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Symmetric and asymmetric DNA N6-adenine methylation regulates different biological responses in Mucorales

Author

Listed:
  • Carlos Lax

    (Universidad de Murcia)

  • Stephen J. Mondo

    (Lawrence Berkeley National Laboratory
    Colorado State University
    Lawrence Berkeley National Laboratory)

  • Macario Osorio-Concepción

    (Universidad de Murcia)

  • Anna Muszewska

    (Polish Academy of Sciences)

  • María Corrochano-Luque

    (Universidad de Sevilla)

  • Gabriel Gutiérrez

    (Universidad de Sevilla)

  • Robert Riley

    (Lawrence Berkeley National Laboratory)

  • Anna Lipzen

    (Lawrence Berkeley National Laboratory)

  • Jie Guo

    (Lawrence Berkeley National Laboratory)

  • Hope Hundley

    (Lawrence Berkeley National Laboratory)

  • Mojgan Amirebrahimi

    (Lawrence Berkeley National Laboratory)

  • Vivian Ng

    (Lawrence Berkeley National Laboratory)

  • Damaris Lorenzo-Gutiérrez

    (Universidad de Murcia)

  • Ulrike Binder

    (Medical University of Innsbruck)

  • Junhuan Yang

    (Lingnan Normal University)

  • Yuanda Song

    (Shandong University of Technology)

  • David Cánovas

    (Universidad de Sevilla)

  • Eusebio Navarro

    (Universidad de Murcia)

  • Michael Freitag

    (Oregon State University)

  • Toni Gabaldón

    (Barcelona Supercomputing Centre (BSC-CNS)
    The Barcelona Institute of Science and Technology
    Catalan Institution for Research and Advanced Studies (ICREA)
    Centro de Investigación Biomédica en Red de Enfermedades Infecciosas (CIBERINFEC))

  • Igor V. Grigoriev

    (Lawrence Berkeley National Laboratory
    Lawrence Berkeley National Laboratory
    University of California Berkeley)

  • Luis M. Corrochano

    (Universidad de Sevilla)

  • Francisco E. Nicolás

    (Universidad de Murcia)

  • Victoriano Garre

    (Universidad de Murcia)

Abstract

DNA N6-adenine methylation (6mA) has recently gained importance as an epigenetic modification in eukaryotes. Its function in lineages with high levels, such as early-diverging fungi (EDF), is of particular interest. Here, we investigated the biological significance and evolutionary implications of 6mA in EDF, which exhibit divergent evolutionary patterns in 6mA usage. The analysis of two Mucorales species displaying extreme 6mA usage reveals that species with high 6mA levels show symmetric methylation enriched in highly expressed genes. In contrast, species with low 6mA levels show mostly asymmetric 6mA. Interestingly, transcriptomic regulation throughout development and in response to environmental cues is associated with changes in the 6mA landscape. Furthermore, we identify an EDF-specific methyltransferase, likely originated from endosymbiotic bacteria, as responsible for asymmetric methylation, while an MTA-70 methylation complex performs symmetric methylation. The distinct phenotypes observed in the corresponding mutants reinforced the critical role of both types of 6mA in EDF.

Suggested Citation

  • Carlos Lax & Stephen J. Mondo & Macario Osorio-Concepción & Anna Muszewska & María Corrochano-Luque & Gabriel Gutiérrez & Robert Riley & Anna Lipzen & Jie Guo & Hope Hundley & Mojgan Amirebrahimi & Vi, 2024. "Symmetric and asymmetric DNA N6-adenine methylation regulates different biological responses in Mucorales," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50365-2
    DOI: 10.1038/s41467-024-50365-2
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    References listed on IDEAS

    as
    1. Bårbel M. R. Stadler & Peter F. Stadler & Peter R. Wills, 2001. "Evolution in Systems of Ligation-Based Replicators," Working Papers 01-09-052, Santa Fe Institute.
    2. Luis Javier Galindo & Purificación López-García & Guifré Torruella & Sergey Karpov & David Moreira, 2021. "Phylogenomics of a new fungal phylum reveals multiple waves of reductive evolution across Holomycota," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    3. Jiyun Chen & Rong Hu & Ying Chen & Xiaofeng Lin & Wenwen Xiang & Hong Chen & Canglin Yao & Liang Liu, 2022. "Structural basis for MTA1c-mediated DNA N6-adenine methylation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Jie Zhao & Meng Zhang & Wenyan Hui & Yue Zhang & Jing Wang & Shaojing Wang & Lai-Yu Kwok & Jian Kong & Heping Zhang & Wenyi Zhang, 2023. "Roles of adenine methylation in the physiology of Lacticaseibacillus paracasei," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
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