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. 2023 Oct 9;51(5):288–299. doi: 10.1080/12298093.2023.2257997

Re-Identification of Aspergillus Subgenus Circumdati Strains in Korea Led to the Discovery of Three Unrecorded Species

Anbazhagan Mageswari a, Yunhee Choi a, Le Dinh Thao a,b, Daseul Lee a, Dong-Hyun Kim a, Myung Soo Park c, Seung-Beom Hong a,✉
PMCID: PMC10621256  PMID: 37929011

Abstract

Aspergillus is one of the largest and diverse genera of fungi with huge economical, biotechnological, and social significance. Taxonomically, Aspergillus is divided into six subgenera comprising 27 sections. In this study, 235 strains of Aspergillus subgenus Circumdati (section: Candidi, Circumdati, Flavi, Flavipedes, Nigri, and Terrei) preserved at the Korean Agricultural Culture Collection (KACC) were analyzed and re-identified using a combined dataset of partial β-tubulin (BenA), Calmodulin (CaM) gene sequences and morphological data. We confirmed nineteen species to be priorly reported in Korea (A. neotritici, A. terreus, A. floccosus, A. allahabadii, A. steynii, A. westerdijkiae, A. ochraceus, A. ostianus, A. sclerotiorum, A. luchuensis, A. tubingensis, A. niger, A. welwitschiae, A. japonicus, A. nomius, A. tamarii, A. parasiticus, A. flavi, and A. oryzae). Among the studied strains, three species (A. subalbidus, A. iizukae, and A. uvarum), previously unreported or not officially documented, were discovered in Korea, to the best of our knowledge. We have given a detailed description of the characteristic features of the three species, which remain uncharted in Korea.

Keywords: Aspergillus subgenus circumdati, unrecorded species, A. subalbidus, A. iizukae, A. uvarum

1. Introduction

The genus Aspergillus is one of the most ubiquitous and cosmopolitan filamentous fungi of the order Eurotiales. Species belonging to this genus are ecologically abundant and can be found in the air, soil, vegetation as well as indoor environments [1,2]. Several of the Aspergillus species are economically, biotechnologically, and medically important due to their ability to produce enzymes, organic acids, antibiotics, and other bioactive metabolites [3]. Nevertheless, some of the species are also frequently reported for their detrimental effects such as food spoilage, mycotoxin production, and as causal agents of mycoses [4]. The genus was first introduced in 1729 and has more than one thousand recorded taxa in the database “Index Fungorum.” According to a recent research on the Aspergillus taxonomy, the genus comprises – six subgenera (namely, Aspergillus, Circumdati, Cremei, Fumigati, Nidulantes, and Polypaecilum), 27 sections, 75 series with 446 species [5].

Species delimitation is a vital aspect of taxonomic research and precise identification of strains is essential for targeted applications as well as linking of research taking place across the world. In this regard, microbial resource centers play an important role in phenetic analysis and conservation of microbial strains of potential value in industry, medicine, environment, agriculture, and other scientific purposes [6]. Among such institutions around the world, Korean Agricultural Culture Collection (KACC) is a major research organization specializing in identification and long-term storage of fungal biodiversity which can serve as a potential source of useful fungal strains. It was established as a part of the Rural Development Administration (RDA) in the year 1995 and the collection currently preserves 14,079 strains of fungi from 3346 species covering all major fungal taxonomic groups, and among these, 9.2% (n = 1297) belong to Aspergillus.

In earlier days, Aspergillus strains were identified based on their morphology and deposited in KACC. In the last two decades, morphology-based identification was often found to be misleading, especially within the Aspergillus sections due to the occurrence of cryptic species [7]. Therefore, for accurate identification of Aspergillus, a polyphasic approach has been proposed which includes morphological analysis as well as molecular analysis, ecology, and extrolite profiling [8]. Basically, current identification and phylogeny of Aspergillus can be majorly relied on DNA barcodes which include internal transcribed spacer (ITS) region, Calmodulin (CaM), β-tubulin (BenA), and the RNA polymerase II second largest subunit (RPB2) [2].

At present, to improve the quality of the KACC resources, focus has shifted towards re-identification of the conserved strains using molecular techniques mainly based on DNA barcodes mentioned above, in addition to their morphological characteristics. In this context, a subset of Aspergillus strains stored in the KACC from 1995 to 2022 was studied using their sequence data as well as morphological characteristics. The identification of all strains was based on partial β-tubulin (BenA) and Calmodulin (CaM) gene sequences. To date, 81 different Aspergillus species have been described from Korea [9,10]. This study aimed to re-identify Korean strains of Aspergillus subgenus Circumdati preserved in KACC and provide a description of hitherto unrecorded species in Korea based on their morphological and molecular characteristics. This study complements existing knowledge on the diversity of Aspergillus species in Korea.

2. Materials and methods

2.1. Strains

A total of 235 strains belonging to genus Aspergillus subgenus Circumdati in KACC were studied. All the reagents and media used in the study were procured from Merck, Seoul, South Korea and Oxoid, Basingstoke, UK. The strains were isolated from diverse ecological niches in Korea. All the strains were revived in 4 mL of Malt extract broth, and subsequently transferred to malt extract agar (MEA). The strains examined in the study have been listed in Table 1.

Table 1.

Aspergillus subgenus Circumdati strains used in this study.

Section Re-identified scientific name Scientific name by depositor KACC number Deposited year Substrate Region Location RDA GeneBank accession no.
  CaM BenA
Candidi A. subalbidus a A. candidus 46481 2011 Meju Gyeongsangbuk-do Chilgok-gun RDA0061631 RDA0061627
A. candidus 46482 2011 Meju Gyeonggi-do Icheon-si RDA0061632 RDA0061628
A. neotritici A. candidus 44245 2005 Rice Seoul Seongbuk-gu RDA0061630 RDA0061629
A. tritici 46483 2011 Meju Gyeonggi-do Yeoju-si RDA0062637 RDA0062638
A. tritici 48027 2015 Nuruk Gyeongsangnam-do Jinju-si RDA0062591 RDA0062592
Terrei A. allahabadii A. allahabadii 49964 2021 Soil Jeollanam-do Damyang-gun RDA0062655 RDA0062656
A. floccosus A. floccosus 49740 2020 Soil Jeollabuk-do Buan-gun RDA0062653 RDA0062654
A. terreus A. terreus 47277 2013 Rice straw Jeollanam-do Haenam-gun RDA0062649 RDA0062650
A. terreus 47390 2014 Air Korea Anseong-si RDA0062647 RDA0062648
A. terreus 48446 2017 Water Busan Saha-gu, RDA0062651 RDA0062652
Flavipedes A. iizukae A. flavipes 43789 2008 Creosote contaminated soil Seoul Sangam-dong RDA0064667 RDA0064670
A. iizukae 48444 2017 Crab Busan Saha-gu RDA0064668 RDA0064672
A. iizukae 48864 2019 Soil Gyeongsangnam-do Miryang-si RDA0064669 RDA0064671
Circumdati A. ochraceus A. ochraceus 46484 2011 Meju Jeollanam-do Haenam-gun RDA0064675 RDA0064694
A. ochraceus 46485 2011 Meju Gyeonggi-do Icheon-si RDA0064676 RDA0064695
A. ochraceus 46486 2011 Meju Gyeonggi-do Yeoju-si RDA0064677 RDA0064696
A. ochraceus 47132 2013 Soybean Korea unknown RDA0064682 RDA0064701
A. ochraceus 47273 2013 Rice straw Jeollabuk-do Sunchang-gun RDA0064685 RDA0064704
A. ochraceus 47384 2014 Air Gyeongsangbuk-do Chilgok-gun RDA0064687 RDA0064706
A. ostianus A. ostianus 47134 2013 Soybean Korea unknown RDA0064711 RDA0064702
A. sclerotiorum A. sclerotiorum 47387 2014 Air Gyeongsangbuk-do Chilgok-gun RDA0064688 RDA0064707
A. sclerotiorum 48445 2017 Rice Jeollanam-do Gwangju-si RDA0064691 RDA0064710
A. steynii A. ochraceus 46821 2012 Air Gyeongsangbuk-do Chilgok-gun RDA0064679 RDA0064698
A. steynii 47388 2014 Air Gyeonggi-do Icheon-si RDA0064689 RDA0064708
A. westerdijkiae A. ochraceus 46822 2012 Wheat straw Jeollanam-do Damyang-gun RDA0064680 RDA0064699
A. ochraceus 46823 2012 Soybean Gyeonggi-do Yangpyeong-gun RDA0064681 RDA0064700
A. westerdijkiae 46487 2011 Meju Jeollabuk-do Sunchang-gun RDA0064678 RDA0064697
A. westerdijkiae 47139 2013 Soybean Korea unknown RDA0064684 RDA0064703
A. westerdijkiae 47280 2013 Rice straw Jeollanam-do Damyang-gun RDA0064686 RDA0064705
A. westerdijkiae 47394 2014 Air Gyeonggi-do Yongin-si RDA0064690 RDA0064709
Nigri A. japonicus A. japonicus 42845 2007 Soil Gyeonggi-do Suwon-si RDA0064715 RDA0064763
A. japonicus 43791 2008 Creosote contaminated soil Seoul Sangam-dong RDA0064716 RDA0064764
A. aculeatus 47127 2013 Soybean Chungcheongnam-do Gongju-si RDA0065389 RDA0065410
A. japonicus 48322 2017 Unknown Gyeongsangbuk-do Sangju-si RDA0064754 RDA0064798
A. luchuensis A. luchuensis 41731 1995 Nuruk Chungcheongbuk-do Boeun-gun RDA0064713 RDA0064761
A. luchuensis 46420 2011 Traditional yeast Gyeongsangbuk-do Andong-si RDA0064722 RDA0064770
A. luchuensis 46490 2011 Meju Gyeonggi-do Yeoju-si RDA0064724 RDA0064772
A. luchuensis 46491 2011 Meju Jeollabuk-do Sunchang-gun RDA0064725 RDA0064773
A. welwitschiae 46492 2011 Meju Jeollanam-do Haenam-gun RDA0065375 RDA0065396
A. niger 46493 2011 Meju Gyeonggi-do Icheon-si RDA0065376 RDA0065397
A. niger 46494 2011 Meju Gangwon-do Hoengseong-gun RDA0065377 RDA0065398
A. luchuensis 46516 2011 Nuruk Korea unknown RDA0064727 RDA0064775
A. luchuensis 46879 2012 Meju Gyeonggi-do Yongin-si RDA0064729 RDA0064777
A. luchuensis 46958 2012 Nuruk Gyeonggi-do Hwaseong-si RDA0064733 RDA0064781
A. luchuensis 48309 2017 Meju Korea Yangpyeong RDA0064744 RDA0064788
A. luchuensis 48310 2017 Meju Korea Hoengseong RDA0064745 RDA0064789
A. luchuensis 48312 2017 Meju Korea Yongin-si RDA0064746 RDA0064790
A. luchuensis 48313 2017 Meju Korea Yongin-si RDA0064747 RDA0064791
A. luchuensis 48314 2017 Meju Korea Yongin-si RDA0064748 RDA0064792
A. luchuensis 48315 2017 Meju Korea Yongin-si RDA0064749 RDA0064793
A. luchuensis 48316 2017 Meju Korea Yongin-si RDA0064750 RDA0064794
A. luchuensis 48318 2017 Meju Korea Yongin-si RDA0064751 RDA0064795
A. luchuensis 48319 2017 Meju Korea Anseong-gun RDA0064752 RDA0064796
A. luchuensis 48320 2017 Meju Korea Yongin-si RDA0064753 RDA0064797
A. luchuensis 49930 2021 Soy bean paste Jeollabuk-do Wanju-gun RDA0064758 RDA0064802
A. luchuensis 49931 2021 Soy bean paste Jeollabuk-do Wanju-gun RDA0064759 RDA0064803
A. niger A. niger 40279 1997 Unknown Korea unknown RDA0064712 RDA0064760
A. niger 42589 2007 Man Korea Seoul RDA0064714 RDA0064762
A. niger 44333 2009 Sputum Korea Seoul RDA0064719 RDA0064767
A. tubingensis 46498 2011 Meju Gangwon-do Hoengseong-gun RDA0065382 RDA0065403
A. luchuensis 46880 2012 Meju Gyeonggi-do Yangpyeong-gun RDA0065380 RDA0065401
A. luchuensis 48321 2017 Meju Gyeonggi-do Yangpyeong-gun RDA0065381 RDA0065402
A. tubingensis A. niger 40278 1997 Unknown Korea unknown RDA0065393 RDA0065414
A. niger 40280 1997 Unknown Korea unknown RDA0065394 RDA0065415
A. niger 41018 2002 Soil Korea unknown RDA0065392 RDA0065413
A. niger 43547 2008 White pine Korea Daejeon RDA0065395 RDA0065416
A. tubingensis 43792 2008 Ground soil Seoul Sangam-dong RDA0064717 RDA0064765
A. tubingensis 44304 2008 Unknown Chungcheongnam-do Gongju-si RDA0064718 RDA0064766
A. tubingensis 44334 2009 Sputum Korea Seoul RDA0064720 RDA0064768
A. tubingensis 44335 2009 Sputum Korea Seoul RDA0064721 RDA0064769
A. tubingensis 46446 2011 Campbell early Chungcheongbuk-do Yeongdong-gun RDA0064723 RDA0064771
A. tubingensis 46883 2012 Unknown Gyeonggi-do Yeoju-si RDA0064732 RDA0064780
A. tubingensis 47137 2013 Soybean Korea unknown RDA0064734 RDA0064782
A. aculeatus 47267 2013 Rice straw Jeollabuk-do Sunchang-gun RDA0065378 RDA0065399
A. tubingensis 47278 2013 Rice straw Gyeonggi-do Anseong-si RDA0064735 RDA0064783
A. tubingensis 47391 2014 Air Jeollabuk-do Sunchang-gun RDA0064737 RDA0064785
A. luchuensis 48311 2017 Meju Korea Yeoju-si RDA0065391 RDA0065412
A. luchuensis 48317 2017 Meju Jeollabuk-do Sunchang-gun RDA0065379 RDA0065400
A. tubingensis 49868 2021 Plastic debris Jeollanam-do Gwangju-si RDA0064757 RDA0064801
A. uvarum A. uvarum 48630 2018 Decayed tree Seoul Gwanak-gu RDA0064755 RDA0064799
A. welwitschiae A. niger 46495 2011 Meju Gyeonggi-do Gimpo-si RDA0065384 RDA0065405
A. welwitschiae 46496 2011 Meju Chungcheongbuk-do Goesan-gun RDA0064726 RDA0064774
A. niger 46497 2011 Meju Gyeonggi-do Yangpyeong-gun RDA0065383 RDA0065404
A. tubingensis 46499 2011 Meju Jeollabuk-do Sunchang-gun RDA0065385 RDA0065406
A. welwitschiae 46881 2012 Meju Gyeonggi-do Yeoju-si RDA0064730 RDA0064778
A. welwitschiae 46882 2012 Meju Jeollanam-do Haenam-gun RDA0064731 RDA0064779
A. niger 47249 2013 Onion Jeollanam-do Muan-gun RDA0065388 RDA0065409
A. niger 47272 2013 Rice straw Jeollanam-do Haenam-gun RDA0065387 RDA0065408
A. awamori 47376 2014 Air Gyeonggi-do Yongin-si RDA0065386 RDA0065407
A. niger 47383 2014 Air Jeollabuk-do Sunchang-gun RDA0065390 RDA0065411
A. welwitschiae 48728 2019 Groundnut Jeollabuk-do Wanju-gun RDA0064756 RDA0064800
Flavi A. flavus* A. flavus 45443 2010 Meju Chungcheongbuk-do Cheongju-si RDA0064859 RDA0064879
A. nomiae A. nomius 49741 2020 Soil Jeollanam-do Jangseong-gun RDA0064848 RDA0064868
A. oryzae* A. oryzae 46469 2011 Meju Korea unknown RDA0064866 RDA0064886
A. oryzae 46471 2011 Meju Gyeonggi-do Icheon-si RDA0064865 RDA0064885
A. oryzae 46640 2012 Meju Korea unknown RDA0064863 RDA0064883
A. oryzae 46641 2012 Meju Korea unknown RDA0064864 RDA0064884
A. oryzae 46810 2012 Meju Jeollabuk-do Sunchang-gun RDA0064862 RDA0064882
A. oryzae 47133 2013 Soybean Korea unknown RDA0064861 RDA0064881
A. oryzae 47488 2013 Unknown Korea Seoul RDA0064860 RDA0064880
A. oryzae 48141 2016 Air, Indoor Gyeonggi-do Bucheon-si RDA0064867 RDA0064887
A. parasiticus A. parasiticus 46037 2011 Meju environment Gyeongsangbuk-do Andong-si RDA0064856 RDA0064876
A. parasiticus 46475 2011 Meju environment Jeollanam-do Gangjin-gun RDA0064857 RDA0064877
A. parasiticus 46901 2012 Peanut Gyeonggi-do Yeoju-si RDA0064858 RDA0064878
A. tamarii A. parasiticus 46034 2011 Silkworm Gyeonggi-do Suwon-si RDA0064855 RDA0064875
A. tamarii 46476 2011 Meju Jeollabuk-do Jeongeup-si RDA0064849 RDA0064869
A. tamarii 46477 2011 Meju Gyeongsangbuk-do Goryeong-gun RDA0064850 RDA0064870
A. tamarii 46478 2011 Meju Gyeonggi-do Icheon-si RDA0064851 RDA0064871
A. tamarii 46479 2011 Meju Gyeonggi-do Suwon-si RDA0064852 RDA0064872
A. tamarii 46480 2011 Meju Gyeonggi-do Icheon-si RDA0064853 RDA0064873
A. tamarii 47276 2013 Rice straw Gangwon-do Yangyang-gun RDA0064854 RDA0064874
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aThe unrecorded Aspergillus species in Korea are represented in bold.

*Only nine representative strains were taken from section Flavi.

2.2. DNA extraction, PCR amplification, and sequencing

Genomic DNA was extracted from the strains grown on MEA using the DNeasy® Plant Mini kit (Qiagen, Hilden, Germany) following the manufacturer’s instructions. Fragments of the BenA (primers Bt2a and Bt2b) and CaM (primers CMD5 and CMD6) genes were amplified as outlined by Glass and Donaldson [11], and Hong et al. [12]. The PCR products were sequenced bidirectionally at Macrogen Inc., South Korea, using the same primers used for PCR. Consensus sequences were computed from forward and reverse sequences using DNA STAR Lasergene SeqMan Pro version 10.0.1 (DNASTAR, Inc. Madison, WI).

2.3. Phylogenetic analyses

The newly generated sequences were supplemented with reference (preferably ex-type) sequences retrieved from previously published studies [5]. Alignment of the sequences was performed using the CLUSTAL W program [13] and were manually edited with MEGA version 7.0 (University Park, PA) [14]. The maximum likelihood (ML) method was used for the phylogenetic analysis. For ML analysis, the data were first analyzed using the nucleotide substitution model and the best substitution pattern was then used to construct the ML tree with MEGA version 7.0 [14]. To determine the support for each clade, a bootstrap analysis was performed with 1000 replications. The sequence of Aspergillus calidoustus CBS 121601T was used as an outgroup. The reference sequences used in this analysis have been listed in Table 2. Sequences generated in this study were deposited to KACC-GeneBank (http://genebank.rda.go.kr).

