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Novel soil bacteria possess diverse genes for secondary metabolite biosynthesis

Author

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  • Alexander Crits-Christoph

    (University of California, Berkeley
    University of California, Berkeley)

  • Spencer Diamond

    (University of California, Berkeley)

  • Cristina N. Butterfield

    (University of California, Berkeley)

  • Brian C. Thomas

    (University of California, Berkeley)

  • Jillian F. Banfield

    (University of California, Berkeley
    University of California, Berkeley
    Policy, and Management, University of California, Berkeley
    Lawrence Berkeley National Laboratory)

Abstract

In soil ecosystems, microorganisms produce diverse secondary metabolites such as antibiotics, antifungals and siderophores that mediate communication, competition and interactions with other organisms and the environment1,2. Most known antibiotics are derived from a few culturable microbial taxa 3 , and the biosynthetic potential of the vast majority of bacteria in soil has rarely been investigated 4 . Here we reconstruct hundreds of near-complete genomes from grassland soil metagenomes and identify microorganisms from previously understudied phyla that encode diverse polyketide and nonribosomal peptide biosynthetic gene clusters that are divergent from well-studied clusters. These biosynthetic loci are encoded by newly identified members of the Acidobacteria, Verrucomicobia and Gemmatimonadetes, and the candidate phylum Rokubacteria. Bacteria from these groups are highly abundant in soils5–7, but have not previously been genomically linked to secondary metabolite production with confidence. In particular, large numbers of biosynthetic genes were characterized in newly identified members of the Acidobacteria, which is the most abundant bacterial phylum across soil biomes 5 . We identify two acidobacterial genomes from divergent lineