Taxonomy and Phylogeny of Four New Species in Absidia (Cunninghamellaceae, Mucorales) From China

Abstract

Four new species within the genus Absidia, A. globospora, A. medulla, A. turgida, and A. zonata, are proposed based on a combination of morphological traits, physiological features, and molecular evidences. A. globospora is characterized by globose sporangiospores, a 1.0-to 3.5-µm-long papillary projection on columellae, and sympodial sporangiophores. A. medulla is characterized by cylindrical to oval sporangiospores, a 1.0-to 4.5-µm-long bacilliform projection on columellae, and spine-like rhizoids. A. turgida is characterized by variable sporangiospores, up to 9.5-µm-long clavate projections on columellae, and swollen top of the projection and inflated hyphae. A. zonata is characterized by cylindrical to oval sporangiospores, a 2.0-to 3.5-µm-long spinous projection on columellae, and as many as eight whorled sporangiophores. Phylogenetic analyses based on sequences of internal transcribed spacer rDNA and D1-D2 domains of LSU rDNA support the novelty of these four species within the Absidia. All new species are illustrated, and an identification key to all the known species of Absidia in China is included.

Full text

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ORIGINAL RESEARCH
published: 04 August 2021
doi: 10.3389/fmicb.2021.677836
Edited by:
Hyang Burm Lee,
Chonnam National University,
South Korea
Reviewed by:
Kerstin Voigt,
Friedrich Schiller University Jena,
Germany
Thuong Nguyen,
Chonnam National University,
South Korea
*Correspondence:
Xiao-Yong Liu
liuxiaoyong@im.ac.cn
Chang-Lin Zhao
fungichanglinz@163.com
Specialty section:
This article was submitted to
Microbe and Virus Interactions with
Plants,
a section of the journal
Frontiers in Microbiology
Received: 10 March 2021
Accepted: 12 July 2021
Published: 04 August 2021
Citation:
Zong T-K, Zhao H, Liu X-L,
Ren L-Y, Zhao C-L and Liu X-Y (2021)
Taxonomy and Phylogeny of Four
New Species in Absidia
(Cunninghamellaceae, Mucorales)
From China.
Front. Microbiol. 12:677836.
doi: 10.3389/fmicb.2021.677836
Taxonomy and Phylogeny of Four
New Species in Absidia
(Cunninghamellaceae, Mucorales)
From China
Tong-Kai Zong1,2, Heng Zhao2,3, Xiao-Ling Liu2,3, Li-Ying Ren4, Chang-Lin Zhao1,5*and
Xiao-Yong Liu2*
1Key Laboratory for Forest Resources Conservation and Utilization in the Southwest Mountains of China, Ministry
of Education, Southwest Forestry University, Kunming, China, 2State Key Laboratory of Mycology, Institute of Microbiology,
Chinese Academy of Sciences, Beijing, China, 3College of Life Science, University of Chinese Academy of Sciences, Beijing,
China, 4College of Plant Protection, Jilin Agricultural University, Changchun, China, 5College of Biodiversity Conservation,
Southwest Forestry University, Kunming, China
Four new species within the genus Absidia,A. globospora,A. medulla,A. turgida,
and A. zonata, are proposed based on a combination of morphological traits,
physiological features, and molecular evidences. A. globospora is characterized by
globose sporangiospores, a 1.0- to 3.5-µm-long papillary projection on columellae,
and sympodial sporangiophores. A. medulla is characterized by cylindrical to oval
sporangiospores, a 1.0- to 4.5-µm-long bacilliform projection on columellae, and spine-
like rhizoids. A. turgida is characterized by variable sporangiospores, up to 9.5-µm-long
clavate projections on columellae, and swollen top of the projection and inflated hyphae.
A. zonata is characterized by cylindrical to oval sporangiospores, a 2.0- to 3.5-µm-
long spinous projection on columellae, and as many as eight whorled sporangiophores.
Phylogenetic analyses based on sequences of internal transcribed spacer rDNA and
D1–D2 domains of LSU rDNA support the novelty of these four species within the
Absidia. All new species are illustrated, and an identification key to all the known species
of Absidia in China is included.
Keywords: morphology, molecular phylogeny, taxonomy, Mucoromycetes, Mucoromycota
INTRODUCTION
The genus Absidia Tiegh. (Cunnighamellaceae, Mucorales, Mucoromycetes, Mucoromycota) was
proposed by van Tieghem (1876).Absidia members are ubiquitous in soil and also often associated
with warm decaying plant matter, such as compost heaps. Some Absidia can be used to produce
chitin, chitosan, and chitooligosaccharides (Kaczmarek et al., 2019) and hydrocortisone (Chen
et al., 2020). Absidia species typically have sporangiophores arising from stolons, rhizoids never
opposite the sporangiophores, pyriform sporangia and their deliquescent wall, obvious apophyses,
a septum beneath the sporangium, and zygospores surrounded by appendages from the suspensors
(Hoffmann et al., 2007;Hoffmann, 2010).
The classification and circumscription of the Absidia have been debated since it was described.
According to zygospore morphology, Hesseltine and Ellis (1964) divided Absidia into two
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Zong et al. Four New Species of Absidia
subgenera, the subgenus Absidia and the subgenus Mycocladus
(Beauverie) Hesselt. & J.J. Ellis. Different from the former, the
subgenus Mycocladus does not form any appendages from the
suspensors of zygospores. This classification framework was
followed by Schipper (1990), who further divided the subgenus
Absidia into six groups. However, this kind of delimitation
are not accepted nowadays, and six genera are synonymized
with the genus Absidia instead (Hawksworth et al., 1995).
They are Tieghemella Berl. & De Toni 1888, Mycocladus
Beauverie 1900, Lichtheimia Vuill 1903, Proabsidia Vuill 1903,
Pseudoabsidia Bainier 1903, and Protoabsidia Naumov 1935.
Among these synonyms, Lichtheimia,Mycocladus,Pseudoabsidia,
and Protoabsidia lack appendages.
Recently, a combined study of molecular phylogenetics,
morphology, and physiology has provided a more reliable
delimitation among Absidia species (Hoffmann et al., 2007),
where Absidia was classified into three groups: (1) the
thermotolerant species with an optimal growth temperature of
37–45◦C, which were then transferred into the genus Lichtheimia
(Hoffmann et al., 2009a); (2) the mesophilic species with an
optimal growth temperature of 25–34◦C, which have been
accepted up to now as Absidia sensu stricto; and (3) the
mycoparasitic species, potential to parasitize other mucoralean
hosts with optimal growth temperatures below 30◦C, which were
then transferred into the genus Lentamyces Kerst. Hoffm. & K.