Table 2.

Reference sequences of Aspergillus species used in the phylogenetic analyses.

Section Species Strain no. Country GenBank Accession no.
CaM BenA
Candidi A. campestris NRRL 13001 T USA EF669535 EU014091
A. candidus NRRL 303 T Unknown EF669550 EU014089
A. dobrogensis CCF 4651 T Romania LT558722 LT627027
A. magnus UAMH 1324 T Canada ON164619 ON164570
A. neotritici CCF 3853 T Czech Republic HE661598 FR775327
A. pragensis CCF 3962 T Czech Republic FR751452 HE661604
A. subalbidus NRRL 312 T Brazil EF669551 MN969366
A. taichungensis DTO 031-C6 T Taiwan EU076310 MN969367
A. tenebricus DTO 337-H7 T South Africa ON164623 ON164584
Terrei A. allahabadii NRRL 4539 T India EF669559 EF669531
A. floccosus CBS 116.37 T China KP987066 FJ491714
A. terreus NRRL 255 T USA EF669544 EF669519
Flavipedes A. flavipes NRRL 302 T Unknown EF669549 EU014085
A. iizukae NRRL 3750 T Japan EF669555 EU014086
Circumdati A. elegans NRRL 4850 T USA EF661390 EF661349
A. ochraceus NRRL 398 T Unknown EF661381 EF661322
A. ostianus NRRL 420 T Unknown EF661385 EF661324
A. sclerotiorum NRRL 415 T USA EF661384 EF661337
A. steynii NRRL 35675 T India EF661378 EF661347
A. westerdijkiae NRRL 3174 T South Africa EF661360 EF661329
Nigri A. aculeatus
A. japonicus 		NRRL 5094 T
CBS 114.51 T 		Unknown
Unknown		 EF661148
FN594551 		HE577806
HE577804
JX500062
A. luchuensis KACC 46772 T Japan JX500071
A. niger NRRL 326 T USA EF661154 EF661089
A. tubingensis NRRL 4875 T Unknown EF661151 EF661086
A. uvarum ITEM 4834 T Italy AM745755 AM745751
A. welwitschiae CBS 139.54 T Namibia KC480196 MN969369
Flavi A. flavus NRRL 1957 T South Pacific Islands EF661508 EF661485
A. nomiae NRRL 13137 T USA AY017588 AF255067
A. oryzae NRRL 447 T Unknown EF661506 EF661483
A. parasiticus NRRL 502 T USA AY017584 EF661481
A. tamarii NRRL 20818 T Unknown EF661526 EF661474
Outgroup A. calidoustus CBS 121601 T Netherlands HE616559 FJ624456
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CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands; CCF: Culture Collection of Fungi at the Department of Botany of Charles University in Prague; ITEM: Microbial Culture Collection, Institute of Sciences of Food Production, Bari, Italy; KACC: Korean Agricultural Culture Collection, Wanju, Republic of Korea; NRRL: ARS culture collection, Peoria, IL, USA; T: ex-type strain.

2.4. Phenotypic analysis

The strains were three-point inoculated on Czapek Yeast extract agar (CYA), Dichloran 18% Glycerol agar (DG18), MEA, and yeast extract sucrose agar (YES) [15]. Media preparation, inoculation, and incubation were performed as described by Samson et al. [2] and all Petri dishes were incubated at 25 °C for 7 d. After 7 d of incubation, colony diameters were measured and colony characteristics were recorded (presence of soluble pigments, exudates, obverse and reverse colony colors, color of conidia). Microscopic examination was performed on colonies grown on MEA using Zeiss Axio imager A1 light microscope equipped with Axio cam ICc3 camera (ZEISS, Seoul, South Korea). Slides were prepared with lactic acid, which was used as the mounting fluid, and ethanol was, at times used to remove excess conidia. The size, shape, and pigmentation of conidia and conidiophores were recorded.

3. Results and discussion

3.1. Phylogenetic analyses

In this study, phylogenetic position of strains belonging to subgenus Circumdati was studied using concatenated data on BenA and CaM sequences (Figure 1). In the section Flavi, most of the strains belonging to A. flavus and A. oryzae exhibited highly similar BenA and CaM gene sequences. Therefore, we selected a few representative strains (9 out of 133) of A. flavus and A. oryzae for further phylogenetic analysis. Information about these strains is given in Table 1. In total, the concatenated alignment included 144 sequences: 111 derived from strains of the KACC and the others from publicly available (ex-) type species. The total length of the aligned data set was 1187 characters. The most optimal substitution model was K2 + G + I for the BenA and CaM data set.

