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Journal of FungiJournal of Fungi
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2 May 2026

29 Pages

Descriptions of Four New Species in Cunninghamellaceae (Mucoromycota) from the Brazilian Savanna Through Integrative Taxonomy

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1
Departamento de Mycologia, Universidade Federal de Pernambuco, Avenida da Engenharia, s/n, Recife 50740-600, Pernambuco, Brazil
2
Laboratório de Micologia, Instituto de Patologia Tropical e Saúde Pública (IPTSP), Universidade Federal de Goiás, Rua 235, s/n, Goiânia 74605-050, Goiás, Brazil
3
Department of General and Applied Biology, São Paulo State University (UNESP), Av. 24-A, 1515, Bela Vista, Rio Claro 13506-900, São Paulo, Brazil
4
Environmental Microbiology Laboratory, Department of Agricultural Biological Chemistry, College of Agriculture and Life Sciences, Chonnam National University, Yongbong-Dong 300, Buk-Gu, Gwangju 61186, Republic of Korea
J. Fungi2026, 12(5), 329;https://doi.org/10.3390/jof12050329
This article belongs to the Special Issue Taxonomy, Phylogeny, and Ecology of Fungi from Different Ecological Niches
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Abstract

During a survey on Mucorales fungi from soil in the world’s most biodiverse savanna, the the Brazilian Cerrado, nine specimens belonging to the Cunninghamellace were isolated. Morphological, multiloci analyses (ITS-nLSU-act) and maximum temperature growth data revealed that those specimens represent four new species: two in Absidia and two in Gongronella. Morphological characteristics of the isolates distinguishes them from other species: Absidia rhizoidea sp. nov. forms rhizopodiform rhizoids at the end of stolons, commonly next to the sporangiophores; A. variabilis sp. nov., mostly with slightly dorsiventrally flattened sporangia; Gongronella longapophysata sp. nov., which forms a long apophysis below sporangia; and G. verticilatta sp. nov., with whorled-branched sporangiophores. The maximum temperatures growth (Tmax) of those new species are as follows: A. rhizoidea (33 °C on MEA and 32 °C on PDA), A. variabilis (31 °C on MEA and 32 °C on PDA), G. longapophysata (32 °C on MEA and 33 °C on PDA), and G. verticilatta (31 °C on MEA and PDA). The present study highlights and discusses the micromorphological, physiological (Tmax) and phylogenetic characteristics of the new species.

1. Introduction

The Cerrado biome (Brazilian Savanna), located in the Central Plateau of Brazil, is the second largest biome in extension in the country (over 2,000,000 km2, covering about 23% of the Brazilian territory), only surpassed by the Amazon Rainforest [1,2]. Different types of forest formations are observed in the Cerrado, such as riparian forest, gallery forest, dry forest, “cerradão”, savanna and grassland [1,3]. To date (as of 3 March 2026), 613 fungal species have been reported from the Brazilian Cerrado, which corresponds to 0.43% of circa (ca.) 140,000 known fungal species [4] and to 7.74% of the 7918 fungal species registered in Brazil [5]. Regarding the order Mucorales Dumort., only 17 species have been officially registered in this biome [5], from which Backusella gigacellularis J.I. de Souza, Pires-Zottarelli & Harakava [6]; and Isomucor trufemiae J.I. de Souza, Pires-Zottarelli & Harakava [7] were introduced as new species. As for Cunninghamellaceae Naumov ex R.K. Benj., reports of species in this family in the Cerrado are restricted to five species, namely, Absidia caerulea Bainier, A. cylindrospora Hagem, A. spinosa Lendn., Cunninghamella elegans Lendn., and C. phaeospora Boedijn [5]. Despite being one of the largest Brazilian biomes, our knowledge about fungal diversity of the Cerrado is limited, especially regarding Cunninghamellaceae. Furthermore, this biome suffers from constant deforestation, soil degradation, water depletion and fires [8], which makes its unknown mycodiversity even more threatened, making its discovery urgent.
Species in the Cunninghamellaceae form sporangiophores with a columellate sporangium or sporophores with a terminal vesicle with uni- to multispored pedicellate sporangiola. Zygospores are globose with opposed suspensors [9,10]. Naumov [11] accepted Cunninghamella Matr., Sigmoideomyces Thaxt., and Thamnocephalis Blakeslee in this family, and other genera were added to Cunninghamellaceae later, such as Chaetocladium Fresen. [12,13], Mycotypha Fenner [14,15] and Phascolomyces Boedijn [16]. However, Benny et al. [17] and Voigt and Wöstemeyer [18] considered the family as monogeneric, with only Cunninghamella. On the other hand, Voigt [10] and Wijayawardene et al. [4] accepted Absidia Tiegh., Chlamydoabsidia Hesselt. & J. J. Ellis, Cunninghamella, Gongronella Ribaldi, Halteromyces Shipton & Schipper, and Hesseltinella H.P. Upadhyay in the Cunninghamellaceae. Here we are following the classification of Wijayawardene et al. [4].
Absidia species are commonly isolated from herbivore dung, soil, stored food and plant remains [19]. They form stolons and rhizoids not opposed to the sporangium [20,21]. The unbranched or branched sporangiophores arise isolated or in whorls from the stolon. Sporangia are apophysate, globose, subglobose and pyriform (when considering the apophysis), and the varied-shaped columellae commonly present varied-shaped projections on their surface. Zygosporangia are globose to subglobose and born from opposed suspensors with appendages [22]. Some species of this genus are biotechnologically relevant, such as A. caerulea Bainier and A. glauca Hagem, which can produce chitosan and chitin deacetylase [23] and biotransform flavonoids (chrysin, apigenin, luteolin, and diosmetin) and flavanones (pinocembrin, naringenin, eriodictyol, and hesperetin) [24]. Absidia fusca Linnem. and A. cylindrospora Hagem can degrade polycyclic aromatic hydrocarbon compounds [25]. Furthermore, experiments carried out with A. cylindrospora highlighted its capacity to biosorb heavy metals such as cadmium, copper and lead [26]. The genus currently comprises 94 species [27].
Most of the Gongronella species have been reported from soil samples, with only G. namwonensis Hyang B. Lee, A.L. Santiago & H.J. Lim being isolated from fresh water [28]. Species of this genus show morphological characteristics similar to the ones of Absidia species, such as the formation of stolons and rhizoids (although discrete) not opposed to the sporangium and sporangiophores with apophysate sporangia. The columellae are commonly globose, hemispherical and subglobose, and sterile sporangia are formed in some species [9,21]. Sporangiospores are commonly reniform, but may also be lacrimoid, globose and subglobose, and zygosporangia are born from opposed suspensors, without appendages [21,29,30]. Gongronella butleri (Lendn.) Peyronel & Dal Vesco can produce pectinases [31], chitin deacetylase [32], amylases [33], beta-glucosidases [34], and chitosan [35]. This genus currently comprises 28 species [27].
During a survey of Mucorales fungi from the soils of the Chapada das Mesas, an area of Cerrado located in the state of Maranhão, Northeastern Brazil, we discovered four specimens of Gongronella and five of Absidia (Cunninghamellaceae) that differ morphologically and phylogenetically (ITS-LSU-act) from other species. This paper proposes two new species of Absidia and two of Gongronella, as well as discusses their morphology and phylogeny.

