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Journal of Fungi
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25 September 2023

Seven New Species of Eurotiales (Ascomycota) Isolated from Tidal Flat Sediments in China

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1
State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China
2
College of Life Sciences, Yangtze University, Jingzhou 434025, China
*
Author to whom correspondence should be addressed.
J. Fungi2023, 9(10), 960;https://doi.org/10.3390/jof9100960
This article belongs to the Special Issue Diversity, Classification and Taxonomy of Aspergillus, Penicillium, Talaromyces and Related Genera (Eurotiales), 2nd Edition
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Abstract

Tidal flats have been reported to contain many microorganisms and play a critical role in maintaining biodiversity. In surveys of filamentous fungi from tidal flat sediments in China, seven new species of Eurotiales were discovered and described. Morphological characteristics and DNA sequence analyses of combined datasets of the BenA, CaM, and RPB2 regions support their placements and recognition as new species. Aspergillus liaoningensis sp. nov. and A. plumeriae sp. nov. belong to sections Candidi and Flavipedes of subgenus Circumdati, and A. subinflatus sp. nov. is a member of section Cremei of subgenus Cremei. Penicillium danzhouense sp. nov., P. tenue sp. nov., and P. zhanjiangense sp. nov. are attributed to sections Exilicaulis and Lanata-Divaricata of subgenus Aspergilloides. Talaromyces virens sp. nov. is in section Talaromyces. Detailed descriptions and illustrations of these novel taxa are provided. Their differences from close relatives were compared and discussed.

1. Introduction

Tidal flats, which link the ocean and the land, contain plentiful microorganisms [1]. Filamentous fungi were reported to be dominant in the intertidal fungal ecosystem [2,3]. The order Eurotiales is one of the most abundant groups, which contains five families with about 28 genera, including Aspergillus P. Micheli, Penicillium Link, and Talaromyces C.R. Benj. [4]. These genera are economically important in the fields of human health, agriculture, industry, and pharmaceutics [2,4,5,6,7]. For example, A. fumigatus Fresen. and T. marneffei (Segretain, Capponi & Sureau) Samson, N. Yilmaz, Frisvad & Seifert are two well-known human pathogens [8,9]. Penicillin, an effective anti-infective drug [10], was produced by P. chrysogenum Thom. Aspergillus oryzae (Ahlb.) Cohn can be used in food fermentation and was reported as a producer of enzymes [11,12]. Therefore, the discovery of these fungi is of theoretical and practical importance.
Due to the sophisticated classification, infrageneric taxonomy has commonly been used for Aspergillus, Penicillium, and Talaromyces [4]. With the application of multiple loci phylogeny, the inter-specific relationships within these genera have become more clear [13,14,15]. Currently, the genus Aspergillus comprises 483 species belonging to 27 sections [11,16,17,18,19,20,21,22], Penicillium contains 530 species in 33 sections [20,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38], and Talaromyces includes 204 species in 7 sections [6,18,32,39,40,41,42]. They show a broad range of habitats, such as woody substratum, sandy soil, tidal flats, water, and indoor air [43,44,45,46,47].
During the examinations of filamentous fungi isolated from tidal flat sediments in different provinces in China, seven undescribed taxa were encountered. Judging by the cultural and microscopic characteristics, they belong to Aspergillus, Penicillium, and Talaromyces. Their taxonomic placements were further confirmed by carrying out multilocus phylogenetic analyses of β-tubulin (BenA), calmodulin (CaM), and the second-largest subunit of RNA polymerase II (RPB2). The distinctions between the novel species and their close relatives were compared.

2. Materials and Methods

2.1. Sampling and Fungal Isolation

Tidal flat sediment samples were collected from Guangdong, Hainan, and Liaoning provinces from August to October 2020. Sediment samples were kept at 4 °C until used. Strains were isolated using a 3% sea salt medium with the dilution plate method and were preserved in the China General Microbiological Culture Collection Center (CGMCC). Dried cultures were deposited in the Herbarium Mycologicum Academiae Sinicae (HMAS).

2.2. Morphological Observations

Colony characteristics were observed and described following the method of Visagie et al. [14]. Four standard growth media were used: Czapek yeast autolysate agar (CYA, yeast extract Oxoid), malt extract agar (MEA, Amresco), yeast extract agar (YES), and potato dextrose agar (PDA) [48,49,50]. A twenty-five percent lactic acid (LA) solution was used as the mounting medium for the microscopic examinations of structures and measurements of the conidial head, stipe, phialide, vesicle, and conidia. The methods for inoculation, morphological observation, and digital recordings were performed following previous studies [51,52].

2.3. DNA Extraction, PCR Amplification, and Sequencing

Genomic DNA was extracted from fungal mycelium with the Plant Genomic DNA Kit (Tiangen Biotech (Beijing) Co., Ltd., Beijing, China). The sequences of nuclear the ribosomal DNA ITS1-5.8S-ITS2 (ITS), BenA, CaM, and RPB2 regions were amplified on an ABI 2720 Thermal Cycler (Applied Biosciences, Foster City, CA, USA) with the primer pairs ITS5 and ITS4 [53], T1 and Bt2a (or Bt2b) [54,55], CMD5 and CMD6 [56], and fRPB2-5F and fRPB2-7cR [57], respectively. PCR products were sequenced in both directions on an ABI 3730 DNA Sequencer (Applied Biosciences, Foster City, CA, USA).

