Journal of Microbiology

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Metal ion homeostasis regulates condensin-dependent chromatin architecture and chromosome segregation in Schizosaccharomyces pombe: Seong Ho An, Kyoung-Dong Kim; J. Microbiol. 2025;63(9):e2505008. Published online August 29, 2025; DOI: https://doi.org/10.71150/jm.2505008

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Abstract PDF Supplementary Material: Condensin plays a central role in mitotic chromosome organization and segregation by mediating long-range chromatin interactions. However, the extent to which cellular metabolic status influences condensin function remains unclear. To gain insights into the relationship of metal ion homeostasis and the function of condensin, we conducted genome-wide chromatin immunoprecipitation sequencing (ChIP-seq) using Schizosaccharomyces pombe under iron- or zinc-deficient conditions. Under iron- or zinc-deficient conditions, ChIP-seq results revealed a selective reduction in condensin binding at high-affinity target loci, particularly genes regulated by Ace2 and Ams2, while cohesin binding remained largely unaffected. Hi-C analysis showed that iron depletion weakened chromatin interactions at these condensin targets and centromeres, without disrupting global genome architecture. DNA fluorescence in situ hybridization (FISH) confirmed that iron deficiency impaired long-range associations between centromeres and Ace2 target loci at the single-cell level. Notably, iron deficiency led to chromosome segregation defects during mitosis, suggesting that diminished condensin occupancy compromised genome stability. These changes occurred without significant alterations in condensin protein levels or global transcription, indicating a direct effect of metal ion availability on condensin activity. Collectively, our findings revealed a previously unrecognized regulatory axis in which cellular metal ion homeostasis modulated condensin-dependent chromatin organization and mitotic chromosome segregation, offering new insights into the integration of metabolic state with genome maintenance.

Journal Articles

Non-Mitochondrial Aconitase-2 Mediates the Transcription of Nuclear-Encoded Electron Transport Chain Genes in Fission Yeast: Ho-Jung Kim, Soo-Yeon Cho, Soo-Jin Jung, Yong-Jun Cho, Jung-Hye Roe, Kyoung-Dong Kim; J. Microbiol. 2024;62(8):639-648. Published online June 25, 2024; DOI: https://doi.org/10.1007/s12275-024-00147-8

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Abstract PDF: Aconitase-2 (Aco2) is present in the mitochondria, cytosol, and nucleus of fission yeast. To explore its function beyond the well-known role in the mitochondrial tricarboxylic acid (TCA) cycle, we conducted genome-wide profiling using the aco2ΔNLS mutant, which lacks a nuclear localization signal (NLS). The RNA sequencing (RNA-seq) data showed a general downregulation of electron transport chain (ETC) genes in the aco2ΔNLS mutant, except for those in the complex II, leading to a growth defect in respiratory-prone media. Complementation analysis with non-catalytic Aco2 [aco2ΔNLS + aco2(3CS)], where three cysteines were substituted with serine, restored normal growth and typical ETC gene expression. This suggests that Aco2's catalytic activity is not essential for its role in ETC gene regulation. Our mRNA decay assay indicated that the decrease in ETC gene expression was due to transcriptional regulation rather than changes in mRNA stability. Additionally, we investigated the Php complex's role in ETC gene regulation and found that ETC genes, except those within complex II, were downregulated in php3Δ and php5Δ strains, similar to the aco2ΔNLS mutant. These findings highlight a novel role for nuclear aconitase in ETC gene regulation and suggest a potential connection between the Php complex and Aco2.

Non-mitochondrial aconitase regulates the expression of iron-uptake genes by controlling the RNA turnover process in fission yeast: Soo-Yeon Cho , Soo-Jin Jung , Kyoung-Dong Kim , Jung-Hye Roe; J. Microbiol. 2021;59(12):1075-1082. Published online October 26, 2021; DOI: https://doi.org/10.1007/s12275-021-1438-4

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Abstract PDF

Aconitase, a highly conserved protein across all domains of life, functions in converting citrate to isocitrate in the tricarboxylic acid cycle. Cytosolic aconitase is also known to act as an iron regulatory protein in mammals, binding to the RNA hairpin structures known as iron-responsive elements within the untranslated regions of specific RNAs. Aconitase-2 (Aco2) in fission yeast is a fusion protein consisting of an aconitase and a mitochondrial ribosomal protein, bL21, residing not only in mitochondria but also in cytosol and the nucleus. To investigate the role of Aco2 in the nucleus and cytoplasm of fission yeast, we analyzed the transcriptome of aco2ΔN mutant that is deleted of nuclear localization signal (NLS). RNA sequencing revealed that the aco2ΔN mutation caused increase in mRNAs encoding iron uptake transporters, such as Str1, Str3, and Shu1. The half-lives of mRNAs for these genes were found to be significantly longer in the aco2ΔN mutant than the wild-type strain, suggesting the role of Aco2 in mRNA turnover. The three conserved cysteines required for the catalytic activity of aconitase were not necessary for this role. The UV cross-linking RNA immunoprecipitation analysis revealed that Aco2 directly bound to the mRNAs of iron uptake transporters. Aco2-mediated degradation of iron-uptake mRNAs appears to utilize exoribonuclease pathway that involves Rrp6 as evidenced by genetic interactions. These results reveal a novel role of non-mitochondrial aconitase protein in the mRNA turnover in fission yeast to fine-tune iron homeostasis, independent of regulation by transcriptional repressor Fep1.

Citations

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Review

[Minireview]Potential roles of condensin in genome organization and beyond in fission yeast: Kyoung-Dong Kim; J. Microbiol. 2021;59(5):449-459. Published online April 20, 2021; DOI: https://doi.org/10.1007/s12275-021-1039-2

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The genome is highly organized hierarchically by the function of structural maintenance of chromosomes (SMC) complex proteins such as condensin and cohesin from bacteria to humans. Although the roles of SMC complex proteins have been well characterized, their specialized roles in nuclear processes remain unclear. Condensin and cohesin have distinct binding sites and mediate long-range and short-range genomic associations, respectively, to form cell cycle-specific genome organization. Condensin can be recruited to highly expressed genes as well as dispersed repeat genetic elements, such as Pol III-transcribed genes, LTR retrotransposon, and rDNA repeat. In particular, mitotic transcription factors Ace2 and Ams2 recruit condensin to their target genes, forming centromeric clustering during mitosis. Condensin is potentially involved in various chromosomal processes such as the mobility of chromosomes, chromosome territories, DNA reannealing, and transcription factories. The current knowledge of condensin in fission yeast summarized in this review can help us understand how condensin mediates genome organization and participates in chromosomal processes in other organisms.

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