Voigt (Hoffmann and Voigt, 2008). Currently, 37 species have
been reported worldwide in Absidia (Hesseltine and Ellis, 1961,
1964, 1966;Ellis and Hesseltine, 1965, 1966; Index Fungorum1).
Among these species, 13 were reported in the last decade
using the strategy of combing morphology, physiology, and
phylogeny: Absidia caatinguensis D.X. Lima and A.L. Santiago,
Absidia cornuta D.X. Lima, C.A. de Souza, H.B. Lee, and A.L.
Santiago; Absidia jindoensis Hyang B. Lee, and T.T.T. Nguyen;
Absidia koreana Hyang B. Lee, Hye W. Lee, and T.T. Nguyen;
Absidia multispora T.R.L. Cordeiro, D.X. Lima, Hyang B. Lee,
and A.L. Santiago; Absidia panacisoli T. Yuan Zhang, Ying Yu,
He Zhu, S.Z. Yang, T.M. Yang, Meng Y. Zhang, and Yi X.
Zhang; Absidia pararepens Jurjeviæ, M. Kolaøík, and Hubka;
Absidia pernambucoensis D.X. Lima, C.M. Souza-Motta, and A.L.
Santiago; Absidia saloaensis T.R.L. Cordeiro, D.X. Lima, Hyang B.
Lee, and A.L. Santiago; Absidia stercoraria Hyang B. Lee, H.S. Lee,
and T.T.T. Nguyen; Absidia terrestris Rosas de Paz, Dania García,
Guarro, Cano, and Stchigel; Absidia bonitoensis C.L. Lima, D.X.
Lima, Hyang B. Lee, and A.L. Santiago; and Absidia ovalispora
H. Zhao and X.Y. Liu (Ariyawansa et al., 2015;Li et al., 2016;
Crous et al., 2018, 2020;Wanasinghe et al., 2018;Zhang et al.,
2018;Cordeiro et al., 2020;Lima et al., 2020;de Lima et al., 2021;
Zhao et al., 2021), and nine species have been recorded in China
(Zhang et al., 2018;Zheng and Liu, 2018;Zhao et al., 2021).
Recently, seven strains of Absidia were collected from China
but could not be assigned to any described species. Herein,
morphological, physiological, and molecular phylogenetics
[internal transcribed spacer (ITS) and D1–D2 domains of LSU
rDNA] are presented to support them to four new species in
1http://www.indexfungorum.org
Absidia sensu stricto, and consequently, a revised synoptic key to
all the 13 known species of Absidia in China is provided.
MATERIALS AND METHODS
Isolation and Strains
Strains were isolated from the soil collected in Hubei province,
Shanxi province, Xinjiang province, and Yunnan province,
China. Soil samples (1 g) were suspended in 100 mL sterilized
water and shaken vigorously. Then, a 100 µL of the suspension
was added onto a potato dextrose agar (PDA; Benny, 2008) plate
with antibiotics streptomycin sulfate (100 mg/mL) and ampicillin
(100 mg/mL). The plate was incubated at 27◦C and examined
daily with a stereo microscope (SMZ1500, Nikon Corporation,
Japan). Upon the presence of colonies, a single colony was
picked and transferred to new PDA plates. Living cultures
were deposited in the China General Microbiological Culture
Collection Center, Beijing, China (CGMCC). Dried cultures were
deposited in the Herbarium Mycologicum Academiae Sinicae,
Beijing, China (HMAS).
Morphology and Growth Experiments
Pure cultures were established in triplicate, respectively, with
malt extract agar (MEA; Benny, 2008), modified synthetic mucor
agar (SMA; Zheng and Chen, 2001), and PDA plates. For
morphological observation, they were incubated at 27◦C for 4–
7 days and examined daily under a microscope (Axio Imager A2,
Carl Zeiss Microscopy, Germany). For determining maximum
growth temperatures, pure cultures were initially incubated at
32◦C for 4 days, and then the incubation temperature was
adjusted until the colonies stopped growing. The color of colonies
was designated according to Ridgway (1912).
DNA Extraction, Polymerase Chain
Reaction Amplification, and Sequencing
Mycelia were grown at 27◦C for 5 days on PDA plates, and then
cell DNAs were extracted using a kit (GO-GPLF-400, GeneOnBio
Corporation, Changchun, China). The ITS and D1–D2 domain
of LSU rDNA were amplified with primer pairs NS5M and
LR5M (Wang et al., 2014). The polymerase chain reaction (PCR)
procedure was as follows: an initial temperature at 95◦C for
5 min; then 30 cycles of denaturation at 95◦C for 20 s, annealing
at 55◦C for 60 s, and extension at 72◦C for 60 s; and finally an
extra extension at 72◦C for 10 min. PCR products were purified
and then sequenced with primers ITS5 (White et al., 1990) and
LR5M at BGI Tech Solutions Beijing Liuhe Co., Limited, Beijing,
China. All newly generated sequences were deposited in GenBank
and National Microbiology Data Center (NMDC,2Table 1).
Phylogenetic Analyses
The software platform Geneious 8.13was used to assemble and
proofread DNA sequences. All the sequences were realigned
using AliView version 3.0 (Larsson, 2014). The sequence
2http://nmdc.cn/
3http://www.geneious.com
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Zong et al. Four New Species of Absidia
TABLE 1 | Species, strains, and GenBank/NMDC accession numbers used in this study.
Species Strains GenBank/NMDC* accession no.