2.4. Phylogenetic Analyses

The newly generated sequences and those retrieved from GenBank are listed in Table 1. They were assembled and aligned with BioEdit 7.0.5 [58] and manually edited. To evaluate statistical congruence amongst the loci BenA, CaM, and RPB2, the partition homogeneity test (PHT) was performed in PAUP*4.0b10 [59] with 1000 replicates. To determine the positions of these strains, the datasets of these regions belonging to Aspergillus sect. Candidi, Cremei and Flavipedes, Penicillium sect. Exilicaulis and Lanata-Divaricata, and Talaromyces sect. Talaromyces were compiled and analyzed by the maximum likelihood (ML) and Bayesian inference (BI) methods. ML analysis was performed with the default GTRCAT model using RAxML [60]. The BI analysis was conducted by MrBayes 3.2.5 [61]. Nucleotide substitution models were determined by MrModeltest 2.3 [62]. Dendrogram trees were visualized and edited using TreeView v. 1.6.6 [63] and FigTree v. 1.4.4 (http://tree.bio.ed.ac.uk/software/figtree/ (accessed on 25 November 2018)). A Bayesian inference posterior probability (BIPP) greater than 90% and a maximum likelihood bootstrap support (MLBS) greater than 70% were shown at the nodes.
Table 1. Names, strain numbers, and corresponding GenBank accession numbers of the taxa used in this study.

3. Results

3.1. Phylogenetic Analyses

To determine the positions of the Aspergillus strains, Hamigera avellanea Stolk & Samson and Penicillium expansum Link were used as outgroup taxa. The partition homogeneity tests (p = 0.01 and 0.25, respectively) indicated that the individual partitions were not highly incongruent [64]; thus, these three loci were combined for the phylogenetic analyses. The phylogenetic trees showed that strains CGMCC 3.25201 and 3.25202 were located in sect. Candidi and Flavipedes, respectively (Figure 1). The strain CGMCC 3.25201 shared a close relationship with A. subalbidus Visagie, Hirooka & Samson (BIPP/MLBS = 91%/89%), while CGMCC 3.25202 clustered with A. movilensis A. Nováková, Hubka, S.W. Peterson & M. Kolařík, receiving high supporting values (BIPP/MLBS = 100%/100%). The strain CGMCC 3.25203 grouped with other members of sect. Cremei ser. Inflati, receiving high statistic values (BIPP/MLBS = 100%/100%) (Figure 2).
Figure 1. BI tree generated from analyses of combined BenA, CaM, and RPB2 sequences of Aspergillus sect. Candidi and Flavipedes. BIPP ≥ 90% (left) and MLBS ≥ 70% (right) are indicated at nodes.
Figure 2. BI tree generated from analyses of combined BenA, CaM, and RPB2 sequences of Aspergillus sect. Cremei species. BIPP ≥ 90% (left) and MLBS ≥ 70% (right) are indicated at nodes.
In the phylogenetic analyses of Penicillium sect. Exilicaulis, H. avellanea and A. glaucus (L.) Link served as outgroup taxa. The partition homogeneity test (p = 0.01) indicated that the individual partitions were not highly incongruent [64]; thus, these three loci were combined for the phylogenetic analyses. The phylogenetic trees showed that strains CGMCC 3.25204 and 3.25205 were located in ser. Erubescentia (BIPP/MLBS = 100%/93%) (Figure 3). The strain CGMCC 3.25204 was clustered with P. canis S.W. Peterson, while strain CGMCC 3.25205 was grouped with P. striatisporum Stolk, both receiving full support.
Figure 3. BI tree generated from analyses of combined BenA, CaM, and RPB2 sequences of Penicillium sect. Exilicaulis species. BIPP ≥ 90% (left) and MLBS ≥ 70% (right) are indicated at nodes.
In the phylogenetic analyses of Penicillium sect. Lanata-Divaricata, H. avellanea and P. glabrum (Wehmer) Westling were used as outgroup taxa. The partition homogeneity test (p = 0.01) indicated that the individual partitions were not highly incongruent [64]; thus, these three loci were combined for the phylogenetic analyses. The strain CGMCC 3.25206 was placed in ser. Janthinella and clustered with P. janthinellum Biourge with high supporting values (BIPP/MLBS = 100%/100%) (Figure 4).
Figure 4. BI tree generated from analyses of combined BenA, CaM, and RPB2 sequences of Penicillium sect. Lanata-Divaricata species. BIPP ≥ 90% (left) and MLBS ≥ 70% (right) are indicated at nodes.
To determine the position of the Talaromyces strain, T. trachyspermus (Shear) Stolk & Samson and T. chongqingensis X.C. Wang & W.Y. Zhuang were used as outgroup taxa. The partition homogeneity test (p = 0.01) indicated that the individual partitions were not highly incongruent [64]; thus, these three loci were combined for the phylogenetic analyses. The phylogenetic tree showed that strain CGMCC 3.25207 was grouped with the others of sect. Talaromyces (BIPP/MLBS = 100%/100%) and was closely related to T. xishaensis X.C. Wang, L. Wang & W.Y. Zhuang (BIPP/MLBS = 100%/98%) (Figure 5).
Figure 5. BI tree generated from analyses of combined BenA, CaM, and RPB2 sequences of Talaromyces sect. Talaromyces species. BIPP ≥ 90% (left) and MLBS ≥ 70% (right) are indicated at nodes.

