Abstract
Absidia is widely distributed in soil, koji, and various types of feces. A multi-locus phylogeny covering the small subunit (SSU), internal transcribed spacer (ITS), and large subunit of ribosomal RNA gene (LSU rDNA), translation elongation factor 1-alpha (TEF1α), and actin (Act), combined with morphological characteristics, revealed five new species in this genus. This study provides their descriptions and illustrations and discusses their differences from morphological allies and phylogenetic relatives. Absidiacollariatasp. nov. is distinguished from other species in terms of the length of collars. A.hainanensissp. nov. is named after the geographical location Hainan, distinctive with a higher maximum growing temperature. A.pyriformissp. nov. is different from other species in terms of sporangial shape. A.tardivasp. nov. is characterized by slow growth. And A.tibetensissp. nov. is named after the geographical location Tibet and differentiated by more ampulliform swellings. This study further enriches the species diversity of Absidia as the latest discovery of early-diverging fungi in China.
Key words: Fungal diversity, molecular phylogeny, Mucorales, soil-borne fungi, taxonomy
Introduction
Absidia Tiegh. belongs to Mucoromycota, Mucoromycotina, Mucoromycetes, Mucorales, and Cunninghamellaceae (http://www.indexfungorum.org/, accessed on 1 November 2024). This genus was founded in 1876 and typified by A.reflexa Tiegh (Tieghem 1878). This genus is ubiquitous and widely distributed (Zhang et al. 2018; Crous et al. 2020; Hurdeal et al. 2021; Urquhart and Idnurm 2021; Zhao et al. 2021b; Zhao et al. 2022a); for example, the Czech Republic (688 records), Australia (862), Estonia (1621), Lithuania (422), Italy (372), South Africa (198), and Argentina (515) (https://www.gbif.org/, accessed on 2 November 2024). Absidia are most frequently encountered in July, August, and September, and relatively high temperatures favor Absidia members (https://www.gbif.org/, accessed on 2 November 2024). In China, they are mainly found in tropical regions such as Yunnan and Hainan provinces. They are occasionally isolated in places with low temperatures, such as Tibet and Jilin (Zhao et al. 2022a). The species of Absidia are usually isolated mainly in soil samples. They are also found in plant debris, herbivorous feces, decaying substrates, and air (Lima et al. 2020). The genus Absidia is very important in industry and medicine because it produces steroids, laccases, fatty acids, and other useful substances (Davoust and Persson 1992; Kristanti et al. 2016; Zhao et al. 2021b). Absidia is also frequently used in biotransformation of various natural products, including reduction reactions, hydroxylation, and glycosylation (Zhao et al. 2022a). Moreover, Absidia plays a vital role as the causative agent for human mucormycoses (Constantinides et al. 2008). And it is a contaminant in wine production (Zhao et al. 2022a).
Currently, there are 139 records of Absidia species, variants, and subspecies in the Index Fungorum database (http://www.indexfungorum.org/, accessed November 2, 2024). Absidia usually produces erect or slightly bent sporangia. There is a septum under sporangia. The sporangia are mostly nearly spherical to pyriform, deliquescent-walled, and multi-spored. Sporangiophores arise singly or in whorls. A small protuberance sometimes appears at the apex of columellae. Collars are evident if present. And zygospores have many appendages (Tieghem 1878; Guan et al. 2021; Zhao et al. 2021b; Zong et al. 2021).
Over the past few years, Absidia has experienced a rapid influx of proposed new species. (Lima et al. 2020; Zong et al. 2021; Cordeiro et al. 2020; Zhao et al. 2023). In this paper, five new species, A.collariata sp. nov., A.hainanensis sp. nov., A.pyriformis sp. nov., A.tardiva sp. nov., and A.tibetensis sp. nov., are described from the soils in Yunnan Province, Hainan Province, and Tibet, based on evidence of molecular phylogeny, morphogenetic characteristics, and maximum growth temperature. This is the fifth report of a serial work on the diversity of Chinese early-diverging fungi (Tao et al. 2024; Wang et al. 2024; Zhao et al. 2024; Ding et al. 2025).
Materials and methods
Isolation and morphology
In 2024, soil samples were collected from Yunnan, Tibet, and Hainan in China, following the methods of Yu Li and his colleagues (Liu et al. 2019; Zou et al. 2022). Each sample (approximately 50 g) was placed in a sterile Whirl-Pack plastic bag, labeled with a number, date, vegetation type, altitude, latitude, and longitude. All samples were preserved at 4 °C upon delivery to the laboratory. By combining soil dilution plate and moist-chamber culture methods, pure strains were isolated from soil samples (Constantinides et al. 2008; Kristanti et al. 2016; Zhao et al. 2021a). About 1 g of soil was put into a 10 mL centrifuge tube with 10 mL of sterile water and shaken on a shaker for 25 minutes to prepare a soil suspension. One milliliter of the starting suspension was transferred into 9 mL of sterile water to obtain a 10-2 soil suspension. The above steps were repeated to get 10-3 and 10-4 soil suspensions. Approximately 200 μL of the 10-3 and 10-4 soil suspensions were pipetted onto the Rose Bengal Chloramphenicol agar (RBC: peptone 5.00 g/L, KH2PO4 1.00 g/L, MgSO4·7H2O 0.50 g/L, Rose Bengal 0.05 g/L, glucose 10.00 g/L, chloramphenicol 0.10 g/L, agar 15.00 g/L) and dispersed evenly with a sterilized triangular glass coating rod. The plates were cultivated at 26 °C in the dark for 2–5 days (Corry et al. 1995). Subsequently, the hyphae at the edge of the colony were transferred to a potato dextrose agar (PDA: glucose 100 g, potato 1000 g, agar 100 g, sterilized water 5000 mL, and pH 7). Upon colony forming, a macro shot was taken with a digital camera (Canon PowerShot G7X, Canon, Tokyo, Japan). For the moist chamber, 1 g of soil was evenly sprinkled onto the surface of PDA plates, sealed with Parafilm, and cultivated inverted at 26 °C away from light. After three days, the purification of target strains was performed using an inoculation ring streak. After two days, the agar with hyphae located at the edge of the colony was transferred to a new potato dextrose agar and cultivated as above. Microscopic morphological characteristics of fungi were observed with a stereoscope (SZX10, OLYMPUS, Tokyo, Japan) and a light microscope (BX53, OLYMPUS, Tokyo, Japan) and photographed with a high-definition color digital camera (DP80, OLYMPUS, Tokyo, Japan). Structural measurements were performed using Digimizer software (v5.6.0), and each trait (sporangiospores, stolons, apophyses, and so on) was measured 25 or more times. A gradient method was used to determine its maximum growth temperature (Hoffmann et al. 2007; Hoffmann and Voigt 2009; Hoffmann 2010). Cultured colonies were incubated at 25 °C for two days, and then the temperature was increased by one degree Celsius per day until no further growth was observed. This temperature was recorded as the maximum growth temperature. All strains were stored in 10% sterilized glycerin at -20 °C and preserved in the Shandong Normal University Culture Collection (XG). The living ex-holotype cultures were stored in the China Microbiological Culture Collection Center, Beijing, China (CGMCC). Dry cultures of holotypes were submitted to the Herbarium Mycologicum Academiae Sinicae, Beijing, China (HMAS). The taxonomic information was uploaded to the Fungal Names repository (https://nmdc.cn/fungalnames/).