ITS LSU
Absidia anomala CBS 125.68 MH859085 NG058562
Absidia bonitoensis URM 7889 MN977786 MN977805
Absidia caatinguensis URM 7156 KT308169 KT308171
Absidia coerulea CBS 101.36 MH855718 MH867230
Absidia californica CBS 314.78 MH861141 MH872902
Absidia cornuta URM 6100 MN625256 MN625255
Absidia cuneospora CBS 101.59 NG058559
A. cuneospora FSU 5890 EF030524
Absidia cylindrospora FSU 906 AY944889
A. cylindrospora CBS 100.08 JN206588
Absidia fusca CBS 102.35 NR103625 NG058552
Absidia glauca CBS 129233 MH865253 MH876693
A. glauca CBS 127122 MH864429 MH875867
Absidia globospora* CGMCC 3.16031 MW671537/NMDCN0000JB7* MW671544/NMDCN0000JB0*
A. globospora* CGMCC 3.16035 MW671538/NMDCN0000JB8* MW671545/NMDCN0000JB1*
A. globospora* CGMCC 3.16036 MW671539/NMDCN0000JB9* MW671546/NMDCN0000JB2*
Absidia heterospora SHTH021 JN942683 JN982936
Absidia jindoensis CNUFC-PTI1-2 MF926623 MF926617
Absidia koreana EML-IFS45-1 KR030062 KR030056
A. koreana EML-IFS45-2 KR030063 KR030057
Absidia macrospora FSU 4746 AY944882 EU736303
Absidia medulla* CGMCC 3.16034 MW671542/NMDCN0000JBC* MW671549/NMDCN0000JB5*
A. medulla* CGMCC 3.16037 MW671543/NMDCN0000JBD* MW671550/NMDCN0000JB6*
Absidia multispora URM 8210 MN953780 MN953782
Absidia ovalispora CGMCC 3.16018 MW264071 MW264130
Absidia panacisoli SYPF 7183 MF522181 MF522180
Absidia pararepens CCF 6352 MT193669 MT192308
Absidia pernambucoensis URM 7219 MN635568 MN635569
Absidia pseudocylindrospora CBS 100.62 MH869688
A. pseudocylindrospora FSU5894 EF030526
Absidia psychrophilia FSU 4745 AY944874 EU736306
Absidia repens CBS 115583 NR103624 HM849706
Absidia saloaensis URM 8209 MN953781 MN953783
Absidia spinosa FSU 551 EU736307
Absidia stercoraria EML-DG8-2 KU168829 KT921999
Absidia terrestris FMR 14989 LT795005
A. terrestris FMR 15024 LT795004
Absidia turgida* CGMCC 3.16032 MW671540/NMDCN0000JBA* MW671547/NMDCN0000JB3*
Absidia zonata* CGMCC 3.16033 MW671541/NMDCN0000JBB* MW671548/NMDCN0000JB4*
Chlamydoabsidia padenii CBS 172.67 JN206294 NG070364
Halteromyces radiatus CBS 162.75 JN206290 NG057938
Cunninghamella elegans CBS 167.53 JN205882 HM849700
Cunninghamella blakesleeana CBS 782.68 JN205869 MH870950
*All strains of the four new species are in bold font, and their sequences are deposited at National Microbiology Data Center (NMDC).
alignments and phylogenetic trees were deposited at TreeBase
(submission ID 27734). Sequences of Cunninghamella elegans
and Cunninghamella blakesleeana retrieved from GenBank
were used as outgroups in the ITS and LSU analyses
following Hoffmann et al. (2007).
Phylogenetic analyses were carried out using maximum
parsimony (MP), maximum likelihood (ML), and Bayesian
inference (BI). MP phylogenetic analyses followed Zhao and
Wu (2017), and the tree construction was performed in PAUP∗
version 4.0b10 (Swofford, 2002). All characters were equally
weighted, and gaps were treated as missing data. Trees were
inferred using the heuristic search option with TBR branch
swapping and 1,000 random sequence additions. Max-trees
were set to 5,000; branches of zero length were collapsed,
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and all parsimonious trees were saved. Clade robustness
was assessed using a bootstrap analysis with 1,000 replicates
(Felsenstein, 1985). Descriptive tree statistics tree length (TL),
consistency index (CI), retention index (RI), rescaled CI (RC),
and homoplasy index (HI) were calculated for each maximum
parsimonious tree generated.
Maximum likelihood phylogenetic analyses were conducted
with raxmlGUI 2.0 beta (Edler et al., 2020). A general time
reversible model was used with a gamma-distributed rate
variation (GTR + G) and 1,000 bootstrap replicates.
Bayesian inference phylogenetic analyses was calculated
with MrBayes 3.2.7a by a general time-reversible model with
an estimate of the proportion of invariant sites and a gamma
distribution for variable rates across sites (GTR + I + G;
Ronquist et al., 2012). Four Markov chains were run
simultaneously from random starting trees, for 2,400,000
generations (ITS) or 300,000 generations (LSU). Trees
were sampled every 100 generations. The chains stopped
once the average standard deviation of split frequencies
decreased lower than 0.01. The first one-fourth generations
were discarded as burn-in. A majority rule consensus
tree of all remaining trees was calculated. Branches were
considered as significantly supported if they received ML
bootstrap >75%, MP bootstrap >75%, or Bayesian posterior
probabilities >0.95.
RESULTS
Phylogenetic Analyses
The ITS dataset included sequences from 38 strains
representing 33 species of Absidia and related genera.
The dataset had an aligned length of 903 characters, of
which 248 characters were constant, 136 were variable
and parsimony-uninformative, and 519 were parsimony-
informative. MP analyses yielded two equally parsimonious
trees (TL = 4163, CI = 0.3394, HI = 0.6606, RI = 0.3446,
RC = 0.1170). At the end of the inference, the average standard
deviation of split frequencies was 0.009990. All BI, ML, and
MP phylogenetic trees resulted in similar topologies. The
phylogram (Figure 1) consists of three clades, although with
relatively low support values: (1) except the A. pararepens
and A. bonitoensis, all members in the cylindrospora clade
produce cylindric sporangiospores; (2) all members in the
globospora clade produce globose sporangiospores; and (3)
the Absidia cuneospora G.F. Orr & Plunkett separately groups
as a cuneospora clade, forming conical sporangiospores
(Orr and Plunkett, 1959).
The LSU dataset included sequences from 39 strains
representing 34 species within Absidia. The dataset
had an aligned length of 967 characters, of which 562
characters were constant, 117 were variable and parsimony-
uninformative, and 288 were parsimony-informative. MP
analyses yielded 20 equally parsimonious trees (TL = 1422,
CI = 0.4339, HI = 0.5661, RI = 0.6443, RC = 0.2795). At
the end of the inference, the average standard deviation
of split frequencies was 0.009767. All BI, ML, and MP
phylogenetic trees resulted in similar topologies. The
phylogram (Figure 2) consists of three clades, similar to
the ITS phylogram (Figure 1) but with relatively high
support values, in detail, clade cylindrospora, globospora,
and cuneospora with a support of 80/-/0.99, 98/98/1.00, and
100/100/1.00, respectively.
Taxonomic Treatments
Absidia globospora T.K. Zong & X.Y. Liu, sp. nov.
Fungal names: FN570833 (Figures 3,4).
Holotype: China. Hubei Province, Shennongjia Forestry
District, from soil sample, 20 August 1984, Chen
Guiqing (HMAS 249881, living culture CGMCC 3.16031.
GenBank: ITS = MW671537, LSU = MW671544. NMDC:
ITS = NMDCN0000JB7, LSU = NMDCN0000JB0).