2. Materials and Methods

2.1. Sampling Site and Soil Collection

Soil samples were collected in the Chapada das Mesas region (7°17′51.2″ S 47°28′12.2″ W), which has circa (ca.) 160,000 ha and is located within the municipalities of Carolina, Estreito, and Riachão, in the middle of the Tocantins River basin. The vegetation cover of the Chapada das Mesas is typical of the Cerrado biome with formations of gallery forest; riparian forest; dry forest; herbaceous-shrub physiognomy with spaced shrubs and subshrubs, known as “campo sujo”; and herbaceous physiognomy with few shrubs and no trees, known as “campo limpo” [36,37]. The local soil types are cambisols, red-yellow latosols, quartz sands, and the climate is humid and tropical, with temperatures ranging from 26 to 36 °C [37].
Soil collection was carried out randomly in three different areas near the Parque Nacional da Chapada das Mesas: Cachoeira da Mansinha (7°07′54.0″ S 47°26′55.1″ W), Cachoeira do Dodô (7°05′33.2″ S 47°26′35.5″ W), Encanto Azul (7°14′00.6″ S 46°24′24.3″ W) and São Romão (6°02′09.1″ S 46°34′03.5″ W). The soil samples were collected at 5 cm deep, stored in plastic bags and kept in styrofoam boxes with ice during transportation to the Laboratório de Fungos Zigospóricos of the Universidade Federal de Pernambuco, UFPE.

2.2. Isolation, Purification and Deposit

Five milligrams of soil were added to Petri dishes with wheat germ agar medium [38] with chloramphenicol (80 mg L−1), in triplicate. Colony growth was monitored for 96 h at room temperature (28 ± 2 °C). Fragments of the colonies were transferred to Petri dishes with potato dextrose agar (PDA; HIMEDIA, Vadhani, India) [38] with chloramphenicol (80 mg L−1). The lyophilized holotypes and living cultures were deposited at the URM culture collection of the Universidade Federal de Pernambuco (Recife, Brazil).

2.3. Growth Experiments and Micromorphology

Strains were grown in triplicate on potato dextrose agar (PDA) and malt extract agar (MEA) [39], and incubated at 10, 15, 20, 25, 30, and 35 °C. Colony growth was monitored for 8 days, with colony diameters measured every 24 h. Growth results are shown as the arithmetic mean for all isolates of each species on both PDA and MEA. The maximum growth temperature (Tmax) was determined by incubating all the strains on MEA and PDA at temperatures one degree higher than the last temperature with growth. The Tmax of 50 Absidia species retrieved from literature plus four new species (two of Absidia and two of Gongronella) accessed in this work is shown in Table 1.
For observation, mycelial fragments were removed from the cultures, mounted on microscope slides with 3% KOH and/or Amman blue, and observed under a light microscope Leica DM 500 (Leica Microsystems, Wetzlar, Germany). Images were captured using the Leica DM 2500 microscope (Leica Microsystems, Wetzlar, Germany) equipped with a Leica flexacam C3 and processed using the Leica Application Suite X 3.8.1.2 software. One hundred measurements were made for each fungal structure. Measurements of the structures considered the length × width range, including outliers in parentheses. The colony color designations were determined according to Kornerup and Wanscher [40].
Table 1. Maximum growth temperatures of 52 Absidia and two Gongronella species. New species described in this study are in bold.

