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Complete mitochondrial genome sequence of a xerophilic fungus, Aspergillus pseudoglaucus

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Abstract

Aspergillus pseudoglaucus is a xerophilic filamentous fungus which can produce various secondary metabolites. Here, we reported the complete mitochondrial genome sequence of A. pseudoglaucus isolated from Meju, a soybean brick in Korea. Its mitochondrial genome was successfully assembled from raw reads sequenced using MiSeq by Velvet and SOAPGapCloser. Total length of the mitochondrial genome is 53,882 bp, which is third longest among known Aspergillus mitochondrial genomes and encoded 58 genes (30 protein-coding genes including hypothetical ORFs, two rRNAs, and 26 tRNAs). Nucleotide sequence of coding regions takes over 66.6% and overall GC content is 27.8%. Phylogenetic trees present that A. pseudoglaucus is located outside of section Nidulantes. Additional researches will be required for clarifying phylogenetic position of section Aspergillus.
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Complete mitochondrial genome sequence of a
xerophilic fungus, Aspergillus pseudoglaucus
Jongsun Park, Woochan Kwon, Xiaoxiao Huang, Anbazhagan Mageswari, In-
Beom Heo, Kap-Hoon Han & Seung-Beom Hong
To cite this article: Jongsun Park, Woochan Kwon, Xiaoxiao Huang, Anbazhagan Mageswari, In-
Beom Heo, Kap-Hoon Han & Seung-Beom Hong (2019) Complete mitochondrial genome sequence
of a xerophilic fungus, Aspergillus�pseudoglaucus, Mitochondrial DNA Part B, 4:2, 2422-2423, DOI:
10.1080/23802359.2019.1586468
To link to this article: https://doi.org/10.1080/23802359.2019.1586468
© 2019 The Author(s). Published by Informa
UK Limited, trading as Taylor & Francis
Group.
Published online: 12 Jul 2019.
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MITOGENOME ANNOUNCEMENT
Complete mitochondrial genome sequence of a xerophilic fungus, Aspergillus
pseudoglaucus
Jongsun Park
a,b
, Woochan Kwon
a,b
, Xiaoxiao Huang
c
, Anbazhagan Mageswari
d,e
, In-Beom Heo
d
,
Kap-Hoon Han
c
and Seung-Beom Hong
e
a
InfoBoss Co., Ltd., Seoul, Republic of Korea;
b
InfoBoss Research Center, Seoul, Republic of Korea;
c
Department of Pharmaceutical
Engineering, Woosuk University, Wanju, Republic of Korea;
d
Department of Microbiology, D.G. Vaishnav College, Chennai, India;
e
Agricultural
Microbial Division, National Institute of Agricultural Scinece, Wanjugun, Republic of Korea
ABSTRACT
Aspergillus pseudoglaucus is a xerophilic filamentous fungus which can produce various secondary
metabolites. Here, we reported the complete mitochondrial genome sequence of A. pseudoglaucus iso-
lated from Meju, a soybean brick in Korea. Its mitochondrial genome was successfully assembled from
raw reads sequenced using MiSeq by Velvet and SOAPGapCloser. Total length of the mitochondrial
genome is 53,882bp, which is third longest among known Aspergillus mitochondrial genomes and
encoded 58 genes (30 protein-coding genes including hypothetical ORFs, two rRNAs, and 26 tRNAs).
Nucleotide sequence of coding regions takes over 66.6% and overall GC content is 27.8%. Phylogenetic
trees present that A. pseudoglaucus is located outside of section Nidulantes. Additional researches will
be required for clarifying phylogenetic position of section Aspergillus.
