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Molecular phylogeny and morphology of Cunninghamella guizhouensis sp.

nov. (Cunninghamellaceae, Mucorales), from soil in Guizhou, China

Article  in  Phytotaxa · August 2020

DOI: 10.11646/phytotaxa.455.1.4

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 Phytotaxa 455 (1): 031–039 ISSN 1179-3155 (print edition)
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Article PHYTOTAXA
Copyright © 2020 Magnolia Press ISSN 1179-3163 (online edition)

https://doi.org/10.11646/phytotaxa.455.1.4

Molecular phylogeny and morphology of Cunninghamella guizhouensis sp. nov.

(Cunninghamellaceae, Mucorales), from soil in Guizhou, China
ZHI-YUAN ZHANG1,4, YI-XUAN ZHAO1,5, XIN SHEN1,6, WAN-HAO CHEN2,7, YAN-FENG HAN1,8*, JIAN-
ZHONG HUANG3,9 & ZONG-QI LIANG1,10
1
Institute of Fungus Resources, Department of Ecology, College of Life Sciences, Guizhou University, Guiyang 550025, Guizhou, China
2
Department of Microbiology, Guiyang College of Traditional Chinese Medicine, Guiyang 550025, Guizhou, China.
3
Engineering Research Center of Industrial Microbiology, Ministry of Education, Fujian Normal University, Fuzhou 350108, Fujian,
China.
4

zzymetaC16@163.com; https://orcid.org/0000-0003-2031-7518
5

yxzhao357@163.com; https://orcid.org/0000-0002-7755-5907
6

olivepps@163.com; https://orcid.org/0000-0002-3129-5708
7

cwhisaria@163.com; https://orcid.org/0000-0001-7240-6841
8

swallow1128@126.com; https://orcid.org/0000-0002-8646-3975
9

hjz@fjnu.edu.cn; https://orcid.org/0000-0002-1162-544X
10

zqliang2@hotmail.com; https://orcid.org/0000-0003-2867-2231
*
Corresponding author:
swallow1128@126.com

Abstract

During a survey of keratinolytic fungi in China, three Cunninghamella strains were isolated. Phylogenetic analyses of
ITS and ITS+LSU+EF-1α sequence data showed that these strains constitute a new species related to C. blakesleeana, C.
bigelovii, C. multiverticillata and C. phaeospora. The new species differs from C. multiverticillata and C. phaeospora in
the shape and size of its teminal and lateral vesicles and can be distinguished from C. blakesleeana and C. bigelovii by the
absent of zygosporangia, and the shape and size of it sporangioles. The results of phylogenetic and morphological analyses
indicate that the three strains are a new species of Cunninghamella. Descriptions and illustrations of this novel species are
provided in this paper.

Keywords: molecular phylogeny, taxonomy, 1 new species, Mucoromycetes

Introduction

Matruchot (1903) established Cunninghamella Matr., the type genus of the Cunninghamellaceae (Mucoromycota:
Mucorales) (Spatafora et al. 2016). Zheng & Chen (2001) monographed Cunninghamella based on morphology and
molecular data, and recognized 12 different species and three varieties: C. bertholletiae Stadel, C. binariae R.Y. Zheng,
C. blakesleeana Lendn, C. clavate R.Y. Zheng & G.Q. Chen, C. echinulate (Thaxt.) Thant. ex Blakeslee, C. echinulate
var. antarctica (Caretta & Piont) R.Y. Zheng & G.Q. Chen, C. echinulate var. nodosa R.Y. Zheng, C. echinulate var.
verticillate (F.S. Paine) R.Y. Zheng & G.Q. Chen, C. elegans Lendn., C. homothallica Komin. & Tubaki, C. intermedia
K.B. Deshp. & Mantri, C. multiverticillata R.Y. Zheng & G.Q. Chen, C. phaeospora Boedijn, C. septate R.Y. Zheng,
and C. vesiculosa P.C. Misra). They also re-described all species (Zheng & Chen 2001). Recently, C. bigelovii Z.H.
Xin, Y.Hui Zhao & Hui Wang and C. gigacellularis A.L. Santiago, C.L. Lima & C.A.F. de Souza were introduced on
the basis of phylogenetic analyses and morphological characteristic (Guo et al. 2015, Hyde et al. 2016). Currently,
Cunninghamella consists of 17 species.
Cunninghamella species are generally recognized on the basis of the morphological characteristics of their
sporangial and zygosporic stages, maximum growth temperature, mating compatibility and zygospore formation
processes (Guo et al. 2015). Liu et al. (2001) amplified the ITS regions of all species and varieties of the genus
and established a consensus tree that was topologically consistent with morphological observations. In recent years,
molecular analysis has been used as an auxiliary tool to delimit species, thereby resulting in an increase of the number