3.2. Taxonomy

  • Aspergillus liaoningensis C. Liu, Z.Q. Zeng & W.Y. Zhuang, sp. nov. Figure 6.
    Figure 6. Colonial and microscopic morphology of Aspergillus liaoningensis (CGMCC 3.25201). (a) Colonies after 7 days at 25 °C; top row left to right: obverse CYA, MEA, PDA, and YES; bottom row left to right: reverse CYA, MEA, PDA, and YES; (b–f) Conidiophores; (g) Conidia. Scale bars: (b–g) = 10 μm.
Fungal Names: FN 571613.
Etymology: The specific epithet refers to the type locality “Liaoning Province” of the fungus.
In: Aspergillus subgen. Circumdati sect. Candidi ser. Candidi.
Typification: CHINA, Liaoning Province, Donggang City, Zhongshan District, Yalu River Wetland Park, 39°49′0″ N 124°3′20″ E, in fluvial sediments, 13 October 2020, Chang Liu, tt32414 (holotype HMAS 247877, ex-type strain CGMCC 3.25201).
DNA barcodes: ITS ON563148, BenA ON231293, CaM ON470836, RPB2 ON470844.
Colony diam.: 7 days, 25 °C (unless stated otherwise): CYA 20–23 mm; CYA 37 °C, 8–9 mm; CYA 5 °C no growth; MEA 13–14 mm; PDA 16–22 mm; YES 18–20 mm.
Colony characteristics: On CYA 25 °C, 7 days: Colonies irregular, plain, cracked; margins narrow, nearly entire; mycelia white to cream; texture velutinous to floccose; sporulation dense; conidia en masse cream; no exudate, no soluble pigments; reverse cream to light yellow, white at periphery. On CYA 37 °C, 7 days: Colonies irregular, slightly protuberant in centers; margins narrow to moderately wide; mycelia cream; texture velutinous to floccose; sporulation dense; conidia en masse white to cream; no exudate, no soluble pigments; reverse dark cream, brown at centers. On MEA 25 °C, 7 days: Colonies nearly circular, slightly protuberant in centers; margins narrow to moderately wide, nearly entire; mycelia white to light cream; texture velutinous to floccose; sporulation dense in center, light cream; no exudate, no soluble pigments; reverse cream, brown at centers, white at periphery. On PDA 25 °C, 7 days: Colonies irregular, plain, cracked; margins narrow, nearly entire; mycelia white to grey; texture velutinous to floccose; sporulation dense; conidia en masse grey; no exudate, no soluble pigments; reverse cream, brown at centers, white at periphery. On YES 25 °C, 7 days: Colonies nearly circular, protuberant in centers, edges irregular; margins narrow, nearly entire; mycelium light grey at center, white at margin; texture velutinous to floccose; sporulation moderately dense; no exudate, no soluble pigments; reverse white, light yellow at centers.
Micromorphology: Conidial heads radiate; stipes thick walls, smooth, hyaline, not septate, 50–260 × 5.0–7.5 µm; vesicles globose to broad ellipsoidal, 5.5–17.3 × 5.3–17.1 µm; biseriate; metulae cylindrical to obovate, 5.2–8.0 × 3.3–5.1 µm, covering two-thirds to almost the entire surface of the vesicle; phialides flask-shaped to acerose, 4.8–8.4 × 2.3–3.1 µm; conidia globose to subglobose, smooth, 2.6–4.2 µm in diam.
Note: This species is phylogenetically related to A. subalbidus (Figure 1), but the latter differs in that it lacks growth on CYA at 37 °C, has faster growth rates on MEA (17–19 mm) and YES (25–30 mm) at 25 °C, and its colonies do not crack on CYA and PDA [14].
  • Aspergillus plumeriae C. Liu, Z.Q. Zeng & W.Y. Zhuang, sp. nov. Figure 7.
    Figure 7. Colonial and microscopic morphology of Aspergillus plumeriae (CGMCC 3.25202). (a) Colonies after 7 days at 25 °C; top row left to right: obverse CYA, MEA, PDA, and YES; bottom row left to right: reverse CYA, MEA, PDA, and YES; (b–h) Conidiophores; (i) Conidia. Scale bars: (b–i) = 10 μm.
Fungal Names: FN 571614.
Etymology: The specific epithet refers to the yellowish-white colony on PDA.
In: Aspergillus subgen. Circumdati sect. Flavipedes ser. Spelaei.
Typification: CHINA, Liaoning Province, Dalian City, Zhongshan District, Binhai East Road, 38°52′1″ N 121°41′20″ E, in tidal flat sediments, 12 October 2020, Chang Liu, tt30226 (holotype HMAS 247878, ex-type strain CGMCC 3.25202).
DNA barcodes: ITS ON563147, BenA ON231292, CaM ON470835, RPB2 ON470843.
Colony diameter: 7 days, 25 °C (unless stated otherwise): CYA 24–26 mm; CYA 37 °C no growth; CYA 5 °C no growth; MEA 18–22 mm; PDA 17–19 mm; YES 25–26 mm.