DNA extraction, PCR amplification, and sequencing
Fungal genomic DNA was extracted using a DNA extraction kit (Cat. No.: 70409-20; BEAVER Biomedical Engineering Co., Ltd.) (Doyle et al. 1990; Wang et al. 2023). The ITS, LSU, TEF1α, Act, and SSU regions were amplified using the primer pairs and polymerase chain reaction (PCR) programs specified in Table 1. The final volume of the reaction mixture was 25 μL, containing 12.5 μL 2 × Hieff Canace Plus PCR Master Mix with dye (Yeasen Biotechnology, Cat. No. 10154ES03), 9.5 μL ddH2O, 1 μL forward primer (10 μM), 1 μL reverse primer (10 μM), and 1 µL of genomic DNA template (1 ng/μL). The PCR programs are listed in Table 1. PCR amplification products were observed on a 2% agarose electrophoresis gel. Fragments were visualized at 254 nm UV light (Zhang et al. 2022). The amplified product was purified using a gel extraction kit (Cat# AE0101-C, Shandong Sparkjade Biotechnology Co., Ltd.). Primer synthesis and DNA sequencing were carried out by Tsingke Biotechnology (Beijing, China). MEGA v. 7.0 (Mega Limited, Auckland, New Zealand) was used to obtain consensus sequences. Finally, all sequences generated in this study were deposited in GenBank.
Table 1.
PCR information used in this study.
Loci | PCR primers | Primer sequence (5’ – 3’) | PCR cycles | References |
---|---|---|---|---|
ITS | ITS5 | GGA AGT AAA AGT CGT AAC AAG G | 95 °C 5 min; (95 °C: 30 s, 55 °C: 30 s, 72 °C: 1 min) × 35 cycles; 72 °C 10 min | White et al. (1990) |
ITS4 | TCC TCC GCT TAT TGA TAT GC | |||
LSU | LR0R | GTA CCC GCT GAA CTT AAG C | 95 °C 5 min; (94 °C: 30 s, 52 °C: 45 s, 72 °C: 1.5 min) × 30 cycles; 72 °C 10 min | Hurdeal et al. (2023) |
LR5 | TCC TGA GGG AAA CTT CG | |||
TEF1α | EF1-983F | GCYCCYGGHCAYCGTGAYTTYAT | 95 °C 5 min; (95 °C: 30 s, 55 °C: 60 s, 72 °C: 60 s) × 30 cycles; 72 °C 10 min | Jaklitsch et al. (2005) |
TEF1LLErev | AACTTGCAGGCAATGTGG | |||
Act | ACT-1 | TGG GAC GAT ATG GAI AAI ATC TGG CA | 95 °C 3 min; (95 °C: 60 s, 55 °C: 60 s, 72 °C: 1 min) × 30 cycles; 72 °C 10 min | Voigt and Wöstemeyer (2000) |
ACT-4R | TC ITC GTA TIC TIG CTI IGA IAT CCA CA T | |||
SSU | NS1 | GTA GTC ATA TGC TTG TCT CC | 95 °C 5 min; (94 °C: 60 s, 54 °C: 50 s, 72 °C: 1 min) × 37 cycles; 72 °C 10 min | (White et al. 1990) |
NS4 | CTT CCG TCA ATT CCT TTA AG |
Phylogenetic analyses
Reference sequences were downloaded according to the latest articles (Zhao et al. 2021b; Zhao et al. 2022a; Tao et al. 2024; Zhao et al. 2024). Phylogenetic analyses were performed for each marker individually, followed by a combined analysis (ITS-LSU-SSU-Act-TEF1α). The sequences newly obtained in this study were compared with reference sequences in GenBank using MEGA v.7.0 software (Larsson 2014; Kumar et al. 2016). The phylogeny was inferred using maximum likelihood (ML) and Bayesian inference (BI) algorithms (Nie et al. 2020a; Nie et al. 2020b), which were integrated with the CIPRES Science Portal (https://www.phylo.org/, accessed November 5, 2024). ML analysis was performed using RaxML 8.2.4 (https://www.phylo.org/) in CIPRES Science Gateway V. 3.3 with 1,000 bootstrap replicates (Miller et al. 2010; Nguyen et al. 2015). BI analysis was performed using the GTR + I + G model with a sampling frequency of every 1,000 generations, and eight cold Markov chains were run simultaneously for two million generations (Ronquist et al. 2012; Stamatakis 2014). Utilizing the iTOL website (https://itol.embl.de, accessed November 5, 2024), all trees that resulted were plotted and optimized. Finally, Adobe Illustrator CC 2019 was used to beautify the phylogenetic tree (Jiang et al. 2024).
Results
Molecular phylogeny
Phylogenetic analyses were performed on a dataset containing 103 isolates, including 93 strains retrieved from GenBank and 10 acquired herein. Of these, 99 isolates were classified as the ingroup Absidia, while four strains, Cunninghamellaelegans (CBS 160.28), C.elegans (CBS 167.53), C.blakesleeana (CBS 133.27), and C.blakesleeana (CBS 782.68), were employed as outgroups. In total, it consisted of 5,087 concatenated characters: 1–1,102 (ITS), 1,103–2,072 (LSU), 2,073–3,157 (TEF1α), 3,158–4,118 (Act), and 4,119–5,087 (SSU). Among these, 2,766 characters remained constant, 724 were variable and parsimony-uninformative, and 1,597 were parsimony-informative. The maximum likelihood (ML) tree (Fig. 1) and Bayesian tree showed comparable topological structures.
Figure 1.
Phylogram of the genus Absidia based on a concatenated ITS, LSU, TEF1α, Act, and SSU sequence alignment, with Cunninghamellaelegans and C.blakesleeana serving as outgroups. The robustness of branches is marked at the node with the Maximum Likelihood Bootstrap Value (left, MLBV ≥ 70%) and Bayesian Inference Posterior Probability (right, BIPP ≥ 0.90), which are separated by a slash “/”. Ten newly isolated strains are indicated in red bold. Branches shortened to fit the page are indicated by a double slash “//”. Bold strains marked with a star marker “*” are ex-types or ex-holotypes. The scale at the bottom left indicates 0.1 substitutions per site.
Taxonomy
. Absidia collariata
X.Y. Ji, H. Zhao & X.Y. Liu sp. nov.
9DD6FFC5-9E10-59D9-AF8E-C3F8BCBFE9CD
Fungal Names: FN 572256
Figure 2.
Absidiacollariata ex-holotype CGMCC 3.28536 a, b colonies on PDA (a obverse b reverse) c–e sporangia f, g swelling on sporangiophores h–j columellae k rhizoids l sporangiospores. Scale bars: 10 μm (c–l).
Type.
China • Yunnan Province, Yuxi City, Xinping Yi Dai Autonomous County, Ancient Tea Horse Road (23°57'28"N, 101°30'38"E, 2196.56 m), from soil, 5 Jul. 2024, X.Y. Ji and X.Y. Liu, holotype HMAS 353360, ex-holotype living culture CGMCC 3.28536 (=XG08666-10-1).
Etymology.
The collariata (Lat.) refers to its long collars.
Description.
