52 oC for
2 minutes, elongation at 72 oC for 90 seconds, and a final extension at 72 oC for 10 minutes. The
quality of PCR products was checked by using 1.2% agarose gel electrophoresis stained with
552
ethidium bromide and then sent to sequence at Invitrogen Biotechnology Co., Ltd (Shanghai, P. R.
China). Newly generated sequences have been submitted to GenBank.
Sequence alignment and phylogenetic analyses
Newly generated sequences were checked and combined in the program of BioEdit v.7.1.3
(Hall 1999). Then, a BLAST search with the LSU sequence in GenBank was performed to reveal the
preliminary identification, and additional sequences were downloaded based on their identities and
related publications. Single gene sequence alignments were processed in MAFFT v. 7.215 (Katoh &
Standley 2013: http://mafft.cbrc.jp/alignment/server/index.html) respectively and edited manually
where necessary to minimize the number of uninformative gaps in BioEdit v.7.2. The program of
MEGA v.6.6 (Tamura et al. 2013) was used to concatenate the individual datasets into a combined
dataset. And the data were converted from fasta to nexus format for Bayesian analysis in ClustalX2
v.1.83 (Thompson et al. 1997) or PHYLIP format for RAxML analysis in the online program ALTER
(http://sing.ei.uvigo.es/ALTER/).
Maximum likelihood (ML) analysis with 1000 bootstrap replicates was run in the
RAxMLGUI v. 1.5b1 program (Silvestro & Michalak, 2012), and the default algorithm was used
from a random starting tree for each replicate. The number of replications was inferred using the
stopping criterion. Branches of bootstrap values greater than 75% were shown in the tree. The final
tree was selected among suboptimal trees from each replicate by comparing likelihood scores under
the GTR+GAMMA substitution model.
Bayesian analysis was performed by using MrBayes v. 3.0b4 (Huelsenbeck & Ronquist
2001). The best-fit model of evolution was estimated in MrModeltest 2.3 (Nylander 2004). Posterior
probabilities (PP) (Rannala & Yang 1996, Zhaxybayeva & Gogarten 2002) were determined by
Markov Chain Monte Carlo sampling (MCMC) in MrBayes v. 3.0b4. Six simultaneous Markov
chains were run for 1000000 generations and trees were sampled every 100th generation (resulting
in 10000 total trees). The first 2000 trees, representing the burn-in phase of the analyses, were
discarded and the remaining 8000 trees used for calculating posterior probabilities (PP) in the
majority rule consensus tree. The branches, which posterior probabilities with those equal or greater
than 0.95, were thickened in Fig. 1.
The final layout of phylogenetic tree was visualized with TreeView v. 1.6.6 (Page 1996), and
edit by using Adobe Illustrator CS5 (Adobe Systems Inc., USA).
Results
Phylogenetic analysis
The LSU, SSU, TEF1-α and RPB2 dataset was combined and comprised 25 taxa with
Westerdykella ornata (CBS 379.55) as the outgroup taxon. The dataset comprised 3,677 characters
(LSU-851, SSU-982, TEF1-α-919, RPB2-916) after alignment, of which 2,866 characters are
constant, and 644 characters are parsimony-informative, while 167 variable characters are
parsimony-uninformative in the maximum parsimony (MP) analysis. The best scoring RAxML tree
is shown in Fig. 1. The optimal tree (not shown) generated by Bayesian analysis had a similar
topology with the RAxML tree.
Most of sequence data for this study are selected from Dai et al. (2017) and Hyde et al. (2016),
and most of other families, which are phylogenetically close to this group, are selected from previous
studies (Hyde et al. 2013, Liu et al. 2014). The results show that the two new taxa are placed in the
genus Occultibambusa. Occultibambusa jonesii is phylogenetically close to O. aquatica with high
support (MLBS 97/ BIPP 1.0), and O. maolanensis clusters with O. fusispora with good support
(MLBS 85/ BIPP 0.99). Moreover, all Occultibambusa species formed a well-supported (MLBS 83/
BIPP 1.0) clade in the family of Occultibambusaceae.
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Table 1 GenBank accession numbers of sequences used in phylogenetic analyses. New sequences
from this study are in bold.
Species name
Strain No.
GenBank accession number
LSU SSU TEF1-α RPB2
Biatriospora mackinnonii
CBS 674.75
KF015612
GQ387552
KF407986 KF015703
Biatriospora marina
CY 1228
GQ925848
GQ925835
GU479848 GU479823
Biatriospora sp.
CCF 4485
LN626683
LN626677
LN626671 LN626663
Dendryphion europaeum
CPC 22943
KG869203
---
--- ---
Neooccultibambusa
chiangraiensis
MFLUCC 12-
0559
KU764699
KU712458
--- ---
Neooccultibambusa sp.