Paratype: China. Shanxi Province, Baoji, Tangyu
County, Taibaishan National Forest Park, from soil sample,
11 October 2002, Wang Xuewei (CGMCC 3.16035.
GenBank: ITS = MW671538, LSU = MW671545. NMDC:
ITS = NMDCN0000JB8, LSU = NMDCN0000JB1); Hubei
Province, Shennongjia District, Hubei Shennongjia Forest
Ecosystem National Field Scientific Observation and Research
Station, from an unknown substrate, 16 October 2002, Wang
Xuewei (CGMCC 3.16036. GenBank: ITS = MW671539,
LSU = MW671546. NMDC: ITS = NMDCN0000JB9,
LSU = NMDCN0000JB2).
Etymology: globospora (Lat.) referring to the shape of
sporangiospores.
Description: Colonies on MEA, irregularly zonate, attaining
73-mm diameter after 6 days at 27◦C, white at first and then
elm green (R17) to dark cress green (R31). Hyphae hyaline at
first, becoming brown when mature (6.0–)8.0–13.5(–14.5)-µm
diameter. Stolons branched, hyaline to brown, smooth, with
few septa near the base of sporangiophores (6.0–)7.0–10.5-µm
diameter. Rhizoids root-like, branched mostly twice and rarely
repeatedly, with a septum at the base. Sporangiophores erect or
slightly bent, 1–5 in whorls, unbranched, simple, monopodial or
sympodial, hyaline, or brown, with a septum (9.5–)11.0–21.5 µm
below apophyses, sometimes a swelling beneath sporangia (45.0–
)65.0–350.0(–440.0) ×5.0–8.5(–9.5) µm. Apophyses distinct,
slightly pigmented (3.0–)4.0–14.0(–20.0) µm high, 4.0–11.0(–
13.5) µm wide at the base, and 11.0–24.0(–26.5) µm wide
at the top. Sporangia globose, multispored, deliquescent-
walled (20.5–)23.0–50.0(–55.5) ×(17.0–)23.0–40.0(–57.0) µm.
Columellae hemispherical, hyaline, smooth, sometimes with
a 1–3.5 µm papillary projection at the apex, 12.5–33.5(–
48.5) ×(8.5–)10.0–31.5(–46.5) µm. Collars present or absent, but
indistinct if present. Sporangiospores globose, hyaline, smooth,
3.0–4.0(–4.5) ×2.5–3.5(–4.0) µm. Chlamydospores absent.
Zygospores not observed.
Media and temperatures: Colonies on SMA, flower-shaped,
attaining 74-mm diameter after 6 days at 27◦C, white at first and
then olive-citrine (R16) to Kronberg’s green (R31). Colonies on
PDA, flower-shaped, attaining 73-mm diameter after 6 days at
27◦C, white at first and then cossack green (R6) to cerro green
(R5). No growth at 29◦C.
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Zong et al. Four New Species of Absidia
FIGURE 1 | The maximum parsimony strict consensus tree illustrating the phylogeny of four new species of Absidia and related species in Cunninghamellaceae
based on ITS sequences. Cunninghamella elegans and Cunninghamella blakesleeana serve as outgroups. Branches are labeled with maximum likelihood bootstrap
values higher than 70%, maximum parsimony bootstrap values higher than 50%, and Bayesian posterior probabilities more than 0.95. The lower left scale
represents steps.
Absidia medulla T.K. Zong & X.Y. Liu, sp. nov.
Fungal names: FN570836 (Figures 5–7).
Holotype: China. Yunnan Province, Xishuangbanna Dai
Autonomous Prefecture, Xishuangbanna, from soil sample, 16
June 1992, Hu Fumei (HMAS 249884, living culture CGMCC
3.16034. GenBank: ITS = MW671542, LSU = MW671549.
NMDC: ITS = NMDCN0000JBC, LSU = NMDCN0000JB5).
Paratype: China. Yunnan Province, Kunming, Yunnan
Nationalities Village, from soil sample, 25 August 1995, Guo
Yinglan (CGMCC 3.16037. GenBank: ITS = MW671543,
LSU = MW671550. NMDC: ITS = NMDCN0000JBD,
LSU = NMDCN0000JB6).
Etymology: medulla (Lat.) referring to the spine-like
shape of rhizoids.
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Zong et al. Four New Species of Absidia
FIGURE 2 | The maximum parsimony strict consensus tree illustrating the phylogeny of four new species of Absidia and related species in Absidia based on LSU
sequences. Cunninghamella elegans and Cunninghamella blakesleeana serve as outgroups. Branches are labeled with maximum likelihood bootstrap values higher
than 70%, maximum parsimony bootstrap values higher than 50%, and Bayesian posterior probabilities more than 0.95. The lower left scale represents steps.
Description: Colonies on MEA, regularly zonate, attaining
74-mm diameter after 5 days at 27◦C, white at first and then
smoke gray (R46), sparse, but abundantly sporulated. Hyphae
hyaline at first, becoming brown when mature, septate in age
(5.0–)7.0–15.5-µm diameter. Stolons branched, smooth, with few
septa near the base of sporangiophores, 3.5- to 6.5-µm diameter.
Rhizoids root-like or spine-like, singly to multiply branched,
with a septum at the base. Sporangiophores erect or slightly
bent, 1–6 in whorls, unbranched, simple or monopodial, rarely
sympodial, hyaline, with a septum 12.5–20.5(–27.5) µm below
apophyses (50.0–)75.0–200.0(–220.0) ×(2.5–)3.0–6.0(–7.5) µm.
Apophyses slightly pigmented, 3.0–8.0(–8.5) µm high, 3.0–5.5(–
6.5) µm wide at the base, and 7.5–16.5(–17.5) µm wide at the
top. Sporangia globose to pyriform, multispored, deliquescent-
walled (12.0–)16.0–30.5(–41.0) ×(11.5–)15.0–30.0(–32.5) µm.
Columellae hemispherical, hyaline, smooth, generally with a
single 1.0- to 4.5-µm-long projection, 8.5–20.5 ×7.0–17.5 µm.
Collars present or absent, distinct if present. Sporangiospores
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Zong et al. Four New Species of Absidia
FIGURE 3 | Morphologies of Absidia globospora CGMCC 3.16031. (A) Sporangium; (B,C) columellae; (D) sporangiospores; (E,F) rhizoids; (G) swelling on
sporangiospores; (H) sympodial sporangiophores. Scale bars: (A–C,E–G) 20 µm; (D) 5µm; (H) 100 µm.
FIGURE 4 | Colonies of Absidia globospora CGMCC 3.16031 at 27◦C after 6 days on MEA (A) obverse, (B) reverse; on SMA (C) obverse, (D) reverse; on PDA (E)
obverse, and (F) reverse.
cylindrical to oval, hyaline, smooth, 3.0–4.5 ×2.0–3.0(–3.5) µm.
Chlamydospores absent. Zygospores not observed.