Colonies on PDA at 26 °C for 5 days, reaching 68 mm in diameter, moderately fast growing with a rate of 13.6 mm/d, higher in the center than at margin, at first white, becoming grayish brown when mature, regular shape at reverse. Hyphae light-colored at first, becoming brown when mature, 4.7–9.4 µm (x– = 6.4 µm, n = 20) wide. Stolons branched, hyaline to light brown, smooth, septate, 5.1–6.3 µm (x– = 5.6 µm, n = 15) in diameter. Rhizoids well developed, root-like, branched. Sporangiophores growing on stolons, erect or slightly bent, mostly unbranched or simply branched, smooth, single or 2–4 in whorls, monopodial or sympodial, 21.7–213.5 × 2.3–5.4 µm (x– = 112.8 × 4.1 µm, n = 15). Sporangia globose to pyriform, smooth, hyaline, deliquescent-walled, 16.2–37.0 × 14.0–31.1 µm (x– = 24.2 × 23.2 µm, n = 15), and with a septum 8.8–17.9 µm (x– = 13.9 µm, n = 15) below apophyses; the septum is not obvious when young. Apophyses distinct, funnel-shaped, 6.0–9.5 µm (x– = 8.5 µm, n = 15) high, 5.1–8.8 µm (x– = 6.2 µm, n = 15) wide at the base, and 8.4–13.9 µm (x– = 10.7 µm, n = 15) wide at the top, darker brown when old. Collars present, obvious. Columellae nearly conical, sometimes subspherical to hemispherical, 8.1–13.8 × 7.7–14.9 µm (x– = 10.6 × 10.9 µm, n = 15). Projections absent or present, hyaline, single. Sporangiospores hyaline, smooth, mostly oval, 2.1–3.8 × 1.8–2.7 µm (x– = 3.1 × 2.3 µm, n = 20). Chlamydospores absent. Zygospores not found.
Maximum growth temperature.
29 °C.
Additional specimen examined.
China • Yunnan Province, Yuxi City (23°57'28"N, 101°30'38"E, 2196.56 m), from soil, 5 Jul. 2024, X.Y. Ji and X.Y. Liu, living culture XG08666-10-2.
Notes.
In the molecular phylogeny, A.collariata was closely related to A.psychrophilia (Zhao et al. 2022b). Morphologically, the width of stolons in A.collariata was smaller than that in A.psychrophilia (5.1–6.3 µm vs. 5.5–11 µm). Furthermore, the A.collariata has smaller sporangiophores (2.1–3.8 × 1.8–2.7 µm vs. 3.8–5 × 2.2–3.5 µm). The length and width of sporangiophore were also smaller in A.collariata than those in A.psychrophilia (21.7–213.5 × 2.3–5.4 µm vs. 193–288 × 4.5–9 µm). And the A.psychrophilia has larger sporangia (20–50 μm vs. 16.2–37.0 × 14.0–31.1 μm). Zygospores were not observed in A.collariata.
. Absidia hainanensis
X.Y. Ji, H. Zhao & X.Y. Liu sp. nov.
794BA142-C23B-5F4D-967D-1F915419A3BB
Fungal Names: FN 572258
Figure 3.
Absidiahainanensis ex-holotype CGMCC 3.28535 a, b colonies on PDA (a obverse b reverse) c, d sporangia e–g columellae h rhizoids i sporangiospores; Scale bars: 10 µm (c–i).
Type.
China • Hainan Province, Danzhou City, Tropical Botanical Garden (19°30'42"N, 109°30'3"E, 168.7 m), from soil, 26 Jun. 2024, X.Y. Ji and X.Y. Liu, holotype HMAS 353362, ex-holotype living culture CGMCC 3.28535 (=XG06908-1).
Etymology.
The hainanensis (Lat.) refers to Hainan Province of China, where the type was collected.
Description.
Colonies on PDA at 26 °C for 5 days, reaching 75 mm in diameter, fast growing with a rate of 15 mm/d, at first white, becoming grayish-brown when old. Hyphae hyaline at first, becoming light brown when mature, 2.5–10.2 µm (x– = 5.2 µm, n = 20) in diameter. Rhizoids root-like, simply branched. Stolons hyaline, smooth, branched, 2.9–10.1 µm (x– = 6.1 µm, n = 15) in diameter. Sporangiophores erect or slightly bent, mostly unbranched or simply branched, smooth, monopodial or sympodial, single or 2–4 in whorls, 18.8–159.2 × 1.9–3.7 µm (x– = 75.4 × 2.8 µm, n = 15). Sporangia spherical to subspherical, smooth, hyaline, deliquescent-walled, 15.1–35.2 × 14.3–29.4 µm (x– = 24.2 × 22.1 µm, n = 15), and with a septum 11.5–24.2 µm (x– = 17.0 µm, n = 15) below apophyses. Apophyses obvious, funnel-shaped, 3.3–5.1 µm (x– = 4.6 µm, n = 15) high, 2.5–8.5 µm (x– = 4.3 µm, n = 15) wide at the base, and 7.5–17.4 µm (x– = 11.0 µm, n = 15) wide at the top, light brown, hyaline. Collars present. Columellae mostly oval, 3.9–13.9 × 8.6–19.5 µm (x– = 6.3 × 10.7 µm, n = 15). Projections absent or present, hyaline, single. Sporangiospores ovoid to cylindrical, smooth, hyaline, 3.1–3.7 × 1.9–2.5 µm (x– = 3.6 × 2.2 µm, n = 20). Chlamydospores absent. Zygospores not found.
Maximum growth temperature.
34 °C.
Additional specimen examined.
China • Hainan Province, Danzhou City (19°30'42"N, 109°30'3"E, 168.7 m), from soil, 26 June 2024, X.Y. Ji and X.Y. Liu, living culture XG06908-4.
Notes.
In the molecular phylogeny, A.hainanensis was closely related to A.oblongispora (Zong et al. 2021). Morphologically, the sporangiophores of A.hainanensis were at most four in whorls, while those of A.oblongispora were at most five in whorls. Additionally, the maximum length of the sporangiophores in A.oblongispora was significantly greater than that in A.hainanensis (300 µm vs. 159.2 µm). The sporangiospore size was smaller in A.hainanensis (3.1–3.7 × 1.9–2.5 μm vs. 3.5–4.5 × 2.5–8.5 μm). The A.hainanensis has wider columellae (8.6–19.5 µm vs. 8.5–16.5 µm). Physiologically, the maximum growth temperature of A.hainanensis was higher (34 °C vs. 32 °C).
. Absidia pyriformis
X.Y. Ji, H. Zhao & X.Y. Liu sp. nov.
28DB24F4-CF53-5C0A-956D-2E42209C3DDA
Fungal Names: FN 572255
Figure 4.
Absidiapyriformis ex-holotype CGMCC 3.28538 a, b colonies on PDA (a obverse b reverse) c, d sporangia e–g columellae h rhizoids i sporangiospores; Scale bars: 10 µm (c–i).
Type.
China, Yunnan Province, Pu’er City, Mojiang Hani Autonomous County, Lianzhu Town (23°25'34"N, 101°40'58"E, 1338.32 m), from soil, 4 July 2024, X.Y. Ji and X.Y. Liu, holotype HMAS 353359, ex-holotype living culture CGMCC 3.28538 (=XG09540-14-1).
Etymology.
The epithet pyriformis (Lat.) refers to the shape of the sporangia.
Description.