Colony characteristics: On CYA 25 °C, 7 days: Colonies nearly circular, plain, slightly protuberant in centers; margins narrow to moderately wide, nearly entire; mycelia white to cream; texture velutinous; sporulation dense, conidia en masse white; no exudate, no soluble pigments; reverse light yellow. On MEA 25 °C, 7 days: Colonies nearly circular, wrinkled, slightly protuberant in centers, radially sulcate; margins moderately wide, nearly entire; mycelia white to cream; texture velutinous; sporulation dense in center, cream to light yellow; no exudate, no soluble pigments; reverse yellowish-brown. On PDA 25 °C, 7 days: Colonies nearly circular, wrinkled, slightly concave at centers, radially sulcate; margins moderately wide, nearly entire; mycelia white, bright yellow at center; texture velutinous to floccose; sporulation dense in center, bright yellow; no exudate, no soluble pigments; reverse light–brown at centers, white at periphery. On YES 25 °C, 7 days: Colonies nearly circular, wrinkled, slightly concave at centers, radially sulcate; margins moderately wide, nearly entire; mycelium white to cream at center, white at margin; texture velutinous; sporulation moderately dense, white to cream; no exudate, no soluble pigments; reverse white to light yellow.
Micromorphology: Conidial heads radiate; stipes thick walls, smooth, hyaline or blackish, not septate, longer than 340 µm; vesicles globose to subglobose, 13–22.7 µm in diam.; biseriate; metulae cylindrical, 4.5–7.8 × 2.6–4.9 µm, covering two-thirds to almost the entire surface of the vesicle; phialides flask-shaped to acerose, slightly curved at the mouth, 5.4–8.4 × 1.7–2.9 µm; conidia globose to subglobose, smooth, 2.6–3.3 µm in diam.
Note: Among the known species of Aspergillus, A. plumeriae is distinct because of its yellowish-white colony on PDA. It is phylogenetically related to A. movilensis (Figure 1), but the latter differs in its ability to grow at 37 °C and production of pyriform vesicles with smaller sizes (5.0–16 µm in diam.) [65].
  • Aspergillus subinflatus C. Liu, Z.Q. Zeng & W.Y. Zhuang, sp. nov. Figure 8.
    Figure 8. Colonial and microscopic morphology of Aspergillus subinflatus (CGMCC 3.25203). (a) Colonies after 7 days at 25 °C; top row left to right: obverse CYA, MEA, PDA, and YES; bottom row left to right: reverse CYA, MEA, PDA, and YES; (b–h) Conidiophores; (i) Conidia. Scale bars: (b–i) = 10 μm.
Fungal Names: FN 571615.
Etymology: The specific epithet refers to the similarity of the fungus to A. inflatus.
In: Aspergillus subgen. Cremei sect. Cremei. Ser. Inflati.
Typification: CHINA, Hainan Province, Ledong Li Autonomous County, Liguo Town, 108°56′22″ N 18°24′38″ E, in mangrove sediments, 3 September 2020, Hai-Yan Zhu, tt14122 (holotype HMAS 247879, ex-type strain CGMCC 3.25203).
DNA barcodes: ITS ON563146, BenA ON231291, CaM ON470834, RPB2 ON470845.
Colony diameter: 7 days, 25 °C (unless stated otherwise): CYA 16–17 mm; CYA 37 °C 4–5 mm; CYA 5 °C no growth; MEA 13–14 mm; PDA 17–18 mm; YES 14–16 mm.
Colony characteristics: On CYA 25 °C, 7 days: Colonies nearly circular, wrinkled, protuberant in centers, radially sulcate; margins narrow to moderately wide, nearly entire; mycelia white to grey; texture velutinous; sporulation dense; conidia en masse grey; no exudate, no soluble pigments; reverse light yellow. On CYA 37 °C, 7 days: Colonies nearly circular, lain; mycelia light pink to white; texture velutinous; no sporulation; no exudate, no soluble pigments; reverse light pink to white. On MEA 25 °C, 7 days: Colonies nearly circular, slightly wrinkled, slightly protuberant in centers; margins wide to moderately wide, nearly entire; mycelia white to grey; texture velutinous to floccose; sporulation dense in center, grey; no exudate, no soluble pigments; reverse yellowish-brown, yellow to white at centers. On PDA 25 °C, 7 days: Colonies nearly circular, slightly wrinkled, slightly protuberant in centers; margins moderately wide, nearly entire; mycelia white to light grey; texture velutinous to floccose; sporulation dense in center, light grey; no exudate, no soluble pigments; reverse pale yellow. On YES 25 °C, 7 days: Colonies nearly circular, wrinkled, protuberant in centers; margins narrow, nearly entire; mycelium white, light grey at center; texture velutinous to floccose; sporulation moderately dense, white; no exudate, no soluble pigments; reverse yellow, white at periphery.