Media and temperatures: Colonies on SMA, cottony, regularly
zonate, attaining 70-mm diameter after 5 days at 27◦C, white at
first and then pale olive-gray (R51). Colonies on PDA, regularly
zonate, attaining 74-mm diameter after 5 days at 27◦C, white at
first and then snuff brown (R29) to deep olive (R40) in center. No
growth at 33◦C.
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FIGURE 5 | Morphologies of Absidia medulla CGMCC 3.16034. (A) Sporangium; (B,C) columellae; (D) sporangiospores; (E,F) rhizoids. Scale bars: (A–C,E,F)
20 µm; (D) 5µm.
Absidia turgida T.K. Zong & X.Y. Liu, sp. nov.
Fungal names: FN570834 (Figures 8,9).
Holotype: China. Xinjiang Uygur Autonomous Region,
Urumqi, Urumqi County, Xiejiagou Natural Scenic Resort, from
soil sample, 7 June 2002, Wang Xuewei (HMAS 249882, living
culture CGMCC 3.16032. GenBank: ITS = MW671540,
LSU = MW671547. NMDC: ITS = NMDCN0000JBA,
LSU = NMDCN0000JB3).
Etymology: turgida (Lat.) referring to the swollen hyphae and
the inflate projection on columellae.
Description: Colonies on MEA, irregularly radially gaped,
attaining 23-mm diameter after 3 days, 35-mm diameter
after 7 days, 50-mm diameter after 12 days at 27◦C, white
at first and then drab gray to drab (R45), sparse, but
abundantly sporulated. Hyphae hyaline at first, becoming brown
when mature, occasionally swollen, 9.0- to 23.0-µm diameter.
Stolons branched, smooth, with few septa near the base of
sporangiophores, 8.5- to 16.0-µm diameter. Rhizoids root-like,
thick, short or comparatively long, simple or 2–3 branched, with
a septum at the base. Sporangiophores erect or slight bent, 1–
4 in whorls, unbranched or sometimes simple, hyaline, with
a septum (17.0–)21.0–39.5(–43.5) µm below apophyses, 125.0–
350.0(–370.0) ×(3.5–)4.5–10.0(–11.0) µm. Apophyses distinct,
unpigmented (4.5–)5.0–13.5(–16.5) µm high, 3.5–10.0 µm wide
at the base, and (10.0–)11.0–22.0(–23.5) µm wide at the
top. Sporangia globose to pyriform, multispored, deliquescent-
walled, 20.5–42.5 ×20.0–41.5(–46.0) µm. Columellae mostly
hemispherical, sometimes conical, hyaline, smooth, with a single
clavate projection, up to 9.5 µm in length, with a bulbous
swelling at top (13.0–)14.5–25.0(–26.5) ×(10.0–)11.5–21.5 µm.
Collars present or absent, distinct if present. Sporangiospores
variable, globose, cylindrical or irregular, hyaline, smooth, 4.0–
5.0(–6.5) ×3.0–4.0 µm when cylindrical, 3.5–4.5 ×3.0–4.0 µm
or 2.0- to 2.5-µm diameter when globose. Chlamydospores
absent. Zygospores not observed.
Media and temperatures: Colonies on SMA, sporadic, nebula-
shaped, attaining 22-mm diameter after 3 days, 32-mm diameter
after 7 days, 47-mm diameter after 12 days at 27◦C, white at first
and then pale drab-gray to light cinnamon-drab (R45). Colonies
on PDA, irregularly tree ring-shaped, attaining 21-mm diameter
after 3 days, 32-mm diameter after 7 days, 44-mm diameter after
12 days at 27◦C, growing slowly when aerial hyphae reaching the
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Zong et al. Four New Species of Absidia
FIGURE 6 | Colonies of Absidia medulla CGMCC 3.16034 at 27◦C after 5 days on MEA (A) obverse, (B) reverse; on SMA (C) obverse, (D) reverse; after 7 days on
PDA (E) obverse, and (F) reverse.
FIGURE 7 | Colonies of Absidia medulla CGMCC 3.16037 at 27◦C after 5 days on MEA (A) obverse, (B) reverse; after 6 days on SMA (C) obverse, (D) reverse; after
5 days on PDA (E) obverse, and (F) reverse.
lid of the petri dish, white at first and then drab to hair brown
(R45). No growth at 33◦C.
Absidia zonata T.K. Zong & X.Y. Liu, sp. nov.
Fungal names: FN570835 (Figures 10,11).
Holotype: China. Beijing (39◦5705800 N, 116◦110430 0 E), from
soil sample, 31 December 2019, Liu Xiaoyong (HMAS 249883,
living culture CGMCC 3.16033. GenBank: ITS = MW671541,
LSU = MW671548. NMDC: ITS = NMDCN0000JBB,
LSU = NMDCN0000JB4).
Etymology: zonata (Lat.) referring to the zonate colony.
Description: Colonies on MEA, regularly concentric ring
zonate, attaining 69-mm diameter after 8 days at 27◦C, white
at first and then smoke gray (R46). Hyphae hyaline at first,
becoming brown when mature, 5.0- to 10.5-µm diameter.
Stolons branched, smooth, with few septa near the base of
sporangiophores, 4.0- to 8.0-µm diameter. Rhizoids root-like or
tentaculiform, simple or 2–3 branched, with a septum at the
base. Sporangiophores erect or slightly bent, 1–5(–8) in whorls,
unbranched, sometimes simple, rarely monopodial, hyaline,
with a septum 16.0–26.5 µm below apophyses (44.0–)55.0–
180.0(–280.0) ×2.5–5.5(–6.0) µm. Apophyses distinct, slightly
pigmented, 3.0–8.0(–8.5) µm high, 3.0–5.5(–6.5) µm wide at the
base, and 7.5–16.5(–17.5) µm wide at the top. Sporangia globose
to pyriform, multispored, deliquescent-walled, 14.0–27.0 ×12.5–
26.5 µm. Columellae hemispherical, hyaline, smooth, generally
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Zong et al. Four New Species of Absidia
FIGURE 8 | Morphologies of Absidia turgida CGMCC 3.16032. (A) Sporangium; (B,C) columellae; (D) sporangiospores; (E) rhizoids; (F) swollen on hyphae. Scale
bars: (A–C,E,F) 20 µm; (D) 5µm.
FIGURE 9 | Colonies of Absidia turgida CGMCC 3.16032 at 27◦C after 12 days on MEA (A) obverse, (B) reverse; on SMA (C) obverse, (D) reverse; on PDA (E)
obverse, and (F) reverse.
presenting a single spinous projection, up to 2.0–3.5 µm in
length, 9.5–19.0 ×(6.0–)7.5–14.5(–16.5) µm. Collars present or
absent, distinct if present. Sporangiospores mostly cylindrical,
sometimes oval, hyaline, smooth, 3.5–4.5(–6.0) ×2.0–3.0(–
3.5) µm. Chlamydospores absent. Zygospores not observed.