Colonies on PDA at 26 °C for 5 days, attaining 76 mm in diameter, moderately fast growing with a rate of 15.2 mm/d, white at first, gradually light gray, irregularly at reverse. Hyphae branched, hyaline at first, sometimes brownish when mature, aseptate when juvenile, septate with age, 3.6–15.2 µm (x– = 6.3 µm, n = 20) wide. Stolons branched, hyaline, smooth, septate, 4.5–11.9 µm (x– = 6.9 µm, n = 15) in diameter. Rhizoids well developed, root-like, branched, tapering at the end. Sporangiophores arising from stolons, erect or slightly bent, 2–5 in whorls, monopodial, mostly unbranched or simply branched, smooth, 21.7–279.8 × 1.4–7.4 µm (x– = 97.9 × 4.4 µm, n = 15), with one septum 11.5–26.8 µm (x– = 18.5 µm, n = 15) below apophyses. Sporangia are mostly pyriform, deliquescent-walled, smooth, multi-spored, colorless when young, brownish when old, 11.7–38.8 × 11.0–29.7 µm (x– = 27.9 × 22.1 µm, n = 15). Apophyses distinct, subhyaline, usually brownish when old, 5.0–8.4 µm (x– = 7.0 µm, n = 15) high, 2.4–6.1 µm (x– = 4.4 µm, n = 15) wide at the base, and 8.9–19.2 µm (x– = 12.5 µm, n = 15) wide at the top. Collars distinct. Columellae hemispherical, subglobose to globose, smooth, subhyaline or brownish, 8.8–21.4 × 16.7–20.7 µm (x– = 10.9 × 16.7 µm, n = 15). Projections at the apex, when smaller, with an oval projection. Sporangiospores hyaline, smooth, almost cylindrical, 3.2–4.5 × 1.7–2.8 µm (x– = 3.9 × 2.2 µm, n = 20). Chlamydospores absent. Zygospores absent.
Maximum growth temperature.
33 °C.
Additional specimen examined.
China • Yunnan Province, Pu’er City, from soil (23°25'34"N, 101°40'58"E, 1338.32 m), 4 July 2024, X.Y. Ji and X.Y. Liu, living culture XG09540-14-5.
Notes.
Phylogenetically, A.pyriformis was closely related to A.soli (Hurdeal et al. 2021). Compared with A.soli, the A.pyriformis presented a smaller sporangia size (11.7–38.8 × 11.0–29.7 µm vs. 16–51 × 15–45.5 µm), and the septum showed at a shorter distance from apophyses (11.5–26.8 µm vs. 21.5–37.5 µm); conversely, sporangiophores exhibited a larger size (3.2–4.5 µm vs. 1.7–2.8 µm), and columellae had a longer length (8.8–21.4 µm vs. 7.5–12.5 µm).
. Absidia tardiva
X.Y. Ji, H. Zhao & X.Y. Liu sp. nov.
0C92F093-24E0-51BB-B154-B0292C9C8216
Fungal Names: FN 572254
Figure 5.
Absidiatardiva ex-holotype CGMCC 3.28537 a, b colonies on PDA (a obverse b reverse) c, e sporangia f, g a swelling on sporangiophores and hyphae h, i columellae j sporangiospores. Scale bars: 10 µm (c–j).
Type.
China, Yunnan Province, Yuxi County, Jinshan National Forest (23°38'15"N, 101°16'30"E, 2397.53 m), from soil, 14 May 2024, X.Y. Ji and X.Y. Liu, holotype HMAS 353358, ex-holotype living culture CGMCC 3.28537 (=XG08757-4).
Etymology.
The epithet tardiva (Lat.) refers to this species growing more slowly than other strains.
Description.
Colonies on PDA at 26 °C for 4 days, reaching 41 mm in diameter, slow-growing with a rate of 10.25 mm/d; it begins white and gradually turns pale yellow to grayish-brown, irregular at reverse. Hyphae branched, hyaline at first, brownish when mature, 2.6–10.7 µm (x– = 5.6 µm, n = 20) in diameter, sometimes swollen. Stolons hyaline to brownish, smooth, branched, 3.7–8.4 µm (x– = 5.7 µm, n = 15) in diameter. Rhizoids not observed. Sporangiophores erect or slightly bent, single or 2–4 in whorls, unbranched or simply branched, monopodial or sympodial, with a septum 10.6–23.1 µm (x– = 13.8 µm, n = 15) below apophyses, 7.9–141.9 × 1.9–7.4 µm (x– = 70.7 × 4.2 µm, n = 15), sometimes with a swelling beneath sporangia. Sporangia subspherical to spherical, smooth, multi-spored, 12.9–48.3 × 9.3–34 µm (x– = 30.3 × 22.2 µm, n = 15), deliquescent-walled. Apophyses distinct, subhyaline, small, slightly pigmented, 3.2–10.4 µm (x– = 5.2 µm, n = 15) high, 2.9–7.2 µm (x– = 4.4 µm, n = 15) wide at the base, and 8.0–20.5 µm (x– = 13.2 µm, n = 15) wide at the top. Collars absent. Columellae hemispherical, subhyaline to hyaline, smooth, 2.9–13.8 × 4.9–16.3 µm (x– = 8.7 × 9.8 µm, n = 15). Projections present, shaped like a grain of rice. Sporangiospores variously shaped, mostly ovoid; a few are cylindrical or subglobose, smooth, hyaline, 3.4–4.6 × 2.1–2.8 µm (x– = 3.9 × 2.3 µm, n = 20). Chlamydospores absent. Zygospores not observed.
Maximum growth temperature.
27 °C.
Additional specimen examined.
China • Yunnan Province, Yuxi County, from soil (23°38'15"N, 101°16'30"E, 2397.53 m), 14 May 2024, X.-Y. Ji and X.-Y. Liu, living culture XG08757-6.
Notes.
Phylogenetic analysis of five genes showed that A.tardiva was closely related to A.psychrophilia (Zhao et al. 2022b). Morphologically, the sporangia shape of A.psychrophilia was pyriform, while the sporangia of A.tardiva were hemispherical to spherical in shape. And the distance between the septum and apophysis was shorter in A.psychrophilia than in A.tardiva (10–17 µm vs. 10.6–23.1 µm). The columellae of A.psychrophilia were larger than those of A.tardiva (6.5–30 μm in diameter vs. 2.9–13.8 × 4.9–16.3 μm). The overall size of spores in A.psychrophilia was slightly larger than that in A.tardiva (long: 3.8–5 × 2.2–3.5 µm vs. wide: 3.4–4.6 × 2.1–2.8 µm); the shape of sporangiospores in A.psychrophilia was cylindrical, whereas the shape of spores in A.tardiva was oval.
. Absidia tibetensis
X.Y. Ji, H. Zhao & X.Y. Liu sp. nov.
5320FDCE-5F06-5C53-BD2F-13E046DD1D8F
Fungal Names: FN 572257
Figure 6.
Absidiatibetensis ex-holotype CGMCC 3.28534 a, b colonies on PDA (a obverse b reverse) c, d sporangia e–g columellae h, i a swelling on sporangiophores and hyphae j rhizoids k sporangiospores. Scale bars: 10 μm (c–k).
Type.
China • Tibet, Xigaze City, Yadong Country (27°21'53"N, 88°58'26"E, 2827 m), from soil, 1 Oct 2024, X.Y. Ji and X.Y. Liu, holotype HMAS 353361, ex-holotype living culture CGMCC 3.28534 (=XG00415-1).
Etymology.
The tibetensis (Lat.) refers to the Tibet Autonomous Region of China, where the type was collected.
Description.