2.4. DNA Extraction, PCR Amplification and Sequencing

Genomic DNA extraction was carried out with the Wizard Genomic DNA Purification Kit (Promega), following the manufacturer’s guidelines. PCR amplifications for the internal transcribed spacer (ITS), part of the nuclear ribosomal large subunit (nLSU), and actin (act) were performed using primers and PCR conditions, as listed in Table 2. The amplification protocol was performed as described by de Freitas et al. [21,53]. Subsequently, bidirectional sequencing was performed with the same primers using the BigDye® Terminator v.3.1 Cycle Sequencing Kit (Applied Biosystems Life Technologies, Carlsbad, CA, USA) at the Laboratório de Ecologia e Sistemática de Fungos—LESF, UNESP, Rio Claro, São Paulo and at the Centro Multiusuário de Pesquisa de Bioinsumos e Tecnologias em Saúde (CMBiotecs, IPTSP, UFG), Goiânia, Goiás. The sequences obtained in this study are available in the NCBI GenBank database (Table 3).
Table 2. Molecular markers used in this study with respective primer pairs and PCR protocols.
Table 3. GenBank accession numbers of sequences used in this study. Sequences in boldface were obtained during this study. Ex-type strains are marked with (T).

2.5. Phylogenetic Analysis

Phylogenetic analyses were performed using sequences generated in this study and reference sequences obtained from the GenBank database, based on markermultiloci concatenated analysis (ITS, LSU, and act). The sequence datasets used in this study were constructed based on studies on Absidia [20,49] and Gongronella [21,30]. The sequences were aligned using the MAFFT v7 online interface [56,57] and manually edited using MEGA v7 software [58]. The loci were concatenated using Mesquite v3.61 software [59].
The data were first analyzed based on Maximum Likelihood (ML) analysis using IQ-TREE v1.6.12 software [60] and RAxML HPC BlackBox v8.2.12 [61]. The RAxML-HPC BlackBox ML analysis was performed using the default system options in the CIPRES Science Gateway [62] with 5000 bootstrap replicates. The IQ-TREE ML analysis involved 5000 replications, and the ultrafast bootstrap (UFboot2) method was used to calculate the branch support [63]. The ModelFinder software (http://iqtree.cibiv.univie.ac.at, accessed on 3 March 2016) included in IQ-TREE v. 1.6.12 [64] was used to determine the partitioning strategy and models based on the Akaike information criterion. The combined datasets were also analyzed based on Bayesian inference (BI) conducted using MrBayes v3.2.7a [65] in the CIPRES Science Gateway, using the same models and partitions as in the ML analysis (IQ-TREE). The BI analysis was conducted with 5 × 107 generations and a burning value of 25%, with chains sampled every 1000 generations. The resulting phylogenetic trees were visualized using FigTree v1.4.4 [66]. Values ≥ 0.95 BI posterior probability (BPP) and bootstrap support (BS) from IQ-TREE UFboot2-BS and RAxML-BS analyses (both BS ≥ 70%) were plotted near the nodes. The final combined alignment was deposited in Figshare (Study ID 10.6084/m9.figshare.31438165).

3. Results

3.1. Phylogenetic Analyses

3.1.1. Absidia

The combined matrix of three markers of Absidia species (ITS, LSU, and act) comprised sequences from 135 strains, including the outgroup Cunninghamella blakesleeana (CBS 133.27) and Cunninghamella antarctica (CBS 545.75), with a total of 2940 characters, including gaps, with 1267 characters for ITS, 823 for LSU, and 850 for act. The models used for IQ-TREE ML and BI were HKY+I+G for ITS, GTR+I+G for LSU and GTR+G for act. For the ML analysis (RAxML-HPC BlackBox) the model GTR+I+G was used and this matrix had 1918 distinct alignment patterns with 49.30% undetermined characters or gaps, and the final ML optimization likelihood value of the best tree was −43,306.257377. The estimated base frequencies were as follows: A = 0.254330, C = 0.209623, G = 0.232160, and T = 0.303887; substitution rates: AC = 1.172145, AG = 2.820942, AT = 1.449869, CG = 0.733730, CT = 4.396602, and GT = 1.000000; gamma distribution shape parameter: α = 0.637676. Based on our multiloci phylogenetic analysis (Figure 1), our isolates were placed as independent lineages with high support values between other species, with one for the isolates URM 9233, URM 9234, and URM 9235 (IQ-TREE-BS = 100%, RAxML-BS = 100%, and BPP = 1) and the other for URM 9236 and URM 9237 (IQ-TREEBS = 100%, RAxML-BS = 100%, and BPP = 1), therefore justifying their statuses as two new species.
Figure 1. Maximum Likelihood (ML) phylogenetic tree of the combined ITS, LSU and act sequences of Absidia species. The specimens obtained in this study are in bold and highlighted in yellow or green Ex-type strains are marked with (T). Confidence values for ML-BS ≥ 70% (UFboot2/RAxML) and BPP ≥ 0.95 are included near the nodes and “-” indicates statistical support below the threshold values. The tree was rooted to Cunninghamella blakesleeana (CBS 133.27) and Cunninghamella antarctica (CBS 545.75).