Media and temperatures: Colonies on SMA, rough around the
edges, concentric ring-shaped, attaining 69-mm diameter after
8 days at 27◦C, white. Colonies on PDA, regularly wavy zonate,
attaining 72-mm diameter after 7 days at 27◦C, white at first and
then lime green (R31). No growth at 38◦C.
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Zong et al. Four New Species of Absidia
FIGURE 10 | Morphologies of Absidia zonata CGMCC 3.16033. (A) Sporangium; (B,C) columellae; (D) sporangiospores; (E) rhizoids; (F) verticillately branched
sporangiophores. Scale bars: (A–C,E) 20 µm; (D) 5µm; (F) 50 µm.
Key to the known species of Absidia in China
1. Sporangiospores typically globose; Colonies greenish
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .2
1. Sporangiospores typically cylindrical, oval, or other shaped;
Colonies not greenish. . .. . .. . .. . .. . .. . .. . .. . .. . .3
2. Maximum temperatures below 30◦C; Sporangiophores not
reaching 10 µm in width; Sporangia rarely reaching 55-µm
diameter.. . .. . .. . .. . .. . .. . .. . ... . .. . .. . .A. globospora
2. Maximum temperatures above 30◦C; Sporangiophores
reaching 12 µm in width; Sporangia mostly 50- to 60-µm
diameter.. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .A. glauca
3. Columellae without distinct apical projections
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .A. heterospora
3. Columellae with apical projections
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .4
4. Sporangiospores variable, sometimes irregular in shape and
size. . .. . .. . .. . .. . .. . .. . .5
4. Sporangiospores invariable, always regular
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .6
5. Hyphae without swelling, <9-µm diameter;
sporangiophores sometimes simple, more often monopodial
or verticillate; columellae sometimes with a short
projection. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .Absidia
idahoensis
5. Hyphae occasionally swelling, >9-µm diameter;
Sporangiophores unbranched or sometimes simple;
columellae always with a projection up to 9 µm in length
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .A. turgida
6. Abundant secondary sporangia in older cultures
. . .. . .. . .. . .. . .. . .. . .. . .. . .A. repens
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Zong et al. Four New Species of Absidia
FIGURE 11 | Colonies of Absidia zonata CGMCC 3.16033 at 27◦C after 8 days on MEA (A) obverse, (B) reverse; on SMA (C) obverse, (D) reverse; after 7 days on
PDA (E) obverse, and (F) reverse.
TABLE 2 | Comparisons of morphological characteristics of Absidia zonata and Absidia koreana on SMA media at 25◦C.
Characteristics A. zonata A. koreana
Colonies 5.5 cm after 4 days 6.2–6.5 cm after 4 days, reverse irregularly zonate
Sporangiophores 1–5 per whorl, occasionally simple (2.6–) 3.2 – 5.6 (–6.5) µm wide 1–6 per whorl, occasionally branched, 3.8–4.6 µm wide
Sporangia Globose to pyriform, 15.8 – 28.5 (–33.5) ×15 – 25.5 (–31.0) µm Globose to slightly elliptical, 19.3–23.6 ×21.1–26.4 µm
Columellae Hemispherical, 11.6–19.6 ×8.4–15.0 Globose, 10.9–17.0 ×11.5–18.9 µm
Sporangiospores Cylindrical, 3.3–4.5 (–5.0) ×2.1–3.2 (–3.4) µm Short-cylindrical or cylindrical, 3.5–4.5 ×2.2–2.4 µm
Collars Present or absent, distinct if presence Present
Distance from apophyses to septa (14.2–) 15.2–22.0 (–25.5) µm 17.7–23.5 µm
6. No abundant secondary sporangia in older cultures
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .7
7. Sporangiophores never in pairs or in whorls
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .A. panacisoli
7. Sporangiophores in pairs or in whorls
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .8
8. Sporangiophores no more than 6 in whorls
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .9
8. Sporangiophores as many as 7–11 in whorls
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .11
9. Maximum temperatures below 35◦C.
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .A. medulla
9. Maximum temperatures above 35◦C
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .10
10. Sporangiophores up to 6 in whorls, occasionally swollen
below the sporangia; Collar absent; Sporangiospores ovoid to
ellipsoid. . ... . .. . .. . .. . .. . .. . .. . .A. ovalispora
10. Sporangiophores up to 4 in whorls, no
swollen; Collar always present; Sporangiospores
cylindrical. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .A.
cylindrospora
11. Rhizoids typically aseptate. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .
A. spinosa
11. Rhizoids generally or rarely septate
. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .12
12. The projections on columellae <5µm in length, taper at
the end. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .A. zonata
12. The projections on columellae >5µm in length, rounded
at the top. . .. . .. . .. . .. . .. . .. . .. . .A. pseudocylindrospora
DISCUSSION
Phylogenetically, the ITS (Figure 1) and LSU (Figure 2)
trees show that four new species cluster in different clades
of Absidia. The A. globospora (100/100/1.00 for both ITS and
LSU) is located in the globospora clade and most closely
related to A. glauca Hagem (88/100/1.00 for ITS). Their
sibling relationship is completely supported by ITS and
LSU, with 99/100/1.00 and 100/100/1.00 support values,
respectively. Physiologically, A. globospora is similar to
A. glauca in heterothallism but differs in maximum growth
temperature (37 vs. 29◦C). Morphologically, A. globospora is
similar to A. glauca in forming green colonies and globose
sporangiospores. However, A. glauca differs in its wider
sporangiophores (up to 12 µm), glaucous stolons, and larger
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Zong et al. Four New Species of Absidia
sporangia (mostly 50- to 60-µm diameter, Ellis and Hesseltine,
1965).
The other three new species are placed in the cylindrospora
clade where A. zonata is most closely related to A. koreana
(100/100/1.00 for ITS, 99/95/1.00 for LSU), which is strongly
supported with a high value of 100/100/1.00 or 98/99/0.99.
Both A. zonata and A. koreana are physiologically similar
in maximum growth temperatures but morphologically
differentiated by characteristics on SMA media (Table 2;
Ariyawansa et al., 2015). The width of sporangiospores in
A. koreana are more narrow and uniform. In its protologue,
A. koreana did not form projections, but the figure in
the original article illustrated projections. A. turgida is
basal to A. heterospora in ITS tree (Figure 1) or next
to A. repens Tiegh. and A. pararepens in the LSU tree
(Figure 2). A. medulla is closely related to A. repens in ITS
tree (Figure 1) or A. saloaensis and A. ovalispora in LSU
tree (Figure 2).