Colonies on PDA at 26 °C for 5 days, reaching 53 mm in diameter, slow-growing with a rate of 10.6 mm/d, white at first and gradually turning to light brown; the reverse side of the colony resembles a petal-shaped, regularly at reverse. Rhizoids root-like, always branched, with a septum at the top. Hyphae hyaline to slightly gray, 5.0–10.0 µm (x– = 7.1 µm, n = 20) in diameter, sometimes ampulliform-shaped swollen. Stolons hyaline, slightly brownish, branched, smooth, 3.2–11.0 µm (x– = 6.0 µm, n = 15) in diameter. Sporangiophores erect or slightly bent, unbranched or simple branched, smooth, single or 2–5 in whorls, monopodial or sympodial, 14.7–144.0 × 2.5–5.7 µm (x– = 78.2 × 4.0 µm, n = 15), sometimes with a swelling beneath sporangia. Sporangia globose to pyriform, smooth, multi-spored, deliquescent-walled, 11.0–30.2 × 11.1–26.6 µm (x– = 21.5 × 17.1 µm, n = 15), and with a septum 8.4–20.0 µm (x– = 15.6 µm, n = 15) below apophyses. Apophyses obvious, funnel-shaped, gradually widening from the base to the top, 2.5–9.6 µm (x– = 6.7 µm, n = 15) high, 3.2–8.3 µm (x– = 4.2 µm, n = 15) wide at the base, and 7.4–19.0 µm (x– = 11.2 µm, n = 15) wide at the top, hyaline, light brown. Collars absent or present. Columellae conical, nearly globose, occasionally oval, 8.5–19.9 × 10.1–16.5 µm (x– = 11.3 × 11.8 µm, n = 15). Projections present or absent, hyaline when present, needle-pointed. Sporangiospores smooth, hyaline, mostly oval, 2.6–3.9 × 1.6–2.4 µm (x– = 3.6 × 2.1 µm, n = 20). Chlamydospores absent. Zygospores not found.
Maximum growth temperature.
30 °C.
Additional specimen examined.
China • Tibet, Xigaze City, Yadong County (27°21'53"N, 88°58'26"E, 2827 m), from soil, 1 October 2024, X.Y. Ji and X.Y. Liu, living culture XG00415-3.
Notes.
In the molecular phylogeny, A.tibetensis was closely related to A.sichuanensis (Zhao et al. 2022b). Morphologically, the maximum width of the hyphae in A.yunnanensis was greater than that in A.tibetensis (15.5 µm vs. 10.0 µm). Apophyses had a wider base width and top width in A.tibetensis (3.2–8.3 × 7.4–19.0 μm vs. 3.0–5.0 × 5.5–12.0 μm). The sporangiophore size was smaller in A.tibetensis (2.6–3.9 × 1.6–2.4 μm vs. 3.0–4.5 × 2.0–2.5 μm). The swelling on sporangiophores and hyphae was observed in A.tibetensis. The collars were not observed in A.sichuanensis. Physiologically, the maximum growth temperature of A.tibetensis was higher (30 °C vs. 28 °C).
Discussion
Absidia is widely distributed. Some soil samples in Yunnan Province, Tibet Autonomous Region, and Hainan Province were investigated in this study. The cities Pu’er and Yuxi in Yunnan Province have a subtropical monsoon climate with complex terrain, mild and humid climate, and abundant precipitation. The climatic environment is conducive to the growth of various microorganisms. Yadong County of the Tibet Autonomous Region has a plateau and mountainous climate, with significant seasonal changes and extreme weather phenomena. Danzhou City, in Hainan Province, has a tropical humid monsoon climate with abundant sunshine and abundant rainfall. Five new species of the genus Absidia were discovered in these places (Wu et al. 2020; Wang et al. 2021; Zhao et al. 2022b; Jiang et al. 2024).
Based on morphology, growth temperature dynamics, and molecular phylogenetic analyses, five novel species were identified in the genus Absidia, namely A.collariata sp. nov., A.hainanensis sp. nov., A.pyriformis sp. nov., A.tardiva sp. nov., and A.tibetensis sp. nov. In this study, phylogenetic analysis was performed for these five novel species based on five loci, namely ITS, LSU, TEF1α, Act, and SSU. By analyzing these data, strong support was obtained for the clades of these species (A.tardiva 100% MLBV and 1.00 BIPP; A.pyriformis 100% MLBV and 1.00 BIPP; A.collariata 100% MLBV and 1.00 BIPP; A.tibetensis 100% MLBV and 1.00 BIPP; A.hainanensis 100% MLBV and 1.00 BIPP; Fig. 1). At the same time, in terms of morphological structure and physiology, we also found some differences between these five newly discovered species and their closely related species (Benny 2008; Zheng et al. 2009; Hurdeal et al. 2021; Urquhart and Idnurm 2021). They have great differences in sporangiospore size, stolon width, sporangia size, base and top width of the apophyses, and so on (Ellis and Hesseltine 1965; Davoust and Persson 1992; Lima et al. 2020). Besides, the maximum growth temperature between them is also different. These differences laid the foundation for the identification of the five novel species.
Absidia has important physiological functions, which are manifested in many aspects, such as ecology, industry, medicine, and so on. Ecologically, it helps in the decomposition of organic matter, which is essential for nutrient cycling. Industrially, it is used for the biotransformation of various natural products. However, it also has a downside: some species of the genus Absidia that can grow at 37 °C are opportunistic pathogens that cause diseases in humans and animals (Zhao et al. 2022b; Tao et al. 2024). Therefore, there is still great research value in the physiological function of the genus Absidia. As of 11 November 2024, the Global Biodiversity Information Facility (GBIF) (https://www.gbif.org/, accessed 11 November 2024) contains 8,496 globally reported georeferenced records of the genus Absidia species. The genus is most widely distributed in Europe and least in Antarctica (Ellis and Hesseltine 1965; Tran et al. 2019; Liu et al. 2021). In this study, new species of Absidia were found in regions with different climates in Yunnan, Hainan, and Tibet in China, which further revealed the species diversity of Absidia in different regions.
Supplementary Material
Citation
Ji X-Y, Ding Z-Y, Nie Y, Zhao H, Wang S, Huang B, Liu X-Y (2025) Unveiling species diversity within early-diverging fungi from China V: Five new species of Absidia (Cunninghamellaceae, Mucoromycota). MycoKeys 117: 267–288. https://doi.org/10.3897/mycokeys.117.149185
Funding Statement
This study was supported by the National Natural Science Foundation of China (Nos. 32170012, 32470004, 32300011). The Key Technological Innovation Program of Shandong Province, China (no. 2022CXGC020710), the Jinan City’s ‘New University 20 Policies’ Initiative for Innovative Research Teams Project (no. 202228028) and the Innovative Agricultural Application Technology Project of Jinan City (no. CX202210).
Contributor Information
Bo Huang, Email: bhuang@ahau.edu.cn.
Xiao-Yong Liu, Email: liuxy@sdnu.edu.cn.
Additional information
Conflict of interest
The authors have declared that no competing interests exist.
Ethical statement
No ethical statement was reported.
Funding
This study was supported by the National Natural Science Foundation of China (Nos. 32170012, 32470004, 32300011). The Key Technological Innovation Program of Shandong Province, China (no. 2022CXGC020710), the Jinan City’s ‘New University 20 Policies’ Initiative for Innovative Research Teams Project (no. 202228028), and the Innovative Agricultural Application Technology Project of Jinan City (no. CX202210).
Author contributions
X.Y. Ji took charge of the drawings, DNA sequencing, and data analyses and drafted the paper; Z.Y. Ding, H. Zhao, and S. Wang collected samples and isolated cultures; Y. Nie and B. Huang revised the paper; and X.Y. Liu revised the paper and provided funding.
Author ORCIDs
Xin-Yu Ji https://orcid.org/0009-0000-4121-9103
Zi-Ying Ding https://orcid.org/0009-0003-1618-5740
Yong Nie https://orcid.org/0000-0001-8964-1661
Heng Zhao https://orcid.org/0000-0003-2938-5613
Shi Wang https://orcid.org/0000-0002-7376-7638
Bo Huang https://orcid.org/0000-0001-6032-7396
Xiao-Yong Liu https://orcid.org/0000-0002-8808-010X
Data availability
The sequences of this study have been submitted to the NCBI database (https://www.ncbi.nlm.nih.gov/, accessed November 15, 2024) with accession numbers shown in Table 2.