ARTICLE HISTORY
Received 23 December 2018
Accepted 10 February 2019
KEYWORDS
Aspergillus pseudoglaucus;
mitochondrial genome;
a xerophilic fungus;
Ascomycota
Aspergillus pseudoglaucus (Chen et al. 2017), identified in
1929, is a xerophilic filamentous fungus belonging to
Aspergillus section Aspergillus. It has been isolated from sea-
foods and soil (Smetanina et al. 2007;S
eguin et al. 2014). It
has also been used as a start culture for Kastuobushi in
Japan (Pitt and Hocking 2009) and frequently identified
from Meju, a soybean brick used for making soy source and
soybean paste in Korea (Hong et al. 2011). It can produce
various metabolites such as benzyl derivatives binding to
human opioid or cannabinoid receptors (Gao et al. 2011),
mycophenolic acid (Mouhamadou et al. 2017), and various
antibacterial and antifungal compounds (Gao et al. 2012). To
understand phylogenetic relationship of A. pseudoglaucus,we
presented its complete mitochondrial genome.
DNA of A. pseudoglaucus collected from Meju in Korea was
extracted using DNeasy Plant Mini Kit (QIAGEN, Hilden,
Germany). Raw data generated using MiSeq, and de novo
assembly was conducted using Velvet 1.2.10 (Zerbino and
Birney 2008). Gap filling was carried out using SOAPGapCloser
1.12 (Zhao et al. 2011) after confirming each base using BWA
0.7.17 and SAMtools 1.9 (Li et al. 2009;Li2013). Geneious R11
11.0.5 (Biomatters Ltd, Auckland, New Zealand) was used to
annotate its mitochondrial genome by comparing with those of
Aspergillus luchuensis (MK061298; Park, Kwon, Zhu, Mageswari,
Heo, Han, Hong, under review)andAspergillus parasiticus
(MK124769; Park et al. under review). Voucher sample was
deposited into Korean Agricultural Culture Collection (KACC;
Republic of Korea; http://genebank.rda.go.kr/; KACC-93211).
The length of A. pseudoglaucus mitochondrial genome
(Genbank accession is MK202802) is 53,882 bp, which is
third longest among twelve Aspergillus mitochondrial
genomes (Futagami et al. 2011; Joardar et al. 2012;Xuetal.
2018;Park,Kwon,Zhu,Mageswari,Heo,Han,Hong,under
review;Parketal.under review): The longest is Aspergillus cris-
tatus (77,649 bp; Ge et al. 2016) and second longest is
Aspergillus egyptiacus (66,526 bp; Xu et al. 2018). Aspergillus
pseudoglaucus CO1 gene contains eight introns, which is pro-
portion to the length of whole mitochondrial genomes (Joardar
et al. 2012). In addition, other main protein-coding genes
except ND5 have at least one intron, indicating a reason of
expansion of A. pseudoglaucus mitochondrial genome (Joardar
et al. 2012). Moreover, 16 of 20 introns contain partial ORFs,
mostly endonuclease. Its mitochondrial genome encoded 58
genes consisting of 30 protein-coding genes including hypo-
thetical ORFs, two rRNAs, and 26 tRNAs. Protein-coding regions
takes over 66.6% on genome, and overall GC content is 27.8%,
whicharesimilartothoseofAspergillus genus.
Sequence alignment of nine Aspergillus except A. cristatus, A.
egyptiacus,andA. flavus and one Penicillium mitochondrial gen-
ome as an outgroup was conducted using MAFFT 7.388 (Katoh
and Standley 2013). The neighbor joining (10,000 bootstrap
repeats) and maximum likelihood (1,000 bootstrap repeats)
methods were used for constructing phylogenetic tree using
MEGA X (Kumar et al. 2018). Phylogenetic trees showed that A.