Micromorphology: Conidial heads radiate; stipes smooth-walled, slightly swollen at the apex, 12–318 × 3.5–5.0 µm; vesicle ellipsoidal, 5.3–17 × 3.1–6.4 μm; metulae developing successively on the vesicle and also occurring on its subterminal and terminal portion, swollen, cylindrical to obovate, 3.8–9.4 × 2.5–4.1 µm; phialides flask-shaped to acerose, tapering into thin neck, 2.5–7.9 × 1.9–2.6 µm; conidia globose to subglobose, smooth to finely rough, 1.6–2.3 μm in diam.
Note: This species is morphologically similar and phylogenetically related to A. inflatus (Figure 2) but differs in that its metulae occur at the subterminal and terminal positions [13,66]. Moreover, there are 69 bp, 74 bp, and 88 bp divergences in the BenA, CaM, and RPB2 regions between the ex-type cultures of the two taxa (CGMCC 3.25203 and CBS 682.70).
  • Penicillium danzhouense C. Liu, Z.Q. Zeng & W.Y. Zhuang, sp. nov. Figure 9.
    Figure 9. Colonial and microscopic morphology of Penicillium danzhouense (CGMCC 3.25204). (a) Colonies after 7 days at 25 °C; top row left to right: obverse CYA, MEA, PDA, and YES; bottom row left to right: reverse CYA, MEA, PDA, and YES; (b–g) Conidiophores; (h,i) Conidia. Scale bars: (b–i) = 10 μm.
Fungal Names: FN 571616.
Etymology: The specific epithet refers to the type locality “Danzhou City” of the fungus.
In: Penicillium subgen. Aspergilloides sect. Exilicaulis ser. Erubescentia.
Typification: CHINA, Hainan Province, Danzhou City, Eman Town, 19°51′24″ N 109°13′54″ E, in tidal flat sediments, 2 September 2020, Hai-Yan Zhu, tt13610 (holotype HMAS 247880, ex-type strain CGMCC 3.25204).
DNA barcodes: ITS ON563150, BenA ON231295, CaM ON470838.
Colony diameter: 7 days, 25 °C (unless stated otherwise): CYA 21–24 mm; CYA 37 °C 6–7 mm; CYA 5 °C no growth; MEA 14–17 mm; PDA 17–19 mm; YES 12–15 mm.
Colony characteristics: On CYA 25 °C, 7 days: Colonies nearly circular, deep, wrinkled, protuberant at centers, radially sulcate; margins narrow, entire; mycelia white, light pink at center; texture velutinous to floccose; no sporulation; exudate colorless, no soluble pigments; reverse yellow. On CYA 37 °C, 7 days: Colonies nearly circular, plain, strongly wrinkled; margins narrow; mycelia white; texture velutinous to floccose; no sporulation; no exudate, no soluble pigments; reverse light yellow. On MEA 25 °C, 7 days: Colonies nearly circular, concave at centers, protuberant at margins; margins narrow to moderately wide, nearly entire; mycelia white, light grey at center; texture velutinous to floccose; sporulation sparse, light grey; no exudate, no soluble pigments; reverse yellow, white at periphery. On PDA 25 °C, 7 days: Colonies nearly circular, slightly protuberant at centers, edges irregular; margins narrow to moderately wide, nearly entire; mycelia white to cream, grey at center; texture velutinous to floccose; sporulation moderately dense, grey; no exudate, no soluble pigments; reverse light yellow to cream. On YES 25 °C, 7 days: Colonies nearly circular, deep, protuberant at centers; margins narrow, entire; mycelium white; texture velutinous to floccose; sporulation sparse; no exudate, no soluble pigments; reverse yellow, white at periphery.
Micromorphology: Conidiophores monoverticillate, rarely biverticillate; stipes smooth-walled, 12–40 × 2.0–3.0 µm; phialides flask-shaped to acerose, 2–5 per metula, 4.6–8.7 × 1.7–2.2 µm; conidia globose to subglobose, smooth to finely roughened, 2.2–3.0 µm in diam.
Note: This species is phylogenetically related to P. catenatum (Figure 3), but the latter differs in its larger phialides (8.0–12 × 2.5–3.0 µm) [67]. Moreover, the growth rates of P. catenatum were relatively slower than P. danzhouense, and the former inhabited the desert rather than tidal flat sediments.
  • Penicillium tenue C. Liu, Z.Q. Zeng & W.Y. Zhuang, sp. nov. Figure 10.
    Figure 10. Colonial and microscopic morphology of Penicillium tenue (CGMCC 3.25205). (a) Colonies after 7 days at 25 °C; top row left to right: obverse CYA, MEA, PDA, and YES; bottom row left to right: reverse CYA, MEA, PDA, and YES; (b–d) Conidiophores; (e) Conidia. Scale bars: (b–e) = 10 μm.
Fungal Names: FN 571617.
Etymology: The specific epithet refers to the slender phialides.
In: Penicillium subgen. Aspergilloides sect. Exilicaulis ser. Erubescentia.
Typification: CHINA, Hainan Province, Danzhou City, Duntou Town, 19°09′06″ N 108°40′19″ E, in tidal flat sediments, 2 September 2020, Hai-Yan Zhu, tt13918 (holotype HMAS 247881, ex-type strain CGMCC 3.25205).