Accepted by Sinang Hongsanan: 25 Jul. 2020; published: 5 Aug. 2020 31

of new taxa (Guo et al. 2015, Hyde et al. 2016). During investigations of keratinolytic fungi in southwest China, three
strains of Cunninghamella were discovered and identified as a new species base on morphological observation and
multi-locus phylogenetic analysis. This paper provides a phylogenetic tree, descriptions, and illustrations of this novel
species.

Materials & methods

Fungal isolation and morphology

Soil samples were collected from the green grounds of the affiliated hospital of Guizhou Medical University, Guiyang
City, Guizhou Province, China, according to the methods described by Zhang et al. (2019a, b). Briefly, sterile chicken
feathers and human hairs were combined with the soil samples. Samples were placed in sterile Petri dishes, which
were moistened with ddH2O. The baited soil-sample Petri dishes were incubated at 25 °C for 1 month and remoistened
as necessary. Next, 2 g portions of sample were added to test tubes containing 9 mL of ddH2O. The mixture was then
diluted to 1:104 and 1 mL of suspension was evenly spread on plates containing Sabouraud’s dextrose agar (SDA; 10
g peptone, 40 g dextrose, 20 g Agar, 3.3 mL of 1% Bengal red aqueous solution, and 1 L ddH2O) with anti-bacterial
chloramphenicol and cycloheximide medium. Plates were incubated at 25 °C for 5 days. The axenic strains were then
transferred to potato dextrose agar (PDA, Shanghai Bio-way technology Co., Ltd, China) plates for purification and
for retesting of test-tube slants for storage at 4 °C.
Dried holotype, ex-holotype and ex-isotype strains were deposited in the Institute of Fungus Resources, Guizhou
University (formally Herbarium of Guizhou Agricultural College; code GZAC), Guiyang City, Guizhou, China. The
pure strains were incubated on potato extract agar (PDA) at 25 °C in darkness. Macroscopic characterization was
performed after 5 days of incubation, and the colony colors (surface and reverse) were observed. Photomicrographs of
diagnostic structures were made using an optical microscope (OM, DM4 B; Leica, Germany) following pretreatment
with ddH2O.

DNA extraction, PCR amplification, sequencing

DNA extraction was carried out according to Zhang et al. (2019c). PCR amplifications of ITS, LSU and EF-1α
regions was conducted using the following primers: ITS1/ITS4 for ITS, NL1/LR3 for LSU, MEF-1 / MEF-4 (5ʹ-
ATGGGTAAAGA[A/G]AAGACTCACG-3ʹ)/ (5ʹ-ATGACACC[A/G]ACAGCGACGGTTTG-3ʹ) for EF-1α (White
et al. 1999, O’Donnell 1993, O’Donnell et al. 2001). The resulting products were purified, sequenced and edited by
BioSune, Ltd., (Shanghai, China) using the same primers. The new sequences were submitted to the GenBank database
(Table 1).

Phylogenetic analyses

Raw sequences were assembled using Lasergene version 6.0 software (DNASTAR). Sequences data of closely related
Cunninghamella spp. were selected from data previously published by Guo et al. (2015), Walther et al. (2013) and
Yu et al. (2015), and then downloaded from GenBank for molecular phylogenetic analyses (Table 1). Sequences were
aligned using MAFFT v.7.407 (Katoh & Standley 2013), and the alignment was checked in MEGA 6.06 (Tamura et
al. 2013). A dataset of concatenated ITS+LSU+EF-1α sequences was constructed by SequenceMatrix v.1.7.8 (Vaidya
et al. 2011).
The two datasets (ITS and ITS, LSU and EF-1α) were analyzed by Bayesian inference (BI) using MrBayes
v.3.2 (Ronquistet al. 2012). For analysis of the concatenated dataset, the most appropriate model was obtained
using Modeltest v3.7 (Posada & Crandall 1988). After BI analysis, the output of each run was examined with the
program Tracer v1.5 (Drummond & Rambaut 2007) to determine the burin-in interval and confirm that both runs had
converged. In addition, Maximum likelihood (ML) analyses were conducted using IQ-TREE v. 1.6.11 (Nguyen et al.
2015). The best-fit model of substitution for each locus was estimated with the ModelFinder function of IQ-TREE
(Kalyaanamoorthy et al. 2017) based on the Bayesian Information Criterion (BIC). Bootstrapping was performed using
the ultrafast bootstrap approximation (Minh et al. 2013) with 1,000 replicates. A bootstrap support (BS) value ≥95%
was considered as statistically significant. The sequence alignments were deposited in TreeBASE (www.treebase.org,
S25717).

32 • Phytotaxa 455 (1) © 2020 Magnolia Press ZHANG ET AL.

TABLE 1. Sequences information of isolates used in this study.
Species Strains ITS LSU EF-1α
Cunninghamella bertholletiae CBS 190.84 JN205878 HM849701 KJ156485
C. bertholletiae CBS 373.95 JN205873 - KJ156497
C. bertholletiae CBS 693.68 JN205871 JN206600 KJ156490
C. bertholletiae CBS 779.68 JN205874 JN206599 KJ156471
C. binariae NRRL 1375 T AF254935 - -
C. binariae CBS 158.28 JN205888 JN206602 KJ156486
C. binariae CBS 481.66 JN205889 JN206603 KJ156495
C. bigelovii CGMCC 8094 KJ013403 KJ013405 KJ395944
C. blakesleeana CBS 133.27 T JN205865 - KJ156479
C. blakesleeana CBS 177.36 JN205868 - KJ156483
C. blakesleeana CBS 433.84 JN205867 - KJ156482
C. blakesleeana CBS 782.68 JN205869 JN206601 KJ156478
C. clavata CBS 362.95 JN205891 - KJ156473
C. clavata CBS 100178 JN205890 JN206604 KJ156477
C. echinulata CBS 156.28 NT JN205895 HM849702 KJ156500
C. echinulata CBS 656.85 JN942996 JN206598 KJ156491
C. echinulata CBS 766.68 JN205894 - KJ156496
C. echinulata var. antarctica CBS 545.75 T JN205893 JN206597 KJ156492
C. echinulata var. nodosa Cu-34 T AF346407 - -
C. echinulata var. verticillata CBS 595.68 NT AF254937 - -
C. echinulata var. verticillata FSU319 - EU736313 EU736259
C. elegans CBS 160.28 NT AF254928 - KJ156470
C. elegans CBS 167.53 JN205882 HM849700 KJ156494
C. elegans CBS 773.68 JN205887 - KJ156487
C. elegans CBS 781.68 JN205885 - KJ156501
C. gigacellularis URM 7400 KX238886 KX238889 -
C. gigacellularis URM 7400 KX238887 KX238890 -
C. gigacellularis URM 7400 KX238888 KX238891 -
C. homothallica IFO 6736 T AF254941 - -
C. homothallica CBS 168.53 JN205863 JN206605 KJ156498
C. guizhouensis GZUIFR-SX25 MN908596 MN908599 MN912633
C. guizhouensis GZUIFR-SX26 MN908597 MN908600 MN912634
C. guizhouensis GZUIFR-SX27 MN908598 MN908601 MN912635
C. intermedia IMI 200623 T AF254939 - -
C. intermedia CBS 347.69 JN205892 JN206606 -
C. multiverticillata Cu-137 T AF254933 - -
C. phaeospora CBS 692.68 NT JN205864 HM849697 -
C. septata Cu-230 T AF346408 - -
C. vesiculosa CBS 989.96 JN205897 HM849693 KJ156474
C. vesiculosa NRRL 3009 T AF254943 - -
Absidia glauca FSU660 AY944879 EU736302 EU736248
A. psychrophilia SYM0202 T JN942384 JN982947
Note: T=Ex-type, NT=Ex-neotype; New isolates are in bold; The line “-” represents the absence of sequence data in
GenBank.