Table 2.
GenBank accession numbers of sequences used in this study.
Species | Strains | GenBank accession numbers | ||||
---|---|---|---|---|---|---|
ITS | LSU | TEF-1α | Act | SSU | ||
Absidiaabundans | XY09265 | ON074697 | ON074681 | NA | NA | NA |
A.abundans | CGMCC 3.16255* | NR_182590 | ON074683 | NA | NA | NA |
A.abundans | XY09274 | ON074696 | ON074682 | NA | NA | NA |
A.aguabelensis | URM 8213* | NR_189383 | NG_241934 | NA | NA | NA |
A.alpina | CGMCC 3.16104 | OL678133 | NA | NA | NA | NA |
A.ampullacea | CGMCC 3.16054 | MZ354138 | MZ350132 | NA | NA | NA |
A.anomala | CBS 125.68* | MH859085 | MH870799 | NA | NA | NA |
A.anomala | FSU5798 | EF030523 | NA | NA | EF030535 | NA |
A.biappendiculata | CBS 187.64 | MZ354153 | MZ350147 | MZ357420 | MZ357438 | NA |
A.bonitoensis | URM 7889* | MN977786 | MN977805 | NA | NA | NA |
A.brunnea | CGMCC 3.16055* | MZ354139 | MZ350133 | MZ357403 | MZ357421 | NA |
A.caatinguensis | URM 7156* | NR_154704 | NG_058582 | NA | NA | NA |
A.caerulea | XY00608 | OL620081 | NA | NA | NA | NA |
A.caerulea | XY00729 | OL620082 | NA | NA | NA | NA |
A.caerulea | CBS101.36 | MH855718 | MH867230 | NA | NA | NA |
A.caerulea | FSU767 | AY944870 | NA | NA | NA | NA |
A.californica | CBS 314.78 | JN205816 | MH872902 | NA | NA | NA |
A.californica | FSU4748 | AY944873 | EU736301 | EU736247 | EU736224 | EU736274 |
A.californica | FSU4747 | AY944872 | EU736300 | EU736246 | AY944758 | EU736273 |
A.chinensis | CGMCC 3.16057 | MZ354141 | MZ350135 | NA | MZ357422 | NA |
A.chinensis | CGMCC 3.16056* | MZ354140 | MZ350134 | NA | NA | NA |
A.cinerea | CGMCC 3.16062 | MZ354146 | MZ350140 | MZ357407 | MZ357427 | NA |
A.collariata | CGMCC 3.28536* | PQ610533 | PQ605104 | PQ613269 | PQ613279 | PQ605114 |
A.collariata | XG08666-10-2 | PQ610534 | PQ605105 | PQ613270 | PQ613280 | PQ605115 |
A.cornuta | URM 6100* | NR_172976 | MN625255 | NA | NA | NA |
A.cuneospora | CBS 101.59* | MH857828 | MH869361 | NA | NA | NA |
A.cylindrospora | CBS 100.08 | JN205822 | JN206588 | NA | NA | NA |
A.digitula | CGMCC 3.16058* | MZ354142 | MZ350136 | MZ357404 | MZ357423 | NA |
A.edaphica | MFLUCC 20-0088 | NR_172305 | NG_075367 | NA | MT410739 | NG_074951 |
A.frigida | CGMCC 3.16201* | NR_182565 | OM030223 | NA | NA | NA |
A.fusca | CBS 102.35* | NR_103625 | NG_058552 | NA | NA | NA |
A.gemella | CGMCC 3.16202* | OM108488 | OM030224 | NA | NA | NA |
A.glauca | CBS 129233 | MH865253 | MH876693 | NA | NA | NA |
A.glauca | CBS 101.08* | MH854573 | MH866105 | NA | NA | NA |
A.glauca | FSU660 | AY944879 | EU736302 | EU736248 | EU736225 | EU736275 |
A.globospora | CGMCC 3.16031* | NR_189829 | MW671544 | MZ357412 | MZ357431 | NA |
A.globospora | CGMCC 3.16035 | MW671538 | MW671545 | MZ357413 | MZ357432 | NA |
A.globospora | CGMCC 3.16036 | MW671539 | MW671546 | MZ357414 | MZ357433 | NA |
A.hainanensis | CGMCC 3.28535* | PQ610537 | PQ605108 | PQ613273 | PQ613283 | PQ605118 |
A.hainanensis | XG06908-4 | PQ610538 | PQ605109 | PQ613274 | PQ613284 | PQ605119 |
A.heterospora | SHTH021 | JN942683 | JN982936 | NA | NA | JQ004928 |
A.heterospora | CBS101.29* | JN206595.1 | MH866483.1 | NA | NA | NA |
A.jiangxiensis | CGMCC 3.16105* | OL678134 | PP780377 | PP790569 | PP790577 | PP779719 |
A.jindoensis | CNUFC-PTI1-1 | MF926622 | MF926616 | MF926513 | MF926510 | MF926626 |
A.koreana | EML-IFS45-1* | KR030062 | KR030056 | KR030060 | KR030058 | KT321298 |
A.koreana | XY00816 | OL620083 | ON123771 | NA | NA | NA |
A.koreana | XY00596 | OL620084 | NA | NA | NA | NA |
A.lobata | CGMCC 3.16256 | ON074690 | ON074679 | NA | NA | NA |
A.longissima | CGMCC 3.16203* | NR_182566 | OM030225 | NA | NA | NA |
A.macrospora | FSU4746 | AY944882 | EU736303 | EU736249 | AY944760 | EU736276 |
A.macrospora | CBS 697.68* | HM849704.1 | NA | NA | NA | NA |
A.medulla | CGMCC 3.16034 | NR_189832 | MW671549 | MZ357417 | MZ357436 | NA |
A.montepascoalis | URM 8218 | NR_172995 | NA | NA | NA | NA |
A.multispora | URM 8210* | MN953780 | MN953782 | NA | NA | NA |
A.nigra | CBS 127.68* | NR_173068 | MZ350146 | MZ357419 | MZ357437 | NA |
A.nigra | CGMCC 3.16059 | MZ354143 | MZ350137 | MZ357405 | MZ357424 | NA |
A.nigra | CGMCC 3.16060 | MZ354144 | MZ350138 | MZ357406 | MZ357425 | NA |
A.oblongispora | CGMCC 3.16061 | MZ354145 | MZ350139 | NA | MZ357426 | NA |
A.ovalispora | CGMCC 3.16019 | NR_176748 | MW264131 | NA | NA | NA |
A.panacisoli | SYPF 7183* | MF522181 | MF522180 | MF624251 | NA | MF522179 |
A.pararepens | XY00631 | OL620085 | ON123774 | NA | NA | NA |
A.pararepens | XY00615 | OL620086 | NA | NA | NA | NA |
A.pararepens | XY05899 | OL620087 | NA | NA | NA | NA |
A.pararepens | CCF 6352 | MT193669 | MT192308 | NA | NA | NA |
A.pernambucoensis | URM < BRA > 7219 | MN635568 | MN635569 | NA | NA | NA |
A.pseudocylindrospora | EML-FSDY6-2 | KU923817 | KU923814 | NA | KU923815 | KU923819 |
A.psychrophilia | FSU4745 | AY944874 | EU736306 | EU736252 | AY944762 | EU736279 |
A.purpurea | CGMCC 3.16106 | OL678135 | NA | NA | NA | NA |
A.pyriformis | CGMCC 3.28538* | PQ610531 | PQ605102 | PQ613267 | PQ613277 | PQ605112 |
