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Identification of peptides from honeybee gut symbionts as potential antimicrobial agents against Melissococcus plutonius

Author

Listed:
  • Haoyu Lang

    (China Agricultural University)

  • Yuwen Liu

    (China Agricultural University)

  • Huijuan Duan

    (China Agricultural University)

  • Wenhao Zhang

    (China Agricultural University)

  • Xiaosong Hu

    (China Agricultural University)

  • Hao Zheng

    (China Agricultural University)

Abstract

Eusocial pollinators are crucial elements in global agriculture. The honeybees and bumblebees are associated with a simple yet host-restricted gut community, which protect the hosts against pathogen infections. Recent genome mining has led to the discovery of biosynthesis pathways of bioactive natural products mediating microbe-microbe interactions from the gut microbiota. Here, we investigate the diversity of biosynthetic gene clusters in the bee gut microbiota by analyzing 477 genomes from cultivated bacteria and metagenome-assembled genomes. We identify 744 biosynthetic gene clusters (BGCs) covering multiple chemical classes. While gene clusters for the post-translationally modified peptides are widely distributed in the bee guts, the distribution of the BGC classes varies significantly in different bee species among geographic locations, which is attributed to the strain-level variation of bee gut members in the chemical repertoire. Interestingly, we find that Gilliamella strains possessing a thiopeptide-like BGC show potent activity against the pathogenic Melissococcus plutonius. The spectrometry-guided genome mining reveals a RiPP-encoding BGC from Gilliamella with a 10 amino acid-long core peptide exhibiting antibacterial potentials. This study illustrates the widespread small-molecule-encoding BGCs in the bee gut symbionts and provides insights into the bacteria-derived natural products as potential antimicrobial agents against pathogenic infections.

Suggested Citation

  • Haoyu Lang & Yuwen Liu & Huijuan Duan & Wenhao Zhang & Xiaosong Hu & Hao Zheng, 2023. "Identification of peptides from honeybee gut symbionts as potential antimicrobial agents against Melissococcus plutonius," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43352-6
    DOI: 10.1038/s41467-023-43352-6
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    1. Richard S. Ayikpoe & Chengyou Shi & Alexander J. Battiste & Sara M. Eslami & Sangeetha Ramesh & Max A. Simon & Ian R. Bothwell & Hyunji Lee & Andrew J. Rice & Hengqian Ren & Qiqi Tian & Lonnie A. Harr, 2022. "A scalable platform to discover antimicrobials of ribosomal origin," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Haoyu Lang & Hao Wang & Haoqing Wang & Zhaopeng Zhong & Xianbing Xie & Wenhao Zhang & Jun Guo & Liang Meng & Xiaosong Hu & Xue Zhang & Hao Zheng, 2023. "Engineered symbiotic bacteria interfering Nosema redox system inhibit microsporidia parasitism in honeybees," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Kirsten M. Ellegaard & Philipp Engel, 2019. "Genomic diversity landscape of the honey bee gut microbiota," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    4. Francesco Asnicar & Andrew Maltez Thomas & Francesco Beghini & Claudia Mengoni & Serena Manara & Paolo Manghi & Qiyun Zhu & Mattia Bolzan & Fabio Cumbo & Uyen May & Jon G. Sanders & Moreno Zolfo & Evg, 2020. "Precise phylogenetic analysis of microbial isolates and genomes from metagenomes using PhyloPhlAn 3.0," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
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