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Biocontrol strain Aspergillus flavus WRRL 1519 has differences in chromosomal organization and an increased number of transposon-like elements compared to other strains

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Abstract

Aflatoxins are toxic secondary metabolites produced by members of the genus Aspergillus, most notably A. flavus. Non-aflatoxigenic strains of A. flavus are commonly used for biocontrol of the aflatoxigenic strains to reduce aflatoxins in corn, cotton, peanuts and tree nuts. However, genomic differences between aflatoxigenic strains and non-aflatoxigenic strains have not been reported in detail, though such differences may further elucidate the evolutionary histories of certain biocontrol strains and help guide development of other useful strains. We recently reported the genome and transcriptome sequencing of A. flavus WRRL 1519, a strain isolated from almond that does not produce aflatoxins or cyclopiazonic acid due to deletions in the biosynthetic gene clusters. Continued bioinformatics analyses focused on comparing strain WRRL 1519 to the aflatoxigenic strain NRRL 3357. The genome assembly of strain WRRL 1519 was improved by anchoring 84 of the 127 scaffolds to the putative nuclear chromosomes of strain NRRL 3357. The five largest areas of extrachromosomal mismatches observed between WRRL 1519 and NRRL 3357 were not similar to any of the mismatches that were observed with pairwise comparisons of NRRL 3357 to other non-aflatoxigenic strains NRRL 21882, NRRL 30797 or NRRL 18543. Comparisons of predicted secondary metabolite gene clusters uncovered two other biosynthetic gene clusters in which strain WRRL 1519 had large deletions compared to the homologous clusters in NRRL 3357. Additionally, there was a marked overrepresentation of repetitive sequences in WRRL 1519 compared to other inspected A. flavus strains. This is the first report of detection of a large number of putative retrotransposons in any A. flavus strain, initially suggesting that retrotransposons may contribute to the natural occurrence of genetic variation and biocontrol strains. However, the transposons may not be significantly associated with the chromosomal differences. Future experimentation and continued bioinformatics analyses will potentially illuminate causes of the differences and may reveal whether transposon activity in A. flavus can lead to random natural occurrences of non-aflatoxigenic strains.

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Funding

This work was funded by the USDA-ARS Non-Assistance Cooperative Agreement (no. 58-2030-6-053). Use of a company or product name by the U.S. Department of Agriculture does not imply approval or recommendation of the product to the exclusion of others that may also be suitable. We also greatly appreciate additional funding received from the Rutgers University Educational Opportunity Fund (J Gonzalez) and the Mycological Society of America John W. Rippon Award (KK Pennerman).

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Authors and Affiliations

  1. Department of Plant Biology, Rutgers, The State University of New Jersey, New Brunswick, NJ, 08901, USA

    Kayla K. Pennerman, Johanny Gonzalez, Lydia R. Chenoweth, Joan W. Bennett & Guohua Yin

  2. New Mexico Consortium and Pebble Labs Inc., Los Alamos, NM, 87544, USA

    Guohua Yin

  3. U.S. Department of Agriculture, ARS Western Regional Research Center, Albany, CA, 94710, USA

    Sui Sheng T. Hua

Authors
  1. Kayla K. Pennerman
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  2. Johanny Gonzalez
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  3. Lydia R. Chenoweth
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  4. Joan W. Bennett
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  5. Guohua Yin
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  6. Sui Sheng T. Hua
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Corresponding author

Correspondence to Sui Sheng T. Hua.

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Conflict of interest

KK Pennerman declares that she has no conflict of interest. J Gonzalez declares that she has no conflict of interest. LF Chenoweth declares that she has no conflict of interest. JW Bennett declares that she has no conflict of interest. G Yin declares that she has no conflict of interest. SST Hua declares that she has no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

438_2018_1474_MOESM1_ESM.eps

Supplementary Figure 1. Scaffold matching of NRRL 3357 to (A) itself, (B) NRRL 21882, (C) NRRL 30797 and (D) NRRL 18543. Chromosomes of NRRL 3357 are drawn in 16 different colors on the left side of each diagram. The outer track enumerates chromosome nucleotide length in kilobase pairs, and protein-coding gene density is shown by a histogram on the inner track. Scaffolds and chromosomes are connected to the NRRL 3357 chromosomes by lines representing high sequence similarity between two protein-coding genes. There is one extrachromosomal mismatch between NRRL 3357 chromosomes EQ963477.1 to EQ963476.12 due to a match to an apparent paralog. Many of the mismatches between NRRL 3357 and a non-aflatoxigenic strain are the same for different strains. (EPS 9861 KB)

Supplementary material 2 (EPS 9253 KB)

Supplementary material 3 (EPS 9490 KB)

Supplementary material 4 (EPS 9511 KB)

438_2018_1474_MOESM5_ESM.pdf

Supplementary Figure 2. Scaffold organization of strain WRRL 1519. The scaffolds are ordered according to their relative placement to the centromeres. Blue and orange colors indicate the nucleotide sequence direction of the scaffold relative to the deposited NRRL 3357 genomic sequence. An asterisk denotes scaffolds on which one or more AFLAV-like sequences were found by either HMMER or RepeatMasker. Scaffolds 59, 72, 73 and 113 in which AFLAV-like sequences were detected are not represented because they were not confidently aligned to the NRRL 3357 chromosomes. The diagram is not to scale. (PDF 193 KB)

438_2018_1474_MOESM6_ESM.pdf

Supplementary Figure 3. Macrosynteny of A. flavus (A) NRRL 21882, (B) NRRL 30797, (C) NRRL 18543 and (D) WRRL 1519 scaffolds to NRRL 3357 chromosomes. Scaffolds of the strains are listed in the same relative orders as in Figure 2 and Supplementary Figure 1. (PDF 163 KB)

438_2018_1474_MOESM7_ESM.pdf

Supplementary Figure 4. Full alignment of WRRL 1519 candidate retrotransposons to retrotransposon AFLAV AY485786.2 from A. flavus NRRL 3357. Candidate retrotransposons are labeled according to Supplementary Table 4. Black and gray shading indicates strength of nucleotide consensus. The LTR regions, ORF1, ribosomal-1 frameshift site and ORF2 of AY485786.2 are highlighted in yellow, blue, orange and green, respectively. (PDF 1161 KB)

438_2018_1474_MOESM8_ESM.xlsx

Supplementary Table 1. Summary of non-aflatoxigenic A. flavus genome scaffolds matching to putative NRRL 3357 chromosomes. (XLSX 24 KB)

438_2018_1474_MOESM9_ESM.xlsx

Supplementary Table 2. Summary of results of sequence similarity searches of WRRL 1519 putative proteins against the annotated NRRL 3357 proteome. (XLSX 1323 KB)

Supplementary Table 3. Counts of predicted secondary metabolite gene clusters by predicted products. (DOCX 14 KB)

Supplementary Table 4. Candidate AFLAV-like retrotransposons in WRRL 1519. (DOCX 15 KB)

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Pennerman, K.K., Gonzalez, J., Chenoweth, L.R. et al. Biocontrol strain Aspergillus flavus WRRL 1519 has differences in chromosomal organization and an increased number of transposon-like elements compared to other strains. Mol Genet Genomics 293, 1507–1522 (2018). https://doi.org/10.1007/s00438-018-1474-x

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