Mycobiology

The Korean Society of Mycology (한국균학회)
권호 표지
DOI QR코드

DOI QR Code

Are Current Aspergillus sojae Strains Originated from a Native Aflatoxigenic Aspergillus Species Population Also Present in California?

  • Perng-Kuang Chang (Southern Regional Research Center, Agricultural Research Service, U.S. Department of Agriculture) ;
  • Sui Sheng T. Hua (Western Regional Research Center, Agricultural Research Service, U.S. Department of Agriculture)
  • 투고 : 2023.03.28
  • 심사 : 2023.05.19
  • 발행 : 2023.06.30
Download PDF
⟨ Previous Next ⟩

초록

Aspergillus sojae has long been considered a domesticated strain of Aspergillus parasiticus. This study delineated relationships among the two species and an Aspergillus PWE36 isolate. Of 25 examined clustered aflatoxin genes of PWE36, 20 gene sequences were identical to those of A. sojae, but all had variations to those of A. parasiticus. Additionally, PWE36 developmental genes of conidiation and sclerotial formation, overall, shared higher degrees of nucleotide sequence identity with A. sojae genes than with A. parasiticus genes. Examination of defective cyclopiazonic acid gene clusters revealed that the PWE36 deletion pattern was identical only to those of A. sojae. Using A. sojae SMF134 genome sequence as a reference, visualization of locally collinear blocks indicated that PWE36 shared higher genome sequence homologies with A. sojae than with A. parasiticus. Phylogenetic inference based on genome-wide single nucleotide polymorphisms (SNPs) and total SNP counts showed that A. sojae strains formed a monophyletic clade and were clonal. Two (Argentinian and Ugandan) A. parasiticus isolates but not including an Ethiopian isolate formed a monophyletic clade, which showed that A. parasiticus population is genetically diverse and distant to A. sojae. PWE36 and A. sojae shared a most recent common ancestor (MRCA). The estimated divergence time for PWE36 and A. sojae was about 0.4 mya. Unlike Aspergillus oryzae, another koji mold that includes genetically diverse populations, the findings that current A. sojae strains formed a monophyletic group and shared the MRCA with PWE36 allow A. sojae to be continuously treated as a species for food safety reasons.

키워드

참고문헌

  1. Ito K, Matsuyama A. Koji molds for Japanese soy sauce brewing: characteristics and key enzymes. J Fungi. 2021;7(8):658.
  2. Frisvad JC, Hubka V, Ezekiel CN, et al. Taxonomy of Aspergillus section flavi and their production of aflatoxins, ochratoxins and other mycotoxins. Stud Mycol. 2019;93:1-63.
  3. Kim KM, Lim J, Lee JJ, et al. Characterization of Aspergillus sojae isolated from Meju, Korean traditional fermented soybean brick. J Microbiol Biotechnol. 2017;27(2):251-261. https://doi.org/10.4014/jmb.1610.10013
  4. Klich MA. Identification of common Aspergillus species. Utrecht: Centraalbureau voor Schimmelcultures, 2002.
  5. Kurtzman CP, Smiley MJ, Robnett CJ, et al. DNA relatedness among wild and domesticated species in the Aspergillus flavus group. Mycologia. 1986;78(6):955-959. https://doi.org/10.1080/00275514.1986.12025355
  6. Hua SST, Parfitt DE, Sarreal SBL, et al. First report of an atypical new Aspergillus parasiticus isolates with nucleotide insertion in aflR gene resembling to A. sojae. Mycotoxin Res. 2018;34(2):151-157. https://doi.org/10.1007/s12550-018-0309-2
  7. Takahashi T, Chang P-K, Matsushima K, et al. Nonfunctionality of Aspergillus sojae aflR in a strain of Aspergillus parasiticus with a disrupted aflR gene. Appl Environ Microbiol. 2002;68(8):3737-3743. https://doi.org/10.1128/AEM.68.8.3737-3743.2002
  8. Watson AJ, Fuller LJ, Jeenes DJ, et al. Homologs of aflatoxin biosynthesis genes and sequence of aflR in Aspergillus oryzae and Aspergillus sojae. Appl Environ Microbiol. 1999;65(1):307-310. https://doi.org/10.1128/AEM.65.1.307-310.1999
  9. Arias RS, Orner VA, Martinez-Castillo J, et al. Aspergillus section flavi, need for a robust taxonomy. Microbiol Resour Announc. 2021;10(48):e0078421.
  10. Houbraken J, Visagie CM, Frisvad JC. Recommendations to prevent taxonomic misidentification of genome-sequenced fungal strains. Microbiol Resour Announc. 2021;10(48):e0107420.
  11. Kim KU, Kim KM, Choi YH, et al. Whole genome analysis of Aspergillus sojae SMF 134 supports its merits as a starter for soybean fermentation. J Microbiol. 2019;57(10):874-883. https://doi.org/10.1007/s12275-019-9152-1
  12. Bankevich A, Nurk S, Antipov D, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455-477. https://doi.org/10.1089/cmb.2012.0021
  13. Yu J, Chang P-K, Ehrlich KC, et al. Clustered pathway genes in aflatoxin biosynthesis. Appl Environ Microbiol. 2004;70(3):1253-1262. https://doi.org/10.1128/AEM.70.3.1253-1262.2004
  14. Chang P-K, Horn BW, Dorner JW. Clustered genes involved in cyclopiazonic acid production are next to the aflatoxin biosynthesis gene cluster in Aspergillus flavus. Fungal Genet Biol. 2009;46(2):176-182. https://doi.org/10.1016/j.fgb.2008.11.002
  15. Sato A, Oshima K, Noguchi H, et al. Draft genome sequencing and comparative analysis of Aspergillus sojae NBRC4239. DNA Res. 2011;18(3):165-176. https://doi.org/10.1093/dnares/dsr009
  16. Darling AC, Mau B, Blattner FR, et al. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14(7):1394-1403. https://doi.org/10.1101/gr.2289704
  17. Katoh K, Misawa K, Kuma K, et al. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30(14):3059-3066. https://doi.org/10.1093/nar/gkf436
  18. Chang P-K, Chang TD, Katoh K. Deciphering the origin of Aspergillus flavus NRRL21882, the active biocontrol agent of Afla-Guard. Lett Appl Microbiol. 2021;72(5):509-516.
  19. Ehrlich KC, Yu J, Cotty PJ. Aflatoxin biosynthesis gene clusters and flanking regions. J Appl Microbiol. 2005;99(3):518-527. https://doi.org/10.1111/j.1365-2672.2005.02637.x
  20. Calvo AM, Bok J, Brooks W, et al. veA is required for toxin and sclerotial production in Aspergillus parasiticus. Appl Environ Microbiol. 2004;70(8):4733-4739. https://doi.org/10.1128/AEM.70.8.4733-4739.2004
  21. Chang P-K, Scharfenstein LL, Li P, et al. Aspergillus flavus VelB acts distinctly from VeA in conidiation and may coordinate with FluG to modulate sclerotial production. Fungal Genet Biol. 2013;58-59:71-79. https://doi.org/10.1016/j.fgb.2013.08.009
  22. Kale SP, Milde L, Trapp MK, et al. Requirement of LaeA for secondary metabolism and sclerotial production in Aspergillus flavus. Fungal Genet Biol. 2008;45(10):1422-1429. https://doi.org/10.1016/j.fgb.2008.06.009
  23. Yuan XY, Li JY, Zhi QQ, et al. SfgA renders Aspergillus flavus more stable to the external environment. J Fungi. 2022;8(6):638.
  24. Jorgensen TR. Identification and toxigenic potential of the industrially important fungi, Aspergillus oryzae and Aspergillus sojae. J Food Prot. 2007;70(12):2916-2972. https://doi.org/10.4315/0362-028X-70.12.2916
  25. Machida M, Yamada O, Gomi K. Genomics of Aspergillus oryzae: learning from the history of koji mold and exploration of its future. DNA Res. 2008;15(4):173-183. https://doi.org/10.1093/dnares/dsn020
  26. Feng GH, Leonard TJ. Characterization of the polyketide synthase gene (pksL1) required for aflatoxin biosynthesis in Aspergillus parasiticus. J Bacteriol. 1995;177(21):6246-6254. https://doi.org/10.1128/jb.177.21.6246-6254.1995
  27. Chang P-K, Ehrlich KC, Yu J, et al. Increased expression of Aspergillus parasiticus aflR, encoding a sequence-specific DNA-binding protein, relieves nitrate inhibition of aflatoxin biosynthesis. Appl Environ Microbiol. 1995;61(6):2372-2377. https://doi.org/10.1128/aem.61.6.2372-2377.1995
  28. Chang P-K, Matsushima K, Takahashi T, et al. Understanding nonaflatoxigenicity of Aspergillus sojae: a windfall of aflatoxin biosynthesis research. Appl Microbiol Biotechnol. 2007;76(5):977-984. https://doi.org/10.1007/s00253-007-1116-4
  29. Watarai N, Yamamoto N, Sawada K, et al. Evolution of Aspergillus oryzae before and after domestication inferred by large-scale comparative genomic analysis. DNA Res. 2019;26(6):465-472. https://doi.org/10.1093/dnares/dsz024
  30. Garber NP, Cotty PJ. Aspergillus parasiticus communities associated with sugarcane in the Rio Grande Valley of Texas: implications of global transport and host association within Aspergillus section flavi. Phytopathology. 2014;104(5):462-471. https://doi.org/10.1094/PHYTO-04-13-0108-R
  31. Faustinelli PC, Wang XM, Palencia ER, et al. Genome sequences of eight Aspergillus flavus spp. and one A. parasiticus sp., isolated from peanut seeds in Georgia. Genome Announc. 2016;4(2):e00278-e00216.
  32. Zhao G, Yao Y, Hou L, et al. Draft genome sequence of Aspergillus oryzae 100-8, an increased acid protease production strain. Genome Announc. 2014;2(3):e00548-14.
  33. Zhao G, Yao Y, Qi W, et al. Draft genome sequence of Aspergillus oryzae strain 3.042. Eukaryot Cell. 2012;11(9):1178.
  34. Chang P-K. Genome-wide nucleotide variation distinguishes Aspergillus flavus from Aspergillus oryzae and helps to reveal origins of atoxigenic A. flavus biocontrol strains. J Appl Microbiol. 2019;127(5):1511-1520. https://doi.org/10.1111/jam.14419
  35. Pildain MB, Frisvad JC, Vaamonde G, et al. Two novel aflatoxin-producing Aspergillus species from Argentinean peanuts. Int J Syst Evol Microbiol. 2008;58(3):725-735. https://doi.org/10.1099/ijs.0.65123-0
  36. Linz JE, Wee J, Roze LV. Aspergillus parasiticus SU-1 genome sequence, predicted chromosome structure, and comparative gene expression under aflatoxin-inducing conditions: evidence that differential expression contributes to species phenotype. Eukaryot Cell. 2014;13(8):1113-1123. https://doi.org/10.1128/EC.00108-14
  37. Kjaerbolling I, Vesth T, Frisvad JC, et al. A comparative genomics study of 23 Aspergillus species from section flavi. Nat Commun. 2020;11(1):1106.
  38. Steenwyk JL, Shen XX, Lind AL, et al. A robust phylogenomic time tree for biotechnologically and medically important fungi in the genera Aspergillus and Penicillium. mBio. 2019;10(4):e00925-19.