Figure 1.

Phylogenetic position of Aspergillus subgenus Circumdati strains from the KACC based on a combined data set of partial BenA and CaM sequences. Bootstrap values >50 are presented at the nodes. The unrecorded species are represented in bold and red in color. Ex-type strains are denoted by the symbol “T.” A. calidoustus was used as the outgroup.

graphic file with name TMYB_A_2257997_F0001a_C.jpg

graphic file with name TMYB_A_2257997_F0001b_C.jpg

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During our studies, the 235 strains taken were spread across 22 different Aspergillus species, of which 19 species have been previously reported from Korea. Three species constituted by six strains (highlighted in red bold text) were not previously described from Korea (Figure 1).

In the section Flavi, 40 species have been reported worldwide [5,16–18]. Among them, A. flavus, A. nomiae, A. parasiticus, A. tamarii, and A.oryzae have been recorded in Korea [9,19]. One hundred and forty-four strains from this study, belonging to – the section Flavi in Korea clustered with type strains of A. flavus, A. oryzae, A. nomiae, A. parasiticus, and A. tamarii and identified according to their closest type strain. In this section, A. flavus/oryzae complex contributed to a huge number of strains (n = 133). Since their BenA and CaM gene sequences were highly similar, only a few (n = 9) representative strains were selected and shown in Figure 1. Aflatoxin production was used to differentiate the strains between A. flavus and A. oryzae (data not shown), as the two species cannot be differentiated based on their BenA and CaM gene sequences.

In the section Flavipedes, all 3 strains used in this study were clustered with A. iizukae. Nineteen (19) species have been reported in the section Flavipedes [5,20,21]. In Korea, 4 species namely A. capensis, A. flavipes, A. polyporicola, and A. spelaeus have been recorded already [9]. We are adding a new record of A. iizukae in this section which was not previously reported in Korea.

Among 20 known species form the section Terrei [5,6,21], four of them, viz., A. alabamensis, A. allahabadii, A. floccosus, and A. terreus have been recorded in Korea [9]. Five strains of the section Terrei in Korea clustered along with type strains of A. allahabadii, A. floccosus, A. terreus and are therefore identified as A. allahabadii, A. floccosus, A. terreus respectively.

In the section Candidi of subgenus Circumdati, 5 strains were found to be clustered into two groups with A. neotritici and A. subalbidus. Nine species have been recorded in this section [5,22]. Recently, A. tritici was synonymized as A. neotritici [22]. In Candidi, A. candidus, A. pragensis and A. neotritici have been recorded in Korea [9]. A. subalbidus has not yet been recorded in Korea, which is included in the current report.

In the section Circumdati, 17 strains were found to cluster into five groups, comprising of A. ochraceus, A. ostianus, A. sclerotiorum, A. steynii, and A. westerdijkiae as nearest type strains. Thirty species have been recorded in the section [5,23,24], of which, A. ochraceus, A. ostianus, A. insulicola, A. sclerotiorum, A. steynii, and A. westerdijkiae are recorded in Korea [9].

In the section Nigri of subgenus Circumdati, 61 strains grouped into six clusters, with A. japonicus, A. luchuensis, A. niger, A. tubingensis, A. uvarum, and A. welwitschiae as their nearest neighbors. Until now, 32 species have been recorded in this section [5,24,25]. Among them, A. aculeatus, A. brunneoviolaceus, A. costaricaensis, A. floridensis, A. japonicus, A. niger, A. tubingensis, A. luchuensis, and A. welwitschiae are recorded in Korea [9,26]. A. uvarum have not been recorded in Korea, and we are reporting new record of A. uvarum in Korea in this article.

In the past decade, the classification of Aspergillus species has been developed to be based on a combination of molecular data, physiology, morphology, and/or extrolite data [12,27–29]. This approach was used by Houbraken et al. [5] to clarify the taxonomic position of Aspergillus, Pencillium, Talaromyces, and related genera. In this study, the strains used were documented and preserved at KACC well before the overview paper of Houbraken et al. [5] and the identification of these strains would have been most likely based on the morphological characters such as growth rate, color of the colony, thermotolerance, and size of conidial heads and conidia. However, currently, morphological features alone are understood to be inadequate to identify species because of morphological characteristics have been found to vary even with respect to change in their ecological habitats [30,31]. In our study, six strains were found to be clustered with unrecorded species of Korea. Till date, there have been few reports on undescribed Aspergillus species in Korea despite the genus having a cosmopolitan distribution. On the other hand, there has been a rise of several new Aspergillus species worldwide [10].