3.1.2. Gongronella

The combined matrix of three markers of Gongronella species (ITS, LSU, and act) comprised sequences from 58 strains, including the outgroup Absidia digitula (CGMCC 3.16058) and Absidia turgida (CGMCC 3.16032), with a total of 2426 characters, including gaps, with 760 characters for ITS, 928 for LSU and 738 for act. The model used for IQ-TREE ML and BI was GTR+G for both genes. For the ML analysis (RAxML-HPC BlackBox), the model GTR+I+G was used; this matrix had 904 distinct alignment patterns with 35.71% undetermined characters or gaps, and the final ML optimization likelihood value of the best tree was -11879.360036. The estimated base frequencies were as follows: A = 0.250425, C = 0.216708, G = 0.245264, and T = 0.287603; substitution rates: AC = 0.872173, AG = 2.309143, AT = 1.587038, CG = 0.516161, CT = 4.286676, and GT = 1.000000; gamma distribution shape parameter: α = 0.508375. Based on our multiloci phylogenetic analysis (Figure 2), our isolates were placed as independent lineages with high support values between other species, with one for the isolates URM 9240, and URM 9241 (IQ-TREE-BS = 100%, RAxML-BS = 100%, and BPP = 1) and the other for URM 9238 and URM 9239 (IQ-TREEBS = 99%, RAxML-BS = 100%, and BPP = 1), therefore justifying their status as two new species.
Figure 2. Maximum Likelihood (ML) phylogenetic tree of the combined ITS, LSU, and act sequences of Gongronella species. The specimens obtained in this study are in bold and highlighted in yellow or green Ex-type strains are marked with (T). Confidence values for ML-BS ≥ 70% (UFboot2/RAxML) and BPP ≥ 0.95 are included near the nodes and the “-” indicates statistical support below the threshold values. The tree was rooted to Absidia digitula (CGMCC 3.16058) and Absidia turgida (CGMCC 3.16032).

3.2. Taxonomy

3.2.1. Absidia rhizoidea L.W.S. de Freitas & A.L. Santiago, sp. nov. (Figure 3 and Figure 4)

Mycobank number: MB863003.
Etymology: The epitet rhizoidea (Lat.), referring to the rhizopodiform rhizoids formed at the end of solons, commonly next to the sporangiophores.
Diagnosis: The rhizoids are strongly branched, rhizopodiform, commonly formed next to the sporangiophores. Chlamydospores abundant.
Description: Colonies floccose on PDA, initially white (A1), turning brown (6E8), 8.5 cm in diameter after 8 days of incubation at 25 °C; reverse caramel brown (6C6), irregular. Rhizoids caramel brown, commonly formed at the end of stolons and very close to the sporangiophores, rhizopodiform, strongly branched, 2.5–4.5 µm in diameter, smooth-walled. Sporangiophores brown, arising from stolons, isolated or in whorls of up to seven, unbranched, simple or rarely sympodially branched up to three times, (7–)20–350(–575) × (2.5–)5–12(–20) µm, smooth-walled, occasionally with one swelling after 7 days of incubation. One septum is observed near the apophysis. Sporangia light brown, subglobose, 12–40 × 10–40 µm, smooth and deliquescent-walled. Apophysis brownish, short or long, cup or bell-shaped, 5–30 × 6–30 µm. Columellae light brown, hemispherical or subglobose, 2.5–17 × 7–22 µm, occasionally with up to two needle-shaped or filiform with bulbous tip projection, 3–12 × 2–4 µm. Sporangiospores hyaline, cylindrical, some with a slight constriction in the center, ellipsoid and subglobose, 3–8 × 2–6 µm, smooth-walled. Chlamydospores abundant, hyaline, globose and subglobose, many attached to rhizoids or formed in aerial hyphae, 2.5–7 µm in diameter. Zygosporangia not observed.
Growth experiments (8 days): On PDA: At 5 °C—no growth; at 10 °C—1.5 cm diameter; at 15 °C—5.5 cm diameter; at 20 °C—8 cm diameter; at 25 °C—8.5 cm diameter; at 30 °C—8.3 cm diameter; at 35 °C—no growth. On MEA: At 5 °C—no growth; at 10 °C—0.7 cm diameter; at 15 °C—5.3 cm diameter; at 20 °C—8.8 cm diameter; at 25 °C—9 cm diameter; at 30 °C—8.5 cm diameter; at 35 °C—no growth. The Tmax is 33 °C on MEA and 32 °C on PDA.
Habitat and Distribution: Soil from Maranhão state (Brazil).
Specimen examined: BRAZIL, Maranhão, Carolina city, Chapada das Mesas, Cachoeira do Dodô (7°05′33.2″ S 47°26′35.5″ W), soil, 15 May 2023, L.W.S. de Freitas (Holotype URM 9234H metabolically inactive state, Ex-type living culture URM 9234).
GenBank accession numbers: ITS = PZ234078, LSU = PZ227107, act = PZ227661.
Additional specimens examined: BRAZIL, Maranhão, Carolina, Chapada das Mesas, Cachoeira do Dodô (7°05′33.2″ S 47°26′35.5″ W), soil, 15 May 2023, L.W.S. de Freitas (URM 9233); Encanto azul (7°14′00.6″ S 46°24′24.3″ W), soil, 15 May 2023, L.W.S. de Freitas (URM 9235).
GenBank numbers: URM 9233, ITS = PZ234079, LSU = PZ227108, act = PZ227662; URM 9235, ITS = PZ234080, LSU = PZ227109, act = PZ227663.
Notes: In our phylogenetic analysis, Absidia rhizoidea is a sister species of A. variiprojecta (Figure 1). Morphologically, A. rhizoidea forms constant rhizoids close to the sporangiophores, in addition to sporangiophores arising in whorls of up to seven from stolon, while A. variiprojecta has rhizoids not commonly formed close the sporangiophores and forms sporangiophores arising in whorls of up to five from stolon. Furthermore, columellae of the new species are hemispherical or subglobose, occasionally with up to two needle-shaped or filiform with bulbous tip projection, differing from A. rhizoidea that forms columellae subglobose or subglobose to fig-shaped, with one projection generally needle- or triangle-shaped, some bulbous, very rarely feather-shaped. The Tmax of A. variiprojecta is 32 °C, both on PDA and MEA [20], while the Tmax values of the new species are 33 and 32° C on MEA and PDA, respectively.
Figure 3. Absidia rizhoidea (URM 9234, ex-type) on PDA at 25 °C after eight days. (A) Colony verse (left) and reverse (right). (B) Sporangiophore with sporangium. (C) Sporangiophore with a swallow and sporangium. (D) Sporangiophore short branched with sporangium and projection. (E) Two sporangiophores arising from stolon with rhizoid. (F,G) Sporangiophore with apophysis, columella and projection. (H) Sporangiospores. (I) Stolons with sporangiophores and rhizoids (arrows). Scale bars: (B,C) 20 μm; (D,E,I) 15 μm; (F,G) 10 μm; (H) 10 μm.
Figure 4. Absidia variabilis (URM 9236, ex-type) on PDA at 25 °C after eight days. (A) Branched sporangiophore. (B,C) Sporangiophore with a septum below the apophysis, columella and projection. Absidia rizhoidea on PDA at 25 °C after eight days. (D) Sporangiophore with swelling. (E) Sporangiophores in a whorl of four arising from stolon. (F) Sporangiophore with sporangium. (G) Sporangiophore with a long apophysis, columella and projection. (H) Chlamydospores. Scale bars: (A) 5 μm; (B,C) 8 μm; (D,E) 20 μm; (F–H) 10 μm.