pseudoglaucus is located outside of section Nidulantes and does
not form any clades with other species; however, bootstrap
CONTACT Seung-Beom Hong funguy@korea.kr Agricultural Microbial Division, National Institute of Agricultural Scinece, Wanjugun 55365, Republic of
Korea; Kap-Hoon Han khhan@woosuk.ac.kr Department of Pharmaceutical Engineering, Woosuk University, Wanju 55338, Republic of Korea
ß2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
MITOCHONDRIAL DNA PART B
2019, VOL. 4, NO. 2, 24222423
https://doi.org/10.1080/23802359.2019.1586468
supports are not enough (Figure 1). Additional researches will
be required for clarifying phylogenetic position of section
Aspergillus.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This study was carried out with the support of project no. PJ01354902 of
the National Institute of Agricultural Science, Rural Development
Administration, Republic of Korea to SBH and supported by the National
Research Foundation of Korea (NRF) grant funded by the Korea govern-
ment [NRF-2017R1D1A3B06035312].
ORCID
Jongsun Park http://orcid.org/0000-0003-0786-4701
Woochan Kwon http://orcid.org/0000-0001-8665-8097
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(NC_008282), Aspergillus fumigatus (NC_017016), and Penicillium chrysogenum (JMSF01000018). The numbers above branches indicate bootstrap support values of
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Aspergillus section Aspergillus (formerly the genus Eurotium) includes xerophilic species with uniseriate conidiophores, globose to subglobose vesicles, green conidia and yellow, thin walled eurotium-like ascomata with hyaline, lenticular ascospores. In the present study, a polyphasic approach using morphological characters, extrolites, physiological characters and phylogeny was applied to investigate the taxonomy of this section. Over 500 strains from various culture collections and new isolates obtained from indoor environments and a wide range of substrates all over the world were identified using calmodulin gene sequencing. Of these, 163 isolates were subjected to molecular phylogenetic analyses using sequences of ITS rDNA, partial β-tubulin (BenA), calmodulin (CaM) and RNA polymerase II second largest subunit (RPB2) genes. Colony characteristics were documented on eight cultivation media, growth parameters at three incubation temperatures were recorded and micromorphology was examined using light microscopy as well as scanning electron microscopy to illustrate and characterise each species. Many specific extrolites were extracted and identified from cultures, including echinulins, epiheveadrides, auroglaucins and anthraquinone bisanthrons, and to be consistent in strains of nearly all species. Other extrolites are species-specific, and thus valuable for identification. Several extrolites show antioxidant effects, which may be nutritionally beneficial in food and beverages. Important mycotoxins in the strict sense, such as sterigmatocystin, aflatoxins, ochratoxins, citrinin were not detected despite previous reports on their production in this section. Adopting a polyphasic approach, 31 species are recognised, including nine new species. ITS is highly conserved in this section and does not distinguish species. All species can be differentiated using CaM or RPB2 sequences. For BenA, Aspergillus brunneus and A. niveoglaucus share identical sequences. Ascospores and conidia morphologyw, growth rates at different temperatures are most useful characters for phenotypic species identification.
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Background: Aspergillus cristatus is the dominant fungus involved in the fermentation of Chinese Fuzhuan brick tea. Aspergillus cristatus is a homothallic fungus that undergoes a sexual stage without asexual conidiation when cultured in hypotonic medium. The asexual stage is induced by a high salt concentration, which completely inhibits sexual development. The taxon is therefore appropriate for investigating the mechanisms of asexual and sexual reproduction in fungi. In this study, de novo genome sequencing and analysis of transcriptomes during culture under high- and low-osmolarity conditions were performed. These analyses facilitated investigation of the evolution of mating-type genes, which determine the mode of sexual reproduction, in A. cristatus, the response of the high-osmolarity glycerol (HOG) pathway to osmotic stimulation, and the detection of mycotoxins and evaluation of the relationship with the location of the encoding genes. Results: The A. cristatus genome comprised 27.9 Mb and included 68 scaffolds, from which 10,136 protein-coding gene models were predicted. A phylogenetic analysis suggested a considerable phylogenetic distance between A. cristatus and A. nidulans. Comparison of the mating-type gene loci among Aspergillus species indicated that the mode in A. cristatus differs from those in other Aspergillus species. The components of the HOG pathway were conserved in the genome of A. cristatus. Differential gene expression analysis in A. cristatus using RNA-Seq demonstrated that the expression of most genes in the HOG pathway was unaffected by osmotic pressure. No gene clusters associated with the production of carcinogens were detected. Conclusions: A model of the mating-type locus in A. cristatus is reported for the first time. Aspergillus cristatus has evolved various mechanisms to cope with high osmotic stress. As a fungus associated with Fuzhuan tea, it is considered to be safe under low- and high-osmolarity conditions.