DNA barcodes: ITS ON563151, BenA ON231296, CaM ON470839, RPB2 ON470842.
Colony diameter: 7 days, 25 °C (unless stated otherwise): CYA 11–12 mm; CYA 37 °C 12–13 mm; CYA 5 °C no growth; MEA 11–14 mm; PDA 12–13 mm; YES 11–12 mm.
Colony characteristics: On CYA 25 °C, 7 days: Colonies nearly circular, deep, protuberant at centers, radially sulcate; margins narrow, entire; mycelia white, light yellow at center; texture velutinous to floccose; no sporulation; exudate yellow, no soluble pigments; reverse yellow, deepens in the center. On CYA 37 °C, 7 days: Colonies nearly circular, concave at centers, protuberant at margins, slightly wrinkled, radially sulcate; margins narrow; mycelia white, light yellow at centers; texture velutinous to floccose; sporulation sparse; exudate yellow to yellowish-brown, no soluble pigments; reverse yellow, yellowish-brown in centers. On MEA 25 °C, 7 days: Colonies nearly circular, protuberant at centers; margins narrow to moderately wide, nearly entire; mycelia white, light yellow at center; texture velutinous to floccose; sporulation sparse; no exudate, no soluble pigments; reverse yellowish-brown, white at periphery. On PDA 25 °C, 7 days: Colonies nearly circular, protuberant at centers; margins narrow, nearly entire; mycelia white to yellow; texture velutinous to floccose; sporulation sparse; exudate yellow to yellowish-brown, no soluble pigments; reverse light yellow. On YES 25 °C, 7 days: Colonies nearly circular, deep, concave at centers, protuberant at margins; margins narrow, entire; mycelium white; texture velutinous to floccose; no sporulation; no exudate, no soluble pigments; reverse yellowish-brown, white at center and periphery.
Micromorphology: Conidiophores monoverticillate; stipes smooth-walled, 5.0–24 × 2.0–3.0 µm; phialides flask-shaped to acerose, 2–4 metula, 3.1–6.1 × 1.6–2.1 µm; conidia globose to subglobose, spinulose, 2.1–2.7 µm in diam.
Note: This species is phylogenetically related to P. striatisporum (Figure 3), but the latter differs in its ellipsoidal to ovoid and striate conidia [68]. Sequence comparisons between the ex-type cultures of the two species revealed that 8 bp, 12 bp, and 3 bp divergences were detected for the BenA, CaM, and RPB2 regions.
  • Penicillium zhanjiangense C. Liu, Z.Q. Zeng & W.Y. Zhuang, sp. nov. Figure 11.
    Figure 11. Colonial and microscopic morphology of Penicillium zhanjiangense (CGMCC 3.25206). (a) Colonies after 7 days at 25 °C; top row left to right: obverse CYA, MEA, PDA, and YES; bottom row left to right: reverse CYA, MEA, PDA, and YES; (b–h) Conidiophores; (i) Conidia. Scale bars: (b–i) = 10 μm.
Fungal Names: FN 571618.
Etymology: The specific epithet refers to the type locality “Zhanjiang City“ of the fungus.
In: Penicillium subgen. Aspergilloides section sect. Lanata-Divaricata ser. Janthinella.
Typification: CHINA, Guangdong Province, Zhanjiang City, Xuwen County, Southeast Village of China Mainland, 20°59′09″ N 109°40′53″ E, in tidal flat sediments, 30 August 2020, Hai-Yan Zhu, tt12003 (holotype HMAS 247882, ex-type strain CGMCC 3.25206).
DNA barcodes: ITS ON563149, BenA ON231294, CaM ON470837.
Colony diameter: 7 days, 25 °C (unless stated otherwise): CYA 28–30 mm; CYA 37 °C 42–43 mm; CYA 5 °C no growth; MEA 41–48 mm; PDA 36–37 mm; YES 22–24 mm.
Colony characteristics: On CYA 25 °C, 7 days: Colonies nearly circular, concave at centers, protuberant at margins, wrinkled, radially sulcate; margins narrow to moderately wide, nearly entire; mycelia white, light grey at center; texture velutinous to floccose; sporulation sparse; conidia en masse cream to light grey; no exudate, no soluble pigments; reverse yellowish-brown, light green to blackish-green at centers, white at periphery. On CYA 37 °C, 7 days: Colonies nearly circular, concave at centers, protuberant at margins, wrinkled, radially sulcate; margins narrow; mycelia pink, white to yellowish-grey at centers; texture velutinous; texture velutinous to floccose; sporulation sparse; exudate pink to pinkish-brown, no soluble pigments; reverse pink to dark pink, yellow at periphery. On MEA 25 °C, 7 days: Colonies nearly circular, concave at centers, protuberant at margins, wrinkled, radially sulcate; margins narrow to moderately wide, nearly entire; mycelia cream, brown at center; texture