3.2.2. Absidia variabilis L.W.S. de Freitas & A.L. Santiago, sp. nov. (Figure 4 and Figure 5)

Mycobank number: MB863004.
Etymology: The epitet variabilis (lat.) refers to the formation of sporangiophores variable in length.
Diagnosis: Sporangiophores varied in length, arising singular or in whorls of up to five from stolons, commonly unbranched or monopodially branched, never sympodially branched; chlamydospores are abundant.
Description: Colonies floccose on PDA, initially white (A1), becoming light brown (6D8), 8.5 cm in diameter after 8 days of incubation, at 25 °C; reverse light brown (6D8), wave zonate. Rhizoids brown, poorly branched, often with adherent chlamydospores, 2.5–5.5 µm in diameter, with encrusted wall. Sporangiophores erect, light brown, arising from stolons, singular or in whorls of up to five, monopodially, but never sympodially branched, varied in length (15–)60–190(–230) × (2–)3–4(–6) µm, smooth-walled, with no swellings. One septum is observed near the apophysis. Sporangia apophysate, light brown, globose to slightly dorsiventrally flattened, pyriform (when considering the apophysis), (7–)10–20(–30) × (10–)15–30 µm, smooth, with deliquescent wall. Apophysis brownish, short, cup-shaped, (2–)4.5–7(–12) × (3.5–)7.5–15 µm, smooth-walled. Columellae light brown slightly flattened and subglobose (2–)5–17 × (5–)9–22 µm, smooth-walled, collar visible. One filiform, spine-like or occasionally triangular projection, up to 1–4 × 0.5–2.5 µm, can be observed on the columellae surface. Sporangiospores hyaline, mostly cylindrical, constricted in the center, some short cylindrical, 2.5–5.5 × 1.5–2.5 µm, smooth-walled. Chlamydospores abundant, hyaline, globose, subglobose, frequently attached to rhizoids or in aerial hyphae, 2–6 µm in diameter. Zygosporangia not observed.
Growth experiments (8 days): On PDA: At 5 °C—no growth; at 10 °C—1.1 cm diameter; at 15 °C—4.6 cm diameter; at 20 °C—8.6 cm diameter; at 25 °C—9 cm diameter; at 30 °C—8.5 cm diameter; at 35 °C—no growth. On MEA: At 5 °C—no growth; at 10 °C—0.7 cm diameter; at 15 °C—5.1 cm diameter; at 20 °C—8.5 cm diameter; at 25 °C—8.8 cm diameter; at 30 °C—8.6 cm diameter; at 35 °C—no growth. The Tmax is 31 °C on MEA and 32 °C on PDA.
Habitat and Distribution: Soil from Maranhão state (Brazil).
Typification: BRAZIL, Maranhão, Carolina, Chapada das Mesas, São Romão (6°02′09.1′′ S 46°34′03.5′′ W), soil, 15 May 2023, L.W.S de Freitas (Holotype URM 9236H metabolically inactive state, Ex-type living culture URM 9236).
GenBank accession numbers: ITS = PZ234081, LSU = PZ227110, act = PZ227664.
Additional specimen examined: BRAZIL, Maranhão, Carolina, Chapada das Mesas, São Romão (6°02′09.1′′ S 46°34′03.5′′ W), soil, 15 May 2023, L.W.S. de Freitas (URM 9237). GenBank accession numbers: ITS = PZ234082, LSU = PZ227111, act = PZ227665.
Notes: Absidia variabilis is phylogenetically more closely related to A. variispora T.R.L. Cordeiro & A.L. Santiago (Figure 1). The main morphological differences between both species are the formation of sporangiophores arising singular or in whorls of up to six from stolon, as well as the formation of cylindrical, elliptical, globose, and subglobose sporangiospores by A. variispora, while A. variabilis forms sporangiophores single or in whorls of up to five from stolon and produces exclusively cylindrical spores. Furthermore, A. variabilis forms chlamydospores, while A. variispora does not. Absidia variabilis grows up to 31 °C on MEA and 32 °C on PDA, while A. variispora can grow at 32 °C on MEA and PDA [20].
Figure 5. Absidia variabilis (URM 9236, ex-type) on PDA at 25 °C after eight days. (A) Colony verse (left) and reverse (right). (B) Sporangiophore with sporangium. (C–F) Different types of columellae, apophyses, and projections. (G,H) Branched sporangiophore. (I) Two sporangiophores arising from stolon. (J) Rhizoid. (K) Sporangiospores. (L) Chlamydospores. Scale bars: (B) 15 μm; (C–I) 10 μm; (J–L) 5 μm.