MORPHOLOGY OF CUNNINGHAMELLA GUIZHOUENSIS Phytotaxa 455 (1) © 2020 Magnolia Press • 33

FIGURE 1. Phylogenetic tree of Cunninghamella constructed using the ITS sequences. Absidia glauca and A. psychrophilia were used
as out-group taxa. Numbers at nodes are Bayesian prior probabilities (left, BPP ≥0.75) and maximum likelihood bootstrap values (right,
MLBS ≥95%). New taxa are shown in bold and blue, and ex-type strains in bold.

34 • Phytotaxa 455 (1) © 2020 Magnolia Press ZHANG ET AL.

FIGURE 2. Phylogenetic tree based on Bayesian inference (BI) and Maximum likelihood (ML) analyses of a combined DNA data set of
ITS, LSU and EF-1α sequences. Absidia glauca and A. psychrophilia were used as out-group taxa. Numbers at nodes are Bayesian prior
probabilities (left, BPP ≥0.75) and maximum likelihood bootstrap values (right, MLBS ≥95%). New taxa are shown in bold and blue, and
ex-type strains in bold.

MORPHOLOGY OF CUNNINGHAMELLA GUIZHOUENSIS Phytotaxa 455 (1) © 2020 Magnolia Press • 35

Results

Phylogenetic analyses

The phylogenetic trees constructed using ITS dataset and ITS+LSU+EF-1α datasets were rooted with the same
outgroup taxa: Absidia glauca and A. psychrophilia. The ITS dataset included 41 strains (Table 1) and consisted of 552
characters including gaps. The BI and ML analyses of this dataset were based on GTR+I+G and TPM3+F+G4 nucleotide
substitution model, respectively. The three-locus combined dataset contained 1,769 characters with gaps (ITS: 552,
LSU: 667 and EF-1α: 550). GTR+I+G, GTR+I+G and GTR+G models were respectively used for BI analyses of ITS,
LSU and EF-1α partitions, while the corresponding models selected for ML analyses were TPM3u+F+I+G4 for ITS,
TIM3+F+R2 for LSU and TIM2e+R2 for EF-1α.
The topologies of BI and ML trees were almost identical except for several minor, statistically unsupported,
terminal rearrangements. In all phylogenetic trees, the three new strains (GZUIFR-SX25, GZUIFR-SX26 and GZUIFR-
SX27) clustered together with high support values (Bayesian posterior probability = 1 and MLBS = 100%).

Taxonomy

Cunninghamella guizhouensis Zhi.Y. Zhang, Y.F. Han & Z.Q. Liang, sp. nov. (FIG. 3)
MycoBank no.: MB 834099

Type:—CHINA. Guizhou Province: Guiyang City, the green ground of hospital affiliated of Guizhou Medical University (N 26°59′, E
106°71′), soil, October 6, 2017, Xin Shen, dried holotype GZAC SX25, ex-holotype GZUIFR-SX25.

FIGURE 3. Morphology of Cunninghamella guizhouensis sp. nov. A, B. Colony on PDA after 5 days at 25 °C (surface and reverse). C.
Long and slender pedicle. D, E. Sporangia. F. Longer sporophores. G, H. Branching sporophore. Bars: A–B = 10 mm, C–H = 10 μm.