A.pyriformis | XG09540-14-5 | PQ610532 | PQ605103 | PQ613268 | PQ613278 | PQ605113 |
A.radiata | CGMCC 3.16257 | ON074698 | ON074684 | NA | NA | NA |
A.radiata | XY09330-1 | ON074699 | ON074685 | NA | NA | NA |
A.repens | CBS 115583* | NR_103624 | NG_058551 | NA | NA | NA |
A.saloaensis | URM 8209* | MN953781 | MN953783 | NA | NA | NA |
A.sichuanensis | CGMCC 3.16258* | NR_182589 | ON074688 | NA | NA | NA |
A.soli | MFLU-20-0414* | MT396373 | MT393988 | NA | NA | MT394049 |
A.spinosa | FSU551 | AY944887 | EU736307 | EU736253 | EU736227 | EU736280 |
A.stercoraria | EML-DG8-1* | KU168828 | KT921998 | KT922002 | KT922000 | NG_065640 |
A.sympodialis | CGMCC 3.16063* | MZ354147 | MZ350141 | NA | NA | NA |
A.sympodialis | CGMCC 3.16064 | MZ354148 | MZ350142 | MZ357408 | NA | NA |
A.tardiva | CGMCC 3.28537* | PQ610529 | PQ605100 | PQ613265 | PQ613275 | PQ605110 |
A.tardiva | XG08757-6 | PQ610530 | PQ605101 | PQ613266 | PQ613276 | PQ605111 |
A.terrestris | FMR 14989* | LT795003 | LT795005 | NA | NA | NA |
A.tibetensis | CGMCC 3.28534* | PQ610535 | PQ605106 | PQ613271 | PQ613281 | PQ605116 |
A.tibetensis | XG00415-3 | PQ610536 | PQ605107 | PQ613272 | PQ613282 | PQ605117 |
A.turgida | CGMCC 3.16032* | NR_189830 | NG_241931 | MZ357415 | MZ357434 | NA |
A.varians | CGMCC 3.16065* | MZ354149 | MZ350143 | MZ357409 | MZ357428 | NA |
A.virescens | CGMCC 3.16066* | MZ354150 | MZ350144 | MZ357410 | MZ357429 | NA |
A.virescens | CGMCC 3.16067 | MZ354151 | MZ350145 | MZ357411 | MZ357430 | NA |
A.xinjiangensis | CGMCC 3.16107* | OL678136 | NA | NA | NA | NA |
A.yunnanensis | XY09528 | ON074701 | ON074686 | NA | NA | NA |
A.yunnanensis | CGMCC 3.16259* | NR_182591 | NG_149054 | NA | NA | NA |
A.zonata | CGMCC 3.16033* | NR_189831 | MW671548 | MZ357416 | MZ357435 | NA |
A.zygospora | RSPG 214 | KC478527 | NA | NA | NA | NA |
A.zygospora | ANG28 | DQ914420 | NA | NA | NA | NA |
A.zygospora | MFLUCC 23-0016* | OR104965 | OR104992 | NA | NA | NA |
Cunninghamellablakesleeana | CBS 782.68 | JN205869 | MH870950 | NA | NA | NA |
C.blakesleeana | CBS 133.27* | JN205865.1 | MH866397.1 | KJ156479.1 | NA | NA |
C.elegans | CBS 167.53 | MH857146 | HM849700 | NA | NA | NA |
C.elegans | CBS 160.28* | AF254928.1 | NA | KJ156470.1 | NA | NA |
Notes: The newly discovered species identified in the present study are in bold. Ex-type strains are marked with a star marker “*”. NA stands for “not available”.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
The sequences of this study have been submitted to the NCBI database (https://www.ncbi.nlm.nih.gov/, accessed November 15, 2024) with accession numbers shown in Table 2.
Table 2.
GenBank accession numbers of sequences used in this study.
Species | Strains | GenBank accession numbers | ||||
---|---|---|---|---|---|---|
ITS | LSU | TEF-1α | Act | SSU | ||
Absidiaabundans | XY09265 | ON074697 | ON074681 | NA | NA | NA |
A.abundans | CGMCC 3.16255* | NR_182590 | ON074683 | NA | NA | NA |
A.abundans | XY09274 | ON074696 | ON074682 | NA | NA | NA |
A.aguabelensis | URM 8213* | NR_189383 | NG_241934 | NA | NA | NA |
A.alpina | CGMCC 3.16104 | OL678133 | NA | NA | NA | NA |
A.ampullacea | CGMCC 3.16054 | MZ354138 | MZ350132 | NA | NA | NA |
A.anomala | CBS 125.68* | MH859085 | MH870799 | NA | NA | NA |
A.anomala | FSU5798 | EF030523 | NA | NA | EF030535 | NA |
A.biappendiculata | CBS 187.64 | MZ354153 | MZ350147 | MZ357420 | MZ357438 | NA |
A.bonitoensis | URM 7889* | MN977786 | MN977805 | NA | NA | NA |
A.brunnea | CGMCC 3.16055* | MZ354139 | MZ350133 | MZ357403 | MZ357421 | NA |
A.caatinguensis | URM 7156* | NR_154704 | NG_058582 | NA | NA | NA |
A.caerulea | XY00608 | OL620081 | NA | NA | NA | NA |
A.caerulea | XY00729 | OL620082 | NA | NA | NA | NA |
A.caerulea | CBS101.36 | MH855718 | MH867230 | NA | NA | NA |
A.caerulea | FSU767 | AY944870 | NA | NA | NA | NA |
A.californica | CBS 314.78 | JN205816 | MH872902 | NA | NA | NA |
A.californica | FSU4748 | AY944873 | EU736301 | EU736247 | EU736224 | EU736274 |
A.californica | FSU4747 | AY944872 | EU736300 | EU736246 | AY944758 | EU736273 |
A.chinensis | CGMCC 3.16057 | MZ354141 | MZ350135 | NA | MZ357422 | NA |
A.chinensis | CGMCC 3.16056* | MZ354140 | MZ350134 | NA | NA | NA |
A.cinerea | CGMCC 3.16062 | MZ354146 | MZ350140 | MZ357407 | MZ357427 | NA |
A.collariata | CGMCC 3.28536* | PQ610533 | PQ605104 | PQ613269 | PQ613279 | PQ605114 |
A.collariata | XG08666-10-2 | PQ610534 | PQ605105 | PQ613270 | PQ613280 | PQ605115 |
A.cornuta | URM 6100* | NR_172976 | MN625255 | NA | NA | NA |
A.cuneospora | CBS 101.59* | MH857828 | MH869361 | NA | NA | NA |
A.cylindrospora | CBS 100.08 | JN205822 | JN206588 | NA | NA | NA |
A.digitula | CGMCC 3.16058* | MZ354142 | MZ350136 | MZ357404 | MZ357423 | NA |
A.edaphica | MFLUCC 20-0088 | NR_172305 | NG_075367 | NA | MT410739 | NG_074951 |
A.frigida | CGMCC 3.16201* | NR_182565 | OM030223 | NA | NA | NA |
A.fusca | CBS 102.35* | NR_103625 | NG_058552 | NA | NA | NA |
A.gemella | CGMCC 3.16202* | OM108488 | OM030224 | NA | NA | NA |