The two strains, CGMCC 3.16034 and CGMCC 3.16037,
of A. medulla are similar in maximum growth temperature,
micromorphology, and even colonies on MEA and PDA
media, but slightly different in colonies on SMA media.
The ex-paratype CGMCC 3.16037 is more floccose and
thicker and grows more slowly than the ex-holotype CGMCC
3.16034 when they are incubated on SMA at 27◦C, and it
lacks white concentric rings from the reverse side of the
colony (Figure 7).
The species Chlamydoabsidia padenii Hesselt. & J.J.
Ellis and Halteromyces radiatus Shipton & Schipper are
obviously nested within Absidia in LSU tree (Figure 2).
However, morphologically unique multiseptate, easily
pigmented aerial chlamydospores were developed in
C. padenii, whereas dumbbell-shaped sporangia were
formed in H. radiatus (Hesseltine and Ellis, 1966;
Shipton and Schipper, 1975).
The genus Absidia was proposed to be divided into several
groups distinguishable by their sporangiospores (Kwa´
sna et al.,
2006;Hoffmann et al., 2007, 2009b;Hoffmann and Voigt, 2008;
Hoffmann, 2010), which is confirmed in the present study with
three well-supported clades, i.e., cylindrospora clade, globospora
clade, and cuneospora clade (Figures 1,2). Two exceptions are
worth noting, specifically, both A. pararepens and A. bonitoensis
have sub-globose to globose sporangiospores, even though they
are in the cylindrospora clade (Crous et al., 2020).
DATA AVAILABILITY STATEMENT
The datasets presented in this study can be found in
online repositories. The names of the repository/repositories
and accession number(s) can be found in the article/
supplementary material.
AUTHOR CONTRIBUTIONS
T-KZ, C-LZ, and X-YL contributed to conception and design
of the study. T-KZ wrote the draft of the manuscript.
C-LZ and X-YL improved the manuscript. T-KZ, HZ,
C-LZ, and X-YL observed and described the morphology.
X-LL and L-YR collected the molecular data. All authors
contributed to manuscript revision, proofread, and approved
the submitted version.
FUNDING
The study is supported by the National Natural Science
Foundation of China (Grant No. 31970009) and the Yunnan
Fundamental Research Project (Grant No. 202001AS070043).
REFERENCES
Ariyawansa, H. A., Hyde, K. D., Jayasiri, S. C., Buyck, B., Chethana, K. T.,
Dai, D. Q., et al. (2015). Fungal diversity notes 111–252—taxonomic and
phylogenetic contributions to fungal taxa. Fungal Divers. 75, 27–274. doi: 10.
1007/s13225-015- 0346-5
Benny, G. L. (2008). Methods used by Dr. RK Benjamin, and other mycologists, to
isolate zygomycetes. Aliso 26, 37–61. doi: 10.5642/aliso.20082601.08
Chen, J., Fan, F., Qu, G., Tang, J., Xi, Y., Bi, C., et al. (2020). Identification
of Absidia orchidis steroid 11β-hydroxylation system and its application
in engineering Saccharomyces cerevisiae for one-step biotransformation to
produce hydrocortisone. Metab. Eng. 57, 31–42. doi: 10.1016/j.ymben.2019.10.
006
Cordeiro, T. R. L., Nguyen, T. T. T., Lima, D. X., Silva, S. B. G. D.,
Lima, C. F. D., Leitão, J. D., et al. (2020). Two new species of the
industrially relevant genus Absidia (Mucorales) from soil of the Brazilian
Atlantic Forest. Acta Bot. Bras. 34, 549–558. doi: 10.1590/0102-33062020abb
0040
Crous, P. W., Luangsa-Ard, J. J., Wingfield, M. J., Carnegie, A. J., Hernández-
Restrepo, M., Lombard, L., et al. (2018). Fungal Planet description sheets:
785–867. Persoonia 41, 238–417. doi: 10.3767/persoonia.2018.41.12
Crous, P. W., Wingfield, M. J., Chooi, Y. H., Gilchrist, C. L., Lacey, E., Pitt, J. I., et al.
(2020). Fungal Planet description sheets: 1042–1111. Persoonia 44, 301–459.
doi: 10.3767/persoonia.2020.44.11
de Lima, C. L. F., Lima, D. X., Cordeiro, T. R. L., Lee, H. B., Nguyen, T. T. T.,
Gurgel, L. M. S., et al. (2021). Absidia bonitoensis (Mucorales, Mucoromycota),
a new species isolated from the soil of an upland Atlantic forest in Northeastern
Brazil. Nova Hedwigia 112, 241–251. doi: 10.1127/nova_hedwigia/2021/0614
Edler, D., Klein, J., Antonelli, A., and Silvestro, D. (2020). raxmlGUI 2.0: a graphical
interface and toolkit for phylogenetic analyses using RAxML. Methods Ecol.
Evol. [Preprint]. doi: 10.1101/800912
Ellis, J. J., and Hesseltine, C. W. (1965). The genus Absidia: globose-spored species.
Mycologia 57, 222–235. doi: 10.1080/00275514.1965.12018205
Ellis, J. J., and Hesseltine, C. W. (1966). Species of Absidia with ovoid
sporangiospores. II. Sabouraudia 5, 59–77. doi: 10.1080/00362176785190111
Felsenstein, J. (1985). Confidence limits on phylogenetics: an approach
using bootstrap. Evolution 39, 783–791. doi: 10.1111/j.1558-5646.1985.tb004
20.x
Hawksworth, D. L., Kirk, P. M., Sutton, B. C., and Pegler, D. N. (1995). Ainsworth
& Bisby’s Dictionary of the Fungi, 8th Edn. UK: CABI Publishing.
Hesseltine, C. W., and Ellis, J. J. (1961). Notes on Mucorales, especially Absidia.
Mycologia 53, 406–426. doi: 10.1080/00275514.1961.12017970
Hesseltine, C. W., and Ellis, J. J. (1964). The genus Absidia:Gongronella and
cylindrical-spored species of Absidia.Mycologia 56, 568–601. doi: 10.1080/
00275514.1964.12018145
Hesseltine, C. W., and Ellis, J. J. (1966). Species of Absidia with ovoid
sporangiospores. I. Mycologia 58, 761–785. doi: 10.1080/00275514.1966.
12018369
Frontiers in Microbiology | www.frontiersin.org 13 August 2021 | Volume 12 | Article 677836

fmicb-12-677836 July 29, 2021 Time: 16:27 # 14
Zong et al. Four New Species of Absidia
Hoffmann, K. (2010). “Identification of the genus Absidia (Mucorales,
Zygomycetes): a comprehensive taxonomic revision,” in Molecular
Identification of Fungi, eds Y. Gherbawy and K. Voigt (Berlin: Springer).