Colony diameter on PDA at 2 days: 10–12mm at 15 °C; 25–26mm at 20 °C; 51mm at 25 °C; 50–55mm at 30 °C; 62–64
mm at 35 °C; 13–20 mm at 40 °C. The fastest growth temperature was approximately 35 °C. Culture characteristics:
Colonies fast-growing on PDA, reaching up to 71–76 mm in diameter and approximately 8–12 mm in height after 5
days of incubation at 25 °C; initially white, then gradually becoming pale gray. Reverse pale gray, like a laminated

36 • Phytotaxa 455 (1) © 2020 Magnolia Press ZHANG ET AL.

cloud. Micromorphology: Hyphae hyaline, branching, non-septate when young, septate with aging, 5.5–10 μm in
diameter. Sporophores hyaline and erect, straight or recumbent, smooth-walled, arising from aerial hyphae; branches
short, monopodial, verticillate, usually lateral. Septa in sporophores sometimes present at the base, near to the branches
of the sporophores. Vesicles of the main sporophores, smooth-walled, globose to subglobose, 11.5–22.5 μm ( = 18
× 15 μm, n = 50), lateral vesicles smooth-walled, sometimes with long and slender pedicels, globose to subglobose,
9–20 μm ( = 13.5 × 11.5 μm, n=50). Sporangioles having densely echinulate with short, pointed spines 3 μm in
length, globose to subglobose, 9.5-14 μm ( = 11 × 10.5 μm, n = 50). Zygosporangia stage and Chlamydospores not
observed.
Etymology:—Refers to the region from which the fungus was isolated.
Additional specimens examined:—The ex-isotype strains GZUIFR-SX26 and GZUIFR-SX27 were isolated
from soil at the hospital affiliated with Guizhou Medical University, Guiyang City, Guizhou Province, on October 6,
2017 by Xin Shen.
Known distribution:—Guiyang City, Guizhou Province, China.

Discussion

Currently, mycologists give overwhelming importance to molecular data for justifying the establishment of a new
taxon or assessing species relationships (Bauer et al. 2015, Jeewon & Hyde 2016, Maharachchikumbura et al. 2016).
In particular, the use of sequences derived from type specimen is essential to infer a robust phylogenetic framework
on which a natural classification can be established (Hu et al. 2016). Classical morphological classification, however,
is generally accepted as still indispensable. In this study, our new species from China, Cunninghamella guizhouensis,
was characterized on the basis of molecular phylogenetic analyses and morphological characters.
Phylogenetically, ITS, LSU and EF-1α sequences have been applied in the delimitation of Cunninghamella (Guo
et al. 2015, Hyde et al. 2016). Morphologically, members of the genus Cunninghamella are generally distinguished
according to their sporangia and zygosporic stages, maximum growth temperature, mating compatibility and zygospore
formation processes (Zheng & Chen 2001). Our new isolates are phylogenetically related to C. blakesleeana, C.
bigelovii, C. multiverticillata and C. phaeospora, but can be morphologically distinguished from those species. C.
blakesleeana differs from C. guizhouensis by possessing zygosporangia and ovoid, ellipsoid sporangioles, whereas C.
bigelovii and C. guizhouensis can be distinguished by the presence of spherical to ellipsoid sporangioles in the former
(Zheng and Chen 2001). Furthermore, C. multiverticillata is distinguished from C. guizhouensis by the presence of
sporophores that are more often monopodially or verticillately branched, or, alternatively, by the presence of both
monopodially and verticillately branched sporophores that are either single, in pairs, or in 1–3 whorls of 3–8 (Zheng
& Chen 2001). In addition, C. phaeospora is distinguished from C. guizhouensis by the presence of zygosporangia
and ovoid, subglobose to irregularly shaped vesicles (Zheng & Chen 2001). The observed morphological features
are therefore consistent with the molecular phylogenetic analysis, which indicated that these new isolates are a new
species in the genus Cunninghamella, described here as C. guizhouensis.

Acknowledgements

This work was financially supported by Key-Area Research and Development Program of GuangDong Province
(2018B020205003); Ministry of Science and Technology of China (2013FY110400), “Hundred” Talent Projects of
Guizhou Province (Qian Ke He [2020]6005), the National Natural Science Foundation of China (31460010), Construction
Program of Biology First-class Discipline in Guizhou (GNYL[2017]009), and the Graduate Innovation Fund Project
of Guizhou Province (YJSCXJH(2019)026). We thank Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac),
for editing the English text of a draft of this manuscript and appreciate the help of the editor Hongsanan.

MORPHOLOGY OF CUNNINGHAMELLA GUIZHOUENSIS Phytotaxa 455 (1) © 2020 Magnolia Press • 37

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