A.glauca | CBS 129233 | MH865253 | MH876693 | NA | NA | NA |
A.glauca | CBS 101.08* | MH854573 | MH866105 | NA | NA | NA |
A.glauca | FSU660 | AY944879 | EU736302 | EU736248 | EU736225 | EU736275 |
A.globospora | CGMCC 3.16031* | NR_189829 | MW671544 | MZ357412 | MZ357431 | NA |
A.globospora | CGMCC 3.16035 | MW671538 | MW671545 | MZ357413 | MZ357432 | NA |
A.globospora | CGMCC 3.16036 | MW671539 | MW671546 | MZ357414 | MZ357433 | NA |
A.hainanensis | CGMCC 3.28535* | PQ610537 | PQ605108 | PQ613273 | PQ613283 | PQ605118 |
A.hainanensis | XG06908-4 | PQ610538 | PQ605109 | PQ613274 | PQ613284 | PQ605119 |
A.heterospora | SHTH021 | JN942683 | JN982936 | NA | NA | JQ004928 |
A.heterospora | CBS101.29* | JN206595.1 | MH866483.1 | NA | NA | NA |
A.jiangxiensis | CGMCC 3.16105* | OL678134 | PP780377 | PP790569 | PP790577 | PP779719 |
A.jindoensis | CNUFC-PTI1-1 | MF926622 | MF926616 | MF926513 | MF926510 | MF926626 |
A.koreana | EML-IFS45-1* | KR030062 | KR030056 | KR030060 | KR030058 | KT321298 |
A.koreana | XY00816 | OL620083 | ON123771 | NA | NA | NA |
A.koreana | XY00596 | OL620084 | NA | NA | NA | NA |
A.lobata | CGMCC 3.16256 | ON074690 | ON074679 | NA | NA | NA |
A.longissima | CGMCC 3.16203* | NR_182566 | OM030225 | NA | NA | NA |
A.macrospora | FSU4746 | AY944882 | EU736303 | EU736249 | AY944760 | EU736276 |
A.macrospora | CBS 697.68* | HM849704.1 | NA | NA | NA | NA |
A.medulla | CGMCC 3.16034 | NR_189832 | MW671549 | MZ357417 | MZ357436 | NA |
A.montepascoalis | URM 8218 | NR_172995 | NA | NA | NA | NA |
A.multispora | URM 8210* | MN953780 | MN953782 | NA | NA | NA |
A.nigra | CBS 127.68* | NR_173068 | MZ350146 | MZ357419 | MZ357437 | NA |
A.nigra | CGMCC 3.16059 | MZ354143 | MZ350137 | MZ357405 | MZ357424 | NA |
A.nigra | CGMCC 3.16060 | MZ354144 | MZ350138 | MZ357406 | MZ357425 | NA |
A.oblongispora | CGMCC 3.16061 | MZ354145 | MZ350139 | NA | MZ357426 | NA |
A.ovalispora | CGMCC 3.16019 | NR_176748 | MW264131 | NA | NA | NA |
A.panacisoli | SYPF 7183* | MF522181 | MF522180 | MF624251 | NA | MF522179 |
A.pararepens | XY00631 | OL620085 | ON123774 | NA | NA | NA |
A.pararepens | XY00615 | OL620086 | NA | NA | NA | NA |
A.pararepens | XY05899 | OL620087 | NA | NA | NA | NA |
A.pararepens | CCF 6352 | MT193669 | MT192308 | NA | NA | NA |
A.pernambucoensis | URM < BRA > 7219 | MN635568 | MN635569 | NA | NA | NA |
A.pseudocylindrospora | EML-FSDY6-2 | KU923817 | KU923814 | NA | KU923815 | KU923819 |
A.psychrophilia | FSU4745 | AY944874 | EU736306 | EU736252 | AY944762 | EU736279 |
A.purpurea | CGMCC 3.16106 | OL678135 | NA | NA | NA | NA |
A.pyriformis | CGMCC 3.28538* | PQ610531 | PQ605102 | PQ613267 | PQ613277 | PQ605112 |
A.pyriformis | XG09540-14-5 | PQ610532 | PQ605103 | PQ613268 | PQ613278 | PQ605113 |
A.radiata | CGMCC 3.16257 | ON074698 | ON074684 | NA | NA | NA |
A.radiata | XY09330-1 | ON074699 | ON074685 | NA | NA | NA |
A.repens | CBS 115583* | NR_103624 | NG_058551 | NA | NA | NA |
A.saloaensis | URM 8209* | MN953781 | MN953783 | NA | NA | NA |
A.sichuanensis | CGMCC 3.16258* | NR_182589 | ON074688 | NA | NA | NA |
A.soli | MFLU-20-0414* | MT396373 | MT393988 | NA | NA | MT394049 |
A.spinosa | FSU551 | AY944887 | EU736307 | EU736253 | EU736227 | EU736280 |
A.stercoraria | EML-DG8-1* | KU168828 | KT921998 | KT922002 | KT922000 | NG_065640 |
A.sympodialis | CGMCC 3.16063* | MZ354147 | MZ350141 | NA | NA | NA |
A.sympodialis | CGMCC 3.16064 | MZ354148 | MZ350142 | MZ357408 | NA | NA |
A.tardiva | CGMCC 3.28537* | PQ610529 | PQ605100 | PQ613265 | PQ613275 | PQ605110 |
A.tardiva | XG08757-6 | PQ610530 | PQ605101 | PQ613266 | PQ613276 | PQ605111 |
A.terrestris | FMR 14989* | LT795003 | LT795005 | NA | NA | NA |
A.tibetensis | CGMCC 3.28534* | PQ610535 | PQ605106 | PQ613271 | PQ613281 | PQ605116 |
A.tibetensis | XG00415-3 | PQ610536 | PQ605107 | PQ613272 | PQ613282 | PQ605117 |
A.turgida | CGMCC 3.16032* | NR_189830 | NG_241931 | MZ357415 | MZ357434 | NA |
A.varians | CGMCC 3.16065* | MZ354149 | MZ350143 | MZ357409 | MZ357428 | NA |
A.virescens | CGMCC 3.16066* | MZ354150 | MZ350144 | MZ357410 | MZ357429 | NA |
A.virescens | CGMCC 3.16067 | MZ354151 | MZ350145 | MZ357411 | MZ357430 | NA |
A.xinjiangensis | CGMCC 3.16107* | OL678136 | NA | NA | NA | NA |
A.yunnanensis | XY09528 | ON074701 | ON074686 | NA | NA | NA |
A.yunnanensis | CGMCC 3.16259* | NR_182591 | NG_149054 | NA | NA | NA |
A.zonata | CGMCC 3.16033* | NR_189831 | MW671548 | MZ357416 | MZ357435 | NA |
A.zygospora | RSPG 214 | KC478527 | NA | NA | NA | NA |
A.zygospora | ANG28 | DQ914420 | NA | NA | NA | NA |
A.zygospora | MFLUCC 23-0016* | OR104965 | OR104992 | NA | NA | NA |
Cunninghamellablakesleeana | CBS 782.68 | JN205869 | MH870950 | NA | NA | NA |
C.blakesleeana | CBS 133.27* | JN205865.1 | MH866397.1 | KJ156479.1 | NA | NA |
C.elegans | CBS 167.53 | MH857146 | HM849700 | NA | NA | NA |
C.elegans | CBS 160.28* | AF254928.1 | NA | KJ156470.1 | NA | NA |
Notes: The newly discovered species identified in the present study are in bold. Ex-type strains are marked with a star marker “*”. NA stands for “not available”.