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Novel chromosomes and genomes provide new insights into evolution and adaptation of the whole genome duplicated yeast-like fungus TN3-1 isolated from natural honey

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Abstract

Aureobasidium melanogenum TN3-1 strain and A. melanogenum P16 strain were isolated from the natural honey and the mangrove ecosystem, respectively. The former can produce much higher pullulan from high concentration of glucose than the latter. In order to know what happened to their genomes, the PacBio sequencing and Hi-C technologies were used to create the first high-quality chromosome-level reference genome assembly of A. melanogenum TN3-1 (51.61 Mb) and A. melanogenum P16 (25.82 Mb) with the contig N50 of 2.19 Mb and 2.26 Mb, respectively. Based on the Hi-C results, a total of 93.33% contigs in the TN3-1 strain and 92.31% contigs in the P16 strain were anchored onto 24 and 12 haploid chromosomes, respectively. The genomes of the TN3-1 strain had two subgenomes A and B. Synteny analysis showed that the genomic contents of the two subgenomes were asymmetric with many structural variations. Intriguingly, the TN3-1 strain was revealed as a recent hybrid/fusion between the ancestor of A. melanogenum CBS105.22/CBS110374 and the ancestor of another unidentified strain of A. melanogenum similar to P16 strain. We estimated that the two ancient progenitors diverged around 18.38 Mya and merged around 10.66–9.98 Mya. It was found that in the TN3-1 strain, telomeres of each chromosome contained high level of long interspersed nuclear elements (LINEs), but had low level of the telomerase encoding gene. Meanwhile, there were high level of transposable elements (TEs) inserted in the chromosomes of the TN3-1 strain. In addition, the positively selected genes of the TN3-1 strain were mainly enriched in the metabolic processes related to harsh environmental adaptability. Most of the stress-related genes were found to be related to the adjacent LTRs, and the glucose derepression was caused by the mutation of the Glc7-2 in the Snf-Mig1 system. All of these could contribute to its genetic instability, genome evolution, high stress resistance, and high pullulan production from glucose.

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Funding

The research work was supported by the research grants from National Natural Science Foundation of China (Grant Nos. 31970058 and 31770061) and by the research grant from the Fundamental Research Funds for the Central Universities (Grant No. 202061009).

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Authors and Affiliations

  1. College of Marine Life Sciences, Ocean University of China, Yushan Road, No. 5, Qingdao, China

    Shu-Lei Jia, Mei Zhang, Guang-Lei Liu, Zhen-Ming Chi & Zhe Chi

  2. Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266003, China

    Guang-Lei Liu, Zhen-Ming Chi & Zhe Chi

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  1. Shu-Lei Jia
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  2. Mei Zhang
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  3. Guang-Lei Liu
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Shu-Lei Jia and Zhe Chi conceived the study. Guang-Lei Liu was responsible for bioinformatic analysis. Mei Zhang contributed to the experimental work. Zhen-Ming Chi wrote the article with contributions from all other authors. All the authors approved the article before submission.

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Jia, SL., Zhang, M., Liu, GL. et al. Novel chromosomes and genomes provide new insights into evolution and adaptation of the whole genome duplicated yeast-like fungus TN3-1 isolated from natural honey. Funct Integr Genomics 23, 206 (2023). https://doi.org/10.1007/s10142-023-01127-8

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