Among the three hitherto unrecorded species from Korea, the strains KACC 43789, KACC 48444, and KACC 48864 were phylogenetically close to the type strain A. iizukae NRRL255T belonging to the section Flavipedes (Figure 1). Morphological characters of the strains were also consistent with those of A. iizukae described by Hubka et al. [32]. The species was first described by Sugiyama in 1967 [33]. Aspergillus section Flavipedes endured a reexamination study of species limits using advanced species delimitation methods, and the revised section harbors 19 species with most of the species being reported from soil. Though the most common species from the section are ecologically diverse, occurring in the indoor environment, clinical samples, food and feed, droppings and other less common substrates/environments [20], in this study, the isolates were found to have mainly originated from soil and food. A. iizukae have been reported to produce diphenyl derivatives, namely iizukines A (1) and B (2); flavonolignans, namely Silybin A (1), silybin B (2), isosilybin A (3); oxidative enzymes, such as laccase, manganese peroxidase, and lignin peroxidase [34–36].

Based on their phylogeny, KACC 46481 and KACC 46482 were clustered with A. subalbidus NRRL 312T (ex-type strain), in section Candidi (Figure 1). Strains KACC 46481 and KACC 46482 were morphologically similar to A. subalbidus, as described by Visagie et al. [15]. Phylogenetically, A. subalbidus forms a separate clade, closely related to A. tenebricus, A. taichungensis, and A. neotritici (Figure 1). Recently, Aspergillus section Candidi underwent a monographic study, with the revised section Candidi hosting nine species. Members in this section have been reported from house dust, soil, herbivore dung, indoor air, and cave environments, and occasionally from clinical specimens [22]. To our best knowledge, this is first study to isolate A. subalbidus from meju, thereby revealing its significance as a fungus colonizing food environment.

As shown in Figure 1, strain KACC 48630 aligned with A. uvarum ITEM 4834 (ex-type strain) in section Nigri. Morphologically, the isolated strain represents similar characters with type strain ITEM 4834 of A. uvarum described by Perrone et al. [37]. These include sporulation with dark brown conidia; uniseriate conidiophores; globose to elliptical vesicle, 20–30 µm; and conidia globose to subglobose, spinose, 3–4 µm. Moreover, section Nigri, known as black aspergilli includes species with smooth conidiophores and hyaline or pigmentation below the vesicle; globose, subglobose, and pyriform vesicles; typically radiating conidial heads; or divergent columns in certain species [38]. These aspergilli have been isolated from soil samples, air environments, contaminated materials and plants [24,25,39]. In general, 30 species have been accepted in this section [5]. Two additional new species, A. oxumiae and A. hydei, were reported in soil cultivated with Agave sisalana, and from air under the tree Quercus variabilis [24,25]. The species A. uvarum is a rare member of the group of black aspergilli, which has a high significance in the industry due to its ability to produce secalonic acid, commonly produced by black aspergilli; and geodin, erdin, and dihydrogeodin, which are not produced by any other black aspergilli [37]. Based on macro- and micro-morphological characters and phylogenetic concordance between BenA & CaM gene phylogenies, we present here three undescribed species of Korea named A. iizukae, A. subalbidus, and A. uvarum.

3.2. Taxonomy

Aspergillus iizukae Sugiyama, J. Fac. Sci. Univ. Tokyo, Section 3: 390 (1967) [MB#326636] [33]

Colony characteristics: Colonies on CYA at 25 °C attain 21–22 mm diameter in 7 d, velutinous dull white with granular surface, no soluble pigment, reverse light brown. On MEA, the colonies were velutinous to floccose with granular surface, irregularly or radially wrinkled, light yellowish-brown sporulation, no soluble pigment, reverse strong yellowish brown and attains 20–21 mm diameter in 7 d. Colonies on YES attain 23–24 mm diameter after 7 d at 25 °C; light yellowish sporulation at center with white mycelium at margins, reverse pale yellow. On DG18, colonies were slow growth, clear white mycelium, reverse white, and reached 8–9 mm in diameter after 7 d at 25 °C.

Micromorphology: Conidial heads biseriate, stipes hyaline, smooth-walled, long <1000 um. Vesicles pyriform, 14–20 µm. Metulae covering one half to entire surface of the vesicle, 3–6 × 2–3 μm. Phialides 5–7 × 2–3.5 μm. Conidia globose, smooth, connectives sometimes remain on free conidia 2–3 μm (Figure 2).

Figure 2.

Figure 2.

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Morphology of Aspergillus iizukae (KACC 43789). (A–D) Colonies grown on MEA, CYA, DG18, and YES media after 7 d at 25 °C from left to right. (E) Conidial heads on MEA. (F & G) Conidiophores with conidial head. (H) Conidia. Scale bars: E = 100 µm, F = 20 µm, G, H = 10 µm.

Strains examined: KACC 43789, KACC 48864, and KACC 48444

Remarks: A. iizukae is closely related to A. capensis. Recent species delimitation study proposed that A. capensis is synonymized with A. iizukae [20].

Aspergillus subalbidus Visagie, Hirooka & Samson, Studies in Mycology 78: 101 (2014) [MB#809190] [15].