MFLUCC 12-
0564
---
---
KU872761 ---
Neoroussoella bambusae
MFLUCC 11-
0124
KJ474839
---
KJ474848 KJ474856
Occultibambusa aquatica
MFLUCC 11-
0006
KX698110
KX698112
--- ---
Occultibambusa bambusae
MFLUCC 11-
0394
KU863113
KU872117
KU940194 KU940171
Occultibambusa bambusae
MFLUCC 13-
0855
KU863112
KU872116
KU940193 KU940170
Occultibambusa fusispora
MFLUCC 11-
0127
KU863114
---
KU940195 KU940172
Occultibambusa jonesii
GZCC 16-
0117
KY628322
KY628324
KY814756 KY814758
Occultibambusa maolanensis
GZCC 16-
0116
KY628323
KY628325
KY814757 KY814759
Occltibambusa pustulata
MFLUCC 11-
0502
KU863115
KU872118
--- ---
Paradictyoarthrinium
diffractum
MFLUCC 13-
0466
KP744498
KP753960
--- ---
Paradictyoarthrinium
tectonicola
MFLUCC 13-
0465
KP744500
KP753961
--- ---
Roussoella hysterioides
HH 26988
AB524622
AB524481
AB539115 AB539102
Roussoella nitidula
MFLUCC 11-
0182
KJ474843
---
KJ474852 KJ474859
Roussoella nitidula
MFLUCC 11-
0634
KJ474842
---
KJ474851 KJ474858
Roussoella pustulans
KT 1709
AB524623
AB524482
AB539116 AB539103
Seriascoma didymospora
MFLUCC 11-
0179
KU863116
---
KU940196 KU940173
Seriascoma didymospora
MFLUCC 11-
0194
KU863117
---
KU940197 KU940174
Torula herbarum
CBS 111855
KF443386
KF443391
KF443403 KF443396
Torula hollandica
CBS 220.69
KF443384
---
--- ---
Westerdykella ornata
CBS 379.55
GU301880
GU296208
GU349021 GU371803
Abbreviation: CBS: Centraalbureau voor Schimmelcultures, The Netherlands; CPC: Collection of
Pedro Crous housed at CBS; GZCC: Guizhou culture collection, Guizhou, China; MFLUCC: Mae
Fah Luang University Culture Collection, Chiang Rai, Thailand; KT: K. Tanaka.
Taxonomy
Occultibambusa jonesii J.F. Zhang, J.K. Liu, K.D. Hyde & Z.Y. Liu, sp. nov. Fig. 2
Index Fungorum number: IF 552743
Faces of fungi number: FoF 02873
Etymology – Named in honour of E.B. Gareth Jones for his contributions to tropical mycology.
Holotype – GZAAS 16-0162
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Saprobic on dead bamboo culms, forming dark, raised spots on the host surface. Sexual morph
Ascostromata 196–236 µm high, 200–260 µm diam, immersed to erumpent, solitary to gregarious,
subglobose, ostiolate, papillate, coriaceous, flattened at the base. Peridium up to 10–52
Fig. 1 – Maximum likelihood phylogenetic tree by RAxML (GTR+G model) analysis based on
combined LSU, SSU, TEF1-α and RPB2 sequence data. ML values (≥ 75%) resulting from 1000
bootstrap replicates are shown near the nodes and branches with Bayesian posterior probabilities (PP)
greater than 0.95 are in bold. The original isolate numbers are noted after the species names. The tree
is rooted to Westerdykella ornata (CBS 379.55), and the scale bar shows 0.1 changes.
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Fig. 2 – Occultibambusa jonesii (holotype, GZAAS 16-0162). a Appearance of ascostromata on dead
bamboo culms. b Vertical section through ascostroma. c Section through peridium. d
Pseudoparaphyses. e-h Asci with ascospores. i-m Ascospores. Scale bars: b = 100 µm, c = 30 µm, d-
h = 20 µm, i-m = 10 µm
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µm wide, thin at the base and becoming wider laterally, composed of several layers of dark brown
cells, arranged in a textura angularis, and the outermost layer intermingled with host tissue.
Hamathecium comprising dense, 2–3 µm wide, pseudoparaphyses, which anastomose above and
between the asci, embedded in a gelatinous matrix. Asci (65–)75–89(–105) 13.5–19 µm ( = 85
16.5 µm, n = 20), 8-spored, bitunicate, fissitunicate, broadly cylindrical to clavate, short pedicellate,
apically rounded to truncate, with an ocular chamber. Ascospores 27–33.5 5.5–6.5 µm ( = 29.5
6 µm, n = 20), 1–3-seriate, 2-celled, constricted at the septum, and the upper cell swollen near the
septum, inequilateral-fusiform, slightly curved, hyaline and guttulate when young and becoming
brown to grayish when mature, wall smooth, without any mucilaginous sheath and appendages.
Asexual morph – Undetermined.
Culture characters – Ascospores geminating on WA within 12 hours. Colonies reaching 35 mm
diameter on PDA in three weeks at 25 C, circular, dense, regular at the margin, raised at the center,
gray from above and dark olive-green to black from below.
Material examined – CHINA, Guizhou Province, Maolan Town, on dead bamboo culms, 20
July 2016, J.F. Zhang, MLC’-12, (GZAAS 16-0162, holotype); ex-type living culture, GZCC 16-
0117; Ibid., 10 November 2016, J.F Zhang (HKAS96379); living culture KUMCC 17-0136.