3.2.3. Gongronella longapophysata L.W.S de Freitas & A.L. Santiago, sp. nov. (Figure 6 and Figure 7)

Mycobank number: MB863005.
Etymology: The epithet longapophysata (Lat.) refers to the sporangiophores with elongated apophysis.
Diagnosis: The species forms sporangiophores with some very elongated apophyses, some with an elongated swelling below apophyses, and chains of 3 to 12 sterile sporangia along sporangiophores.
Description: Colonies white (A1), cottony, with regular margin, 6.5 cm in diameter on PDA after 8 days, at 25 °C. Reverse white (A1). Rhizoids branched, long, often with adherent chlamydospores, 2–10 μm in diameter, and bulbous, 5–38 μm in diameter. Stolons hyaline, branched and coenocytic. Sporangiophores hyaline, erect, curved to sinuous, (10–)35–230(–350) × 2.5–7(–12) μm, with one to two septa below the sporangium, simple or sympodially branched up to four times, wall smooth to slightly incrusted, rarely verticillately branched in whorls of up to five. Fertile sporangia hyaline, subglobose (5–)12–20(–25) × (6.5–)15–20(–25) μm, wall with vitreous aspect, smooth and deliquescent, leaving a collar. Sterile sporangia hyaline, ellipsoid, cylindrical to constricted frequently formed on short sporangiophores branches, 3–20 μm in diameter, occasionally so short that the sterile sporangia appear to be sessile; 3–6, rarely, 7–12 sterile sporangia are also formed along the sporangiophore. Columellae hyaline, hemispherical, subglobose (2–)5–10 × (3.5–)7–11(–15) μm. Apophyses bell-shaped, long or short, vasiform, (2–)3–7(–10) × (5–)7–10(–13) μm. Some sporangiophores may show an elongated swelling below the apophysis, 10–25 × 5–7 μm. Sporangiospores hyaline, reniform, some irregularly-shaped, 2–5.5 × 1.5–2 μm, smooth-walled. Chlamydospores abundant, hyaline, globose, 4–15 μm in diameter. Zygosporangia not observed.
Growth experiments (8 days): On PDA: At 10 °C—no growth; at 15 °C—1.8 cm diameter; at 20 °C—3.1 cm diameter; at 25 °C—6.3 cm diameter; at 30 °C—7.5 cm diameter; at 35 °C—no growth. On MEA: At 10 °C—no growth; at 15 °C—1.9 cm diameter; at 20 °C—4.4 cm diameter; at 25 °C—6.0 cm diameter; at 30 °C—6.8 cm diameter; at 35 °C—no growth. The Tmax is 32 °C on MEA and 33 °C on PDA.
Habitat and Distribution: Soil from Maranhão state (Brazil).
Specimen examined: Brazil, Maranhão, Carolina city, Chapada das Mesas, Cachoeira da Mansinha (7°07′54.0″ S 47°26′55.1″ W), soil, 15 May 2023, L.W.S. de Freitas (Holotype URM 9240H metabolically inactive state, Ex-type living culture URM 9240).
GenBank accession numbers: ITS = PZ234083, LSU = PZ227112, act = PZ227666.
Additional specimen examined: BRAZIL, Maranhão, Carolina city, Chapada das Mesas, Cachoeira da Mansinha (7°07′54.0″ S 47°26′55.1″ W), soil, 15 May 2023, L.W.S de Freitas (URM 9241).
GenBank accession numbers: ITS = PZ234084, LSU = PZ227113, act = PZ227667.
Notes: Gongronella longapophysata is phylogenetically closely related to G. multiramosa and G. abortosporangia (Figure 1). Morphologically, G. multiramosa and G. abortosporangia can be easily differentiated from G. longapophysata due to no formed stolons, no verticillately branched sporangiophores (rare in G. longapophysata), no sporangiophores with a swelling below apophysis, and no chains of 3 to 12 sterile sporangia along sporangiophores [30]. The Tmax of G. longapophysata is 32 °C on MEA and 33 °C on PDA, but Tmax of G. abortosporangia and G. multiramosa is not indicated in the protologues nor elsewhere [29,30].
Figure 6. Gongronella longapophysata (URM 9240, ex-type) on PDA at 25 °C after eight days. (A) Colony verse (left) and reverse (right). (B–D) Columellae and aphophyses. (E) Sporangiophore with elongated swelling below the apophysis and sterile sporangia. (F) Branched sporangiophore. (G) Sporangiospores. Scale bars: (B–E) 10 μm; (F,G) 5 μm.
Figure 7. Gongronella longapophysata (URM 9240, ex-type) on PDA at 25 °C after eight days. (A,B) Branched sporangiophore with fertile sporangia. (C) Sterile sporangium. (D) Simply branched sporangiophore with sporangia. (E) Simply branched sporangiophore with fertile (terminal) and sterile (branch) sporangia. (F) Apophyses and columellae. (G) Sporangiophore with long and short branches. (H) Rhizoid with chlamydospores. (I) Bulbous rhizoid. Scale bars: (A,B) 30 μm; (C–F) 5 μm; (G–I) 10 μm.