Hoffmann, K., and Voigt, K. (2008). Absidia parricida plays a dominant
role in biotrophic fusion parasitism among mucoralean fungi
(Zygomycetes): Lentamyces, a new genus for A. parricida and
A. zychae.Plant Biol. 11, 537–554. doi: 10.1111/j.1438-8677.2008.0
0145.x
Hoffmann, K., Discher, S., and Voigt, K. (2007). Revision of the genus
Absidia (Mucorales, Zygomycetes) based on physiological, phylogenetic, and
morphological characters; thermotolerant Absidia spp. form a coherent group,
Mycocladiaceae fam. nov. Mycol. Res. 111, 1169–1183. doi: 10.1016/j.mycres.
2007.07.002
Hoffmann, K., Telle, S., Walther, G., Eckart, M., Kirchmair, M., Prillinger, H., et al.
(2009b). “Diversity, genotypic identification, ultrastructural and phylogenetic
characterization of zygomycetes from different ecological habitats and climatic
regions: limitations and utility of nuclear ribosomal DNA barcode markers,” in
Current Advances in Molecular Mycology, eds Y. Gherbawy, R. Mach, and M.
Rai (New York, NY: Nova Science Publishers, Inc), 263–312.
Hoffmann, K., Walther, G., and Voigt, K. (2009a). Mycocladus vs. Lichtheimia: a
correction (Lichtheimiaceae fam. nov., Mucorales, Mucoromycotina). Mycol.
Res. 113, 275–278.
Kaczmarek, M. B., Struszczyk-Swita, K., Li, X., Szczêsna-Antczak, M., and
Daroch, M. (2019). Enzymatic modifications of chitin, chitosan, and
chitooligosaccharides. Front. Bioeng. Biotech. 7:243. doi: 10.3389/fbioe.2019.
00243
Kwa´
sna, H., Elaine, W., and Bateman, G. L. (2006). Phylogenetic relationships
among Zygomycetes from soil based on ITS1/2 rDNA sequences. Mycol. Res.
110, 501–510. doi: 10.1016/j.mycres.2006.02.004
Larsson, A. (2014). AliView: a fast and lightweight alignment viewer and editor
for large datasets. Bioinformatics 30, 3276–3278. doi: 10.1093/bioinformatics/
btu531
Li, G. J., Hyde, K. D., Zhao, R. L., Hongsanan, S., Abdel-Aziz, F. A., Abdel-Wahab,
M. A., et al. (2016). Fungal diversity notes 253–366: taxonomic and phylogenetic
contributions to fungal taxa. Fungal Divers. 78, 1–237. doi: 10.1007/s13225-
016-0366- 9
Lima, D. X., Cordeiro, T. R., De Souza, C. A., De Oliveira, R. J., Lee, H. B.,
Souza-Motta, C. M., et al. (2020). Morphological and molecular evidence for
two new species of Absidia from Neotropic soil. Phytotaxa 446, 61–71. doi:
10.11646/phytotaxa.446.1.8
Orr, G. F., and Plunkett, O. A. (1959). A new species of Absidia from California.
Mycologia 51, 203–209. doi: 10.1080/00275514.1959.12024813
Ridgway, R. (1912). Color Standards and Color Nomenclature. Washington, DC:
Ridgway.
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S.,
et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model
choice across a large model space. Syst. Boil. 61, 539–542. doi: 10.1093/sysbio/
sys029
Schipper, M. A. A. (1990). Notes on Mucorales – I. Observations on Absidia.
Persoonia 14, 133–149.
Shipton, W. A., and Schipper, M. A. (1975). Halteromyces, a new genus in the
Mucorales.Antonie van Leeuwenhoek 41, 337–342. doi: 10.1007/BF02565068
Swofford, D. L. (2002). PAUP∗: Phylogenetic Analysis Using Parsimony (∗and Other
Methods). Version 4.0b10. Sunderland, MA: Sinauer Associates.
van Tieghem, P. (1876). Troisième mémoire sur les Mucorinées. Annales des
Siences Naturelles Botanique 4, 312–399.
Wanasinghe, D. N., Phukhamsakda, C., Hyde, K. D., Jeewon, R., Lee, H. B., Jones,
E. G., et al. (2018). Fungal diversity notes 709–839: taxonomic and phylogenetic
contributions to fungal taxa with an emphasis on fungi on Rosaceae.Fungal
Divers. 89, 1–236. doi: 10.1007/s13225-018- 0395-7
Wang, Y. N., Liu, X. Y., and Zheng, R. Y. (2014). Umbelopsis changbaiensis sp.
nov. from China and the typification of Mortierella vinacea.Mycol. Prog. 13,
657–669. doi: 10.1007/s11557-013- 0948-9
White, T. J., Bruns, T., Lee, S., and Taylor, J. (1990). “Amplification and direct
sequencing of fungal ribosomal RNA genes for phylogenetics,” in PCR Protocols:
a Guide to Methods and Applications, eds M. A. Innis, D. H. Gelfand, J. J.
Sninsky, and T. J. White (San Diego, CA: Academic Press), 315–322. doi:
10.1016/b978-0- 12-372180- 8.50042-1
Zhang, T. Y., Yu, Y., Zhu, H., Yang, S. Z., Yang, T. M., Zhang, M. Y.,
et al. (2018). Absidia panacisoli sp. nov., isolated from rhizosphere of Panax
notoginseng.Int. J. Syst. Evol. Microbiol. 68, 2468–2472. doi: 10.1099/ijsem.0.002
857
Zhao, C. L., and Wu, Z. Q. (2017). Ceriporiopsis kunmingensis sp. nov.
(Polyporales, Basidiomycota) evidenced by morphological characters and
phylogenetic analysis. Mycol. Prog. 16, 93–100. doi: 10.1007/s11557-016-12
59-8
Zhao, H., Zhu, J., Zong, T. K., Liu, X. L., Ren, L. Y., Lin, Q., et al. (2021). Two
New Species in the Family Cunninghamellaceae from China. Mycobiology 49,
142–150. doi: 10.1080/12298093.2021.1904555
Zheng, R. Y., and Chen, G. Q. (2001). A monograph of Cunninghamella.
Mycotaxon 80, 1–75. doi: 10.1007/978-3- 319-23534-9_1
Zheng, R. Y., and Liu, X. Y. (2018). Species Catalogue of China. Volume 3. Fungi:
Chtrid, Zygomycotan, Glomeromycotan Fungi. Beijing: Science Press.
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Frontiers in Microbiology | www.frontiersin.org 14 August 2021 | Volume 12 | Article 677836