velutinous to floccose; sporulation dense; conidia en masse brownish-yellow; no exudate, no soluble pigments; reverse yellowish-brown, deepens in the center. On PDA 25 °C, 7 days: Colonies nearly circular, concave at centers, protuberant at margins, slightly wrinkled, radially sulcate; margins narrow to moderately wide, nearly entire; mycelia light yellow, brown at center; texture velutinous to floccose; sporulation dense; conidia en masse brownish-yellow; no exudate, no soluble pigments; reverse light green to dark green, deepens in the center. On YES 25 °C, 7 days: Colonies nearly circular, deep, concave at centers, protuberant at margins, slightly wrinkled, radially sulcate; margins narrow, nearly entire; mycelium white to cream; texture velutinous to floccose; sporulation sparse; no exudate, no soluble pigments; reverse yellow, white at periphery.
Micromorphology: Conidiophores monoverticillate to biverticillate; stipes smooth-walled, 24–170 × 2.4–3.7 µm; metulae cylindrical, 8.1–28.3 × 2.2–3.1 µm; phialides flask-shaped to acerose, tapering into thin neck, 2–3 per metula, 4.9–15.5 × 1.9–2.9 µm; conidia globose to subglobose, smooth to finely roughened, 2.0–3.3 µm in diam.
Note: This species is phylogenetically related to P. janthinellum (Figure 4), but the latter differs in its faster growth rate on YES (44–46 mm) at 25 °C, while a slower growth rate was observed on CYA at 37 °C (20–30 mm) [69].
  • Talaromyces virens C. Liu, Z.Q. Zeng & W.Y. Zhuang, sp. nov. Figure 12.
    Figure 12. Colonial and microscopic morphology of Talaromyces virens (CGMCC 3.25207). (a) Colonies after 7 days at 25 °C; top row left to right: obverse CYA, MEA, PDA, and YES; bottom row left to right: reverse CYA, MEA, PDA, and YES; (b–h) Conidiophores; (i) Conidia. Scale bars: (b–i) = 10 μm.
Fungal Names: FN 571619.
Etymology: The specific epithet refers to the green conidia.
In: Talaromyces section Talaromyces.
Typification: CHINA, Hainan Province, Wenchang City, Dongjiao Town, 110°50′40″ N 19°32′27″ E, in tidal flat sediments, 1 September 2020, Hai-Yan Zhu, tt13401 (holotype HMAS 247883, ex-type strain CGMCC 3.25207).
DNA barcodes: ITS ON563152, BenA ON231297, CaM ON470840, RPB2 ON470841.
Colony diameter: 7 days, 25 °C (unless stated otherwise): CYA 19–20 mm; CYA 37 °C 6–7 mm; CYA 5 °C no growth; MEA 23–26 mm; PDA 22–23 mm; YES 18–19 mm.
Colony characteristics: On CYA 25 °C, 7 days: Colonies nearly circular, protuberant in centers; margins narrow to moderately wide, nearly entire; mycelia white; texture velutinous; sporulation dense; conidia en masse dark olive green; no exudate, no soluble pigments; reverse light khaki, light brown at centers, light yellow and white at periphery. On CYA 37 °C, 7 days: Colonies nearly circular, deep, wrinkled, deeply concave in centers; margins narrow; mycelia white; texture velutinous; sporulation dense; conidia en masse grey; no exudate, no soluble pigments; reverse grey or white. On MEA 25 °C, 7 days: Colonies nearly circular, slightly protuberant in centers; margins wide, nearly entire; mycelia white; texture velutinous; sporulation dense in center, olive-drab; no exudate, no soluble pigments; reverse light yellow, light orange at centers. On PDA 25 °C, 7 days: Colonies nearly circular, protuberant in centers; margins wide, nearly entire; mycelia white; texture velutinous to floccose; sporulation dense in center, deep green; no exudate, no soluble pigments; reverse white, light coral to red at centers, white at periphery. On YES 25 °C, 7 days: Colonies nearly circular, protuberant in centers; margins narrow to moderately wide, nearly entire; mycelium gray-green to yellowish-green at center, white at margin; texture velutinous to floccose; sporulation moderately dense, yellow to green; no exudate, no soluble pigments; reverse white, dark yellow at centers.
Micromorphology: Conidiophores biverticillate; stipes smooth-walled, 147–220 × 2.4–4.0 µm; metulae cylindrical, 9.1–14.1 × 2.5–3.4 µm; phialides flask-shaped to acerose, tapering into thin neck, 2–6 per metula, 7.7–11.2 × 2.2–3.3 µm; conidia globose to subglobose, green, 2.4–4.0 µm in diam.
Note: This species is morphologically and phylogenetically related to T. xishaensis (Figure 5). However, the latter has greyish-green colonies on CYA, yellowish-green colonies on MEA, and grey to bluish-green colonies on YES [70].