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Introduction. The Ecology of Fungal Food Spoilage. Naming and Classifying Fungi. Methods for Isolation, Enumeration and Identification. Primary Keys and Miscellaneous Fungi. Zygomycetes. Penicillium and Related Genera. Aspergillus and Relataed Teleomorphs. Xerophiles. Yeast. Spoilage of Fresh and Perishable Foods. Spoilage of Stored, Processed and Preserved Foods. Media Appendix. Glossary. Index
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Mycophenolic acid (MPA) is the fungal secondary metabolite displaying a wide range of biological properties including immunosuppressive activities. Up to now, screening of fungal strains producing MPA has mainly been the result of the search of this molecule in their culture medium by chemical methods. Here we developed a molecular approach for the characterization of MPA-producing species by targeting the expression level of the MpaC gene encoding the polyketide synthase, one of the key enzymes involved in the MPA synthesis. Thirty xerophilic Aspergillus strains were identified by molecular methods using the RNA polymerase II subunit and the β-tubulin genes. Seven Aspergillus species were evidenced. The expression level of the MpaC gene was quantified and compared to the MPA production rate. Only A. pseudoglaucus and all the eight strains of this species produced MPA. While the MpaC gene was not expressed or weakly expressed in the MPA non-producing strains, all the A. pseudoglaucus strains presented a high level of expression of this gene. The highest expression level of the MpaC gene among the MPA non-producing strains was significantly lower than the lowest expression level of this gene in the MPA producing strains. To our knowledge, this is the first study that demonstrates the effectiveness of molecular approach for the screening of MPA-producing species and shows that the production of MPA is species dependent in the genus Aspergillus.
Book
The first and second editions of Fungi and Food Spoilage established a reputation as the foremost book on foodborne fungi. This completely revised and updated third edition is an invaluable reference for food microbiologists investigating fungal spoilage and sources of mycotoxin contamination in foods. The introductory chapters of the book deal with the ecology of food spoilage and give an overview of how food processing, packaging and storage affect fungal growth. Subsequent chapters cover the fundamentals of classifying and naming fungi and current methods for isolation and enumeration, including general and special purpose media, incubation conditions, etc. The major part of the book provides keys, descriptions and illustrations of all yeasts and moulds commonly encountered in foods. Characteristics of the species, including their ecology and potential for mycotoxin production, are also included. The broad and practical nature of the coverage will appeal to microbiologists, mycologists and biotechnologists in the food industry, academic, research and public health institutions. Dr John Pitt and Dr Ailsa Hocking are both Honorary Research Fellows at CSIRO Food Science Australia, North Ryde, NSW, Australia. © Springer Science+Business Media, LLC 2009. All rights reserved.
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Mycophenolic acid is considered as an immunosuppressive pharmaceutical drug, but also as a mycotoxin due to its undesirable presence in various feedstuffs. Although Penicillium brevicompactum has been historically identified as the major producer of mycophenolic acid, this study reports for the first time the production of mycophenolic acid by isolates of Eurotium repens collected from agricultural and indoor environments. Fungal identification was achieved by scanning electron microscopy and molecular techniques, and mycophenolic acid production was confirmed by two analytical methods (gas and liquid chromatography coupled to mass spectrometry). These findings suggest that mycophenolic acid production and immunosuppressive properties of other closely related Eurotium should be evaluated in future studies.