Occultibambusa maolanensis J.F. Zhang, J.K. Liu, K.D. Hyde & Z.Y. Liu, sp. nov. Fig. 3
Index Fungorum number: IF 552744
Faces of fungi number: FoF 02874
Etymology – Refers to the holotype was collected from Maolan Town.
Holotype – GZAAS 16-0161
Saprobic on dead bamboo culms, forming dark, rounded spots on the host surface. Sexual
morph – Ascostromata 544–600 µm diameter, solitary to gregarious, immersed under the epidermis,
subglobose, coriaceous, slightly conical in vertical section, and flattened at the base, ostiolate, with
a short, rounded, shiny, black papilla. Peridium up to 20–42 µm laterally composed of several layers
of brown cells, becoming thin-walled and hyaline towards the centrum, arranged in a textura
angularis, thick and darkly pigmented around ostiole, intermingled with host tissue. Hamathecium
comprising dense, 1.5–2.4 µm wide, hypha-like pseudoparaphyses, branched and swollen towards
the terminal cells, anastomosing above and between the asci, embedded in a gelatinous matrix. Asci
(66–)77–85(–94) 17–20(–24) µm ( = 81 20 µm, n = 20), 8-spored, bitunicate, fissitunicate,
broadly cylindrical to clavate, short pedicellate, apically rounded to truncated with a visible ocular
chamber (2.5–3.5 µm wide). Ascospores 25–31 8–10 µm ( = 28 9 µm, n = 30), 2–4-seriate, 2-
celled, and moderately constricted at the septum, inequality-fusiform, apical cells 14–18 µm, basal
cells 11–15 µm, slightly curved, hyaline and guttulate when young and become light brown when
mature, wall smooth, without any mucilaginous sheath and appendages. Asexual morph –
Undetermined.
Culture characters – Ascospores geminating on WA within 24 hours. Colonies reaching 30 mm
diameter on PDA in three weeks at 25 °C, circular, dense, regular at the margin, gray from above and
black from below.
Specimens examined – CHINA, Guizhou Province, Maolan Town, on dead bamboo culms, 8
July 2015, J.F. Zhang, MLC-29, (GZAAS 16-0161, holotype); ex-type living culture, GZCC 16-
0116; Ibid., 10 November 2016, J.F Zhang (HKAS96380); living culture KUMCC 17-0137.
Discussion
The taxa that occur on bamboo are rather unique, often family specific grouping that appear
to have a considerable diversity (Hyde et al. 2002, Liu et al. 2011, Jaklitsch et al. 2015, Dai et al.
2017). In this paper, we introduce two new species, Occultibambusa jonesii and O. maolanensis from
bamboo, with molecular and morphological support. Occultibambusa jonesii is phylogenetically
close to O. aquatica, but can be distinguished from it by its larger asci (65–105 13.5–19 µm vs.
73–86 9–13 µm), longer ascospores (27–33.5 µm vs. 19–25 µm), and the new taxa also lacks a
mucilage sheath surrounding the ascospores. Occultibambusa maolanensis clusters
x
x
x
x
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Fig. 3 – Occultibambusa maolanensis (holotype, GZAAS 16-0161). a Appearance of ascostromata
on dead bamboo culms. b Rounded, shiny black papilla. c Vertical section through ascostroma. d
Section through peridium. e Pseudoparaphyses. f-h Asci with ascospores. i-l Ascospores. Scale bars:
a = 500 µm, b = 200 µm, c = 100 µm, d = 10 µm, e-n = 20 µm
with O. fusispora in a well-supported clade in the phylogenetic analysis, but they can be distinguished
readily by the difference in appearance of ascostromata, the wider asci (17–24 µm vs. 11–16 µm)
and larger ascospores (25–31 8–10 µm vs. 20–26 5–6.5 µm). Both species have
558
pseudoparaphyses embedded in a gelatinous matrix and anastomose between and above the asci and
are more like trabeculae in Occultibambusa maolanensis, but typical of cellular pseudoparaphyses in
O. jonesii. Liew et al. (2000) show that the nature of pseudoparaphyses had little relevance above the
family level, while in this study different types of pseudoparaphyses are found even in the same genus
(Figs 2d, 3e).
The family of Occultibambusaceae includes four genera: Neooccultibambusa,
Occultibambusa, Seriascoma and Versicolorisporium, however, the phylogenetic placement of
Versicolorisporium is not well-resolved. Its placement is not stable and when used in analyses it
affects the molecular placements of genera (results not shown). Therefore, we excluded the molecular
data of Versicolorisporium in our phylogenetic analysis. The two new taxa are both morphologically
and phylogenetically with described Occultibambusa species, and the lack of Versicolorisporium
sequence data has no effect on phylogenetic relationships of species in Occultibambusa.
Acknowledgements
The Research of Featured Microbial Resources and Diversity Investigation in Southwest
Karst area (Project No. 2014FY120100) is gratefully thanked for financial support. We would like to
thank Hai-Yan Ran for the molecular work. Jian-Kui Liu would like to thank Science and Technology
Foundation of Guizhou Province (LH [2015]7061) and National Natural Science Foundation of
China (NSFC 31600032).
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