3.2.4. Gongronella verticillata L.W.S. de Freitas & A.L. Santiago, sp. nov. (Figure 8 and Figure 9)

Mycobank number: MB863006.
Etymology: The epithet verticillate (Lat.) refers to the formation of sporangiophores verticillately branched.
Diagnosis: The species commonly forms sporangiophores branched in whorls with up to five branches.
Description: Colonies white (A1), cottony, regular margin, 7 cm in diameter on PDA after 8 days of incubation, at 25 °C; reverse cream (4A3). Rhizoids of two types: root-shaped, hyaline, branched, with spaced septa and chlamydospores attached, and bulbous, without chlamydospores attached, 2.5–8.5 µm in diameter. Stolons hyaline, simple and coenocytic. Sporangiophores simple or sympodially branched up to six times, and commonly verticillately branched, with up to five branches in a whorl, (25–)95–200(–250) × 2.5–5 μm, with one or two septa below the sporangium, rarely forming three septa, smooth-walled. Some sporangiophores are extremely short, 2.5–10 × 2–3 μm, forming sterile apical or lateral sporangia. Fertile sporangia hyaline, globose, (6–)10–17(–22) μm diameter, with vitreous aspect, smooth and deliquescent-walled, leaving a collar. Abortive sporangia ovoid, subglobose and globose 4–18 μm in diameter. Columellae hyaline, mostly globose 1–5 μm in diameter, subglobose, hemispherical, flattened and rounded-topped (1–)4–7(–9) × (2–)6–9(–12) μm, smooth-walled, occasionally so flattened that they seem inconspicuous. Apophyses hyaline, mostly globose, 3–10 μm diameter, subglobose, some bell-shaped and vasiform, (3–)5–10(–13) × (3.5–)6–12(–15) μm, smooth-walled. Sporangiospores hyaline, elliptical to fusiform, irregular or reniform, 2–7.5 × 1.5–4 μm, smooth-walled. Chlamydospores abundant, hyaline, subglobose and ellipsoidal, 4–15 μm diameter. Zygosporangia not observed.
Growth experiments (8 days): On PDA: At 10 °C—no growth; at 15 °C—1.7 cm diameter; at 20 °C—3.2 cm diameter; at 25 °C—6.8 cm diameter; at 30 °C—2.1 cm diameter; at 35 °C—no growth. On MEA: At 10 °C—no growth; at 15 °C—1.9 cm diameter; at 20 °C—4.2 cm diameter; at 25 °C—5.5 cm diameter; at 30 °C—4 cm diameter; at 35 °C—no growth. The Tmax is 31 °C on both MEA and PDA.
Habitat and Distribution: Soil from Maranhão state (Brazil).
Specimen examined: BRAZIL, Maranhão, Carolina city, Chapada das Mesas, Cachoeira da Mansinha (7°07′54.0″ S 47°26′55.1″ W), soil, 15 May 2023, L.W.S. de Freitas (Holotype URM 9238H metabolically inactive state, Ex-type living culture URM 9238).
GenBank accession numbers: ITS = PZ234085, LSU = PZ227114.
Additional specimen examined: BRAZIL, Maranhão, Carolina city, Chapada das Mesas, Cachoeira da Mansinha (7°07′54.0″ S 47°26′55.1″ W), soil, 15 May 2023, L.W.S. de Freitas (URM 9239).
GenBank accession numbers: ITS = PZ234086, LSU = PZ227115.
Notes: Gongronella verticillata is phylogenetically closely related to G. multispora and G. bartikiae (Figure 1). However, G. verticillata forms sporangiophores sympodially and verticillately branched, with up to five branches in a whorl. The apophyses are globose, subglobose, bell-shaped and vasiform; columellae are globose, subglobose, flattened, rounded-topped and inconspicuous, whereas G. multispora forms sporangiophores sympodially and verticillately branched, with 2–3 branches in a whorl. Apophyses are pyriform to subglobose, and the columellae are hemispheric and some inconspicuous. It is curious that both species form sporangiophores branched in whorls, as to the best of our knowledge, this branch pattern has also been reported in G. namwonensis so far [28]. The Tmax of G. verticillata is 31 °C on MEA and PDA, but Tmax of G. multispora has not been given in the protologue [29]. There is no morphological description of G. bartikiae in the literature for comparison [67].
Figure 8. Gongronella verticillata (URM 9238, ex-type) on PDA at 25 °C after eight days. (A) Colony verse (left) and reverse (right). (B,C) Sporangiophore with sporangium. (D–G) Sporangiophore with columella. (H) Simply branched sporangiophore arising from stolon with rhizoid. (I) Sporangiophore with terminal columella and lateral whorled branches with columellae. (J) Rhizoid with chlamydospores attached. (K) Sporangiospores. Scale bars: (B,C) 20 μm; (D,F,J,K) 10 μm; (G,H) 15 μm; (E,I) 5 μm.
Figure 9. Gongronella verticillata (URM 9238, ex-type) on PDA at 25 °C after eight days. (A) Sporangiophores with sporangia. (B) Sporangiophores with a septum below the apophysis (left) and columellae. (C) =Bulbous rhizoid. (D) Chlamydospores attached to the mycelium. Scale bars: (A,B) 3 μm; (C) 10 μm; (D) 5 μm.