4. Discussion

The genus Aspergillus is divided into six subgenera with 27 sections [13,22]. Our new species A. liaoningensis was well-located in the ser. Candidi of sect. Candidi (BIPP/MLBS = 100%/100%) (Figure 1). Many species within this section have been reported as producers of secondary metabolites, such as taichunamides, shikimic acid derivatives, and terpene-derived taichunins [71,72,73]. Studies on the metabolic application of A. liaoningensis are surely our future goal. Aspergillus plumeriae belongs to ser. Spelaei of sect. Flavipedes, which is in accordance with the growth rate at 37 °C [65]. Aspergillus subinflatus was classified as a member of ser. Inflati, sect. Cremei of subgen. Cremei, and is most related to A. inflatus in both phylogeny and morphology. However, sequence comparisons revealed that there were 69 bp, 74 bp, and 88 bp unmatched loci detected in the BenA, CaM, and RPB2 regions between them.
Both P. danzhouense and P. tenue form monoverticillate conidiophores, consistent with the other members of ser. Erubescentia in sect. Exilicaulis [7,48,74,75]. The phylogenetic results indicate that P. danzhouense is closely related to P. catenatum with high statistical support values (Figure 3); however, the latter differs in having larger phialides (8.0–12 × 2.5–3.0 µm vs. 4.6–8.7 × 1.7–2.2 µm) [67]. Moreover, there were 20 bp and 56 bp divergences in the BenA and CaM regions between them. Our results also showed that P. tenue was grouped with P. striatisporum, receiving full support (Figure 3), but the latter possesses ellipsoidal to ovoid and striate conidia [68]. Penicillium dravuni, a marine-derived species belonging to this section, was not included in our phylogenetic analysis because no sequence data are available at present. However, it can be easily distinguished from P. danzhouense (white to light pink colonies) and P. tenue (white to light yellow colonies) because it forms yellow-gray colonies and has faster growth rates (25–35 mm vs. 21–24 mm, and 11–12 mm in CYA at 25 °C) [76].
Sect. Lanata-Divaricata is a species-rich section in Penicillium, and about 85 species have been described hitherto [4,20,27,28,31,33]. Our phylogenetic tree indicated that P. zhanjiangense was well-located among other species of sect. Lanata-Divaricata, with high supporting values (BIPP/MLBS = 97%/100%), and it clustered with P. janthinellum (BIPP/MLBS = 100%/100%) (Figure 4). A new species of the section was added in this study.
Since the establishment of Talaromyces, eight sections have been proposed: Bacillispori, Helici, Islandici, Purpurei, Subinflati, Talaromyces, Tenues, and Trachyspermi [40]. The phylogenetic overview of the sect. Talaromyces was conducted by Wang and Zhuang [40], and about 88 species are currently known in this section [40,41,42]. The three-locus phylogeny formed a well-supported monophyletic group (BIPP/MLBS = 100%/100%) and indicates that T. virens is related to but distinct from T. xishaensis (Figure 5). They can be easily distinguished by their different colony features on different media [70]. Moreover, there are 11 bp, 34 bp, and 32 bp unmatched loci detected in the BenA, CaM, and RPB2 regions between the ex-type cultures (CGMCC 3.25207 and CGMCC 3.17995).
Species of the genera Penicillium, Aspergillus, and Talaromyces have been isolated from various substrates, including dust, soil, dung, cloth, human tissue, plants, and insects [4,11]. Due to the special ecological habitat, the fungi of these groups within tidal flats have high biodiversity and are an important source of active natural products [77,78,79,80]. Recently, three novel taxa of Penicillium were reported in tidal flats [28]. Similarly, the present study introduces three species of Aspergillus as well as three taxa of Penicillium and one of Talaromyces derived from tidal flat sediments. With the extensive use of molecular approaches, large-scale surveys in these unexplored tidal flats regions will significantly improve our knowledge of fungal species diversity in special ecological environments.

5. Conclusions

The filamentous fungi from tidal flat sediments in China were surveyed, and seven novel taxa of the genera Aspergillus, Penicillium, and Talaromyces were discovered. With the joining of the new species, the phylogenetic relationships among species of these three genera were updated.

Author Contributions

Conceptualization, Z.-Q.Z.; methodology, formal analysis, and investigation, C.L. and Z.-Q.Z.; resources and data curation, W.-Y.Z. and Z.-Q.Z.; original draft preparation and writing, C.L., X.-C.W., Z.-H.Y., Z.-Q.Z. and W.-Y.Z.; supervision and project administration, Z.-Q.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This project was supported by the National Natural Science Foundation of China (32270009, 31870012, 31750001); the Biological Resources Programme, Chinese Academy of Sciences (KFJ-BRP-017-082); the National Project on Scientific Groundwork, Ministry of Science and Technology of the People’s Republic of China (2019FY100700); and the Frontier Key Program of Chinese Academy of Sciences (QYZDY-SSW-SMC029).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The names of the new species were formally registered in the database Fungal Names (https://nmdc.cn/fungalnames (accessed on 10 July 2023)). Specimens were deposited in the Herbarium Mycologicum Academiae Sinicae (https://nmdc.cn/fungarium/ (accessed on 18 February 2023)). Cultures were deposited in the China General Microbiological Culture Collection Center (https://cgmcc.net/ (accessed on 18 July 2023)). The newly generated sequences were deposited in GenBank (https://www.ncbi.nlm.nih.gov/genbank (accessed on 20 May 2022)).

Acknowledgments

The authors would like to thank Feng-Yan Bai and Hai-Yan Zhu for collecting samples jointly for this study.

Conflicts of Interest

The authors declare no conflict of interest.

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Genetic and Molecular Evidence of a Tetrapolar Mating System in the Edible Mushroom Grifola frondosa
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