Colony characteristics: On CYA, Colony mycelium and sporulation were found to be white, no soluble pigment present and reverse turned into light brown and eventually reached 17–19 mm in diameter after 7 d at 25 °C. On MEA, the colony surface was floccose, white mycelial areas and sporulation, soluble pigment absent and turned reverse yellow-orange, and further reached 16–22 mm in diameter after 7 d at 25 °C. On DG18, colony mycelium and sporulation were white in color and reverse white with 16–19 mm in diameter after 7 d at 25 °C. Colonies on YES were floccose after 7 d at 25 °C; conidia white, reverse centrally yellowish orange, fading into light yellow toward margin.

Micromorphology: Conidial heads biseriate, sometimes reduced Penicillium-like structures present, stipes hyaline, smooth-walled, 100–300 × 4–7 µm. Vesicles globose to subglobose, 6–13 µm. covering 100% of the head; Metulae 4–6 × 2–6 μm; Phialides ampulliform, 6–9 × 2.5–3.5 μm; Conidia globose to subglobose, smooth, 3–4 μm (Figure 3).

Figure 3.

Figure 3.

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Morphology of Aspergillus subalbidus (KACC 46482). (A–D) Colonies grown on MEA, CYA, DG18, and YES media after 7 d at 25 °C from left to right. (E) Conidial head on MEA. (F & G) Conidiophores with conidial head. (H) Conidia. Scale bars: E = 100 µm, F, G = 20 µm, H = 10 µm.

Strains examined: KACC 46481 and KACC 46482

Remarks: A. subalbidus is morphologically almost identical to A. candidus [15]. Phylogenetically, it forms a separate clade closely related to A. tenebricus, A. taichungensis, and A. neotritici (Figure 1).

Aspergillus uvarum G. Perrone, Varga & Kozak., International Journal of Systematic and Evolutionary Microbiology 58: 1036 (2008) [MB#510962] [37]

Colony characteristics: On CYA, colonies initially appeared white with flat mycelia and then turned brown–black, followed by reverse white, wrinkled, becoming dull yellow with black colony centers by age, and eventually reached 60–62 mm in diameter after 7 d at 25 °C. On MEA, colonies were dark brown-black, with sporulation, widespread, and turned reverse yellow-orange, and further reached 61–63 mm in diameter after 7 d at 25 °C. Colonies on YES were overgrown (90 mm plates) after 7 d at 25 °C; conidia brown–black, Abundant conidiogenesis, mycelium inconspicuous; reverse light yellow and wrinkled. On DG18, colonies were dark brown with clear white mycelium at margins, reverse white and reached 43–44 mm in diameter after 7 d at 25 °C.

Micromorphology: Conidial heads uniseriate, smooth-walled, 500–1000 × 5–10 µm. Vesicles globose to elliptical, 50–60 µm. Fertile over the entire surface. Phialides 5–7 × 4–5 µm. Conidia brown-black, globose to sub-globose, 4–5 µm, conspicuously spinose at maturity with spines projecting on the surface with 0.59 µm (Figure 4).

Figure 4.

Figure 4.

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Morphology of Aspergillus uvarum (KACC 48630). (A–D) Colonies grown on MEA, CYA, DG18, and YES media after 7 d at 25 °C from left to right. (E) Conidial head on MEA. (F & G) Conidiophores with conidial head. (H) Conidia. Scale bars: E = 100 µm, F= 50 µm, G = 20 µm, H = 5 µm.

Strain examined: KACC 48630

Remarks: A. uvarum is closely related to A. japonicus and A. aculeatus both morphologically and at a molecular level. Both species have echinulate conidial surface, uniseriate like A. uvarum [40]. However, A. japonicus has larger vesicle and similar conidial size to A. uvarum whereas A. aculeatus has a larger vesicle and ellipsoidal conidial shape [37]. KACC 48630 was well differentiated from type strains of A. japonicus and A. aculeatus. The strain KACC 48630 was deposited as A. uvarum in the year 2018. This species was later listed as an unrecorded species within Korea with strain CNUFC YB6 [41], albeit the publication was not effective due to lacking mycological specifics. Therefore, the authors here describe the species officially as unrecorded and publish the species effectively. This paper, therefore, is designed to serve as the official record of A. uvarum in Korea.

Microbial resource centers employ several methods to ensure purity of documented strains as any lapses in storage can negate research progress on particular strains [42]. KACC employs a minimum of two different preservation conditions and some of the strains used in this study have been in storage for more than 25 years. All strains in this study successfully revived and showed morphology that is typical of Aspergillus. Our study focused on re-identification and describing unrecorded species of Aspergillus from various environments, resolving taxonomic problems, and providing high quality organisms to conserve at KACC. The modern culture collection also has the goal to give access to high quality biological materials with associated information. The data presented in this study reinforces the importance of fungal collections and reassess their strain identification using current techniques.

Funding Statement

This study was financially supported by Ministry of Science and ICT [Grant number M3H9A1081254].

Disclosure statement

No potential conflict of interest was reported by the author(s).

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