4. Discussion

Traditionally, new species of Mucorales fungi have been mostly delimited on a morphological basis, leading to further synonymies and generating controversy and doubts among taxonomists. In this context, species of Absidia and Gongronella have been sorted into other genera, as they shared similar morphological characteristics. For instance, G. butleri was first described as A. butleri Lend. in 1926, while Paine [68] proposed A. subpoculata Paine, which was later synonymized with G. butleri. In addition, some species of Absidia have been previously included in Tieghemella, Mycocladus, Proabsidia, Pseudoabsidia, and Protoabsidia [69,70,71]. On the other hand, species of Lichtheimia and Lentamyces have been previously treated as Absidia [72,73].
The advent of the molecular biology allowed the delimitation of new species of Absidia and Gongronella in the last 10–15 years in different countries, such as China, Brazil, South Korea, and Thailand, most of which were proposed based in sequences of ITS and/or LSU rDNA [20,21,29,30,41,42,74,75]. Wang et al. [30] highlighted that the ITS, LSU, Elongation Factor 1-alpha-EF-1α (TEF), act, and RNA Polymerase II Largest Subunit (RPB1) are reliable markers for identification of Gongronella species. Until 1969, only two Gongronella species, namely, G. butleri and G. lacrispora Hesselt. & J. JEllis [76,77], were known, and this number has increased to 28 species (as of 3 March 2026), mostly descried from China. Regarding Absidia, Ji et al. [44] sequenced TEF and act, as well as ITS and LSU, to delimit new species, and 69 new species have been described in the last 15 years [27].
Since Tmax has been successfully used as a discriminative characteristic for delimitation of mucoralean fungi, such as Backusella [39], Cunninghamella [78,79], Lichtheimia [80], Mucor [81], and Rhizopus [82], we believe in the taxonomic relevance of this characteristic for the delimitation of species within Absidia and Gongronella. In this paper, the Tmax of our new Absidia species did not vary much from the phylogenetically close species. However, we retrieved data from the literature on the Tmax of 50 species of Absidia (plus two new species described in this work) and realized that the Tmax varies considerably between species in this genus, from 24 °C (A. frigida) to 37 °C (A. ovalispora and A. zonata) (Table 1); therefore, this feature has taxonomic value. However, as it was also observed in other mucoralean genera [39,78,79,80], some overlapping may occur (e.g., A. menglianensis, A. tarda and A. longissima have a Tmax of 36 °C), which is why this feature should be used along with morphology and phylogeny for delimiting species in Absidia, as well as in other mucoralean genera.
We were unable to compare the Tmax of our new Gongronella species with other species due to the lack of Tmax data in the literature for this genus; therefore, it is still unknown whether this feature is taxonomically informative in Gongronella. Nevertheless, to the best of our knowledge we are providing the first data on Tmax for the genus. Regarding Absidia, Tmax data are available in the literature for only 52% of the known species, mostly for species from China and Korea, with a few species from Brazil and Australia (Table 1). Therefore, studies evaluating the Tmax of all species of both genera should be encouraged.
In this paper, we described, based on an integrated approach, four new species of Cunninghamellaceae from soil samples from the still poorly studied Cerrado biome. As far as we are aware, this is the first report of new Absidia and Gongronella species in this biome. Currently, only 17 species of Absidia have been reported in Brazil, including ten new species [19,20,53,74,75,83,84], whereas only four species of Gongronella were recorded in the country, including three new species [85,86]. All these species were isolated in the Caatinga and Atlantic Forest biomes. This paper increases the number of known species of Absidia and Gongronella to 96 and 30, respectively, as well as the knowledge of these fungi in the Brazilian Savanna. We believe that new inventories of Cunninghamellaceae in other Cerrado areas may unveil additional new species.

Author Contributions

Conceptualization: A.L.C.M.d.A.S. and L.W.S.d.F.; Material collection: L.W.S.d.F.; Methodology: L.W.S.d.F., A.R., A.L.C.M.d.A.S., L.W.S.d.F., C.S.d.O., M.O.d.C., J.D.P.B., M.A.B.d.S., H.B.L., C.M.d.S.-M., R.F.R.M. and L.d.O.F.; writing—preparation of the original draft: L.W.S.d.F., J.D.P.B., A.L.C.M.d.A.S., A.R. and H.B.L.; writing—revision and editing: L.d.O.F., A.R., C.M.d.S.-M., J.D.P.B., R.F.R.M., H.B.L. and A.L.C.M.d.A.S. All authors read and approved the final version of the manuscript.

Funding

This study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for awarding a doctoral fellowship to de Leslie W.S. de Freitas and a research grant to André L.C.M.A. Santiago (313401/2023-3). Jadson D.P. Bezerra and Layanne O. Ferro thank the CNPq, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG) for funding. This research was partially supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (RS-2022-NR075731).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The sequences presented in this study are openly available in https://www.ncbi.nlm.nih.gov/ (see Table 1 for the accession numbers). The alignments and phylogenetic tree files are available in FigShare (https://doi.org/10.6084/m9.figshare.31438165). All new taxa were registered in the Mycobank database (www.mycobank.org). This research was registered in the Brazilian SisGen system (A77E17B).

Acknowledgments

We thank D. Tatiana Baptista Gibertoni for collecting the soil samples.

Conflicts of Interest

The authors declare no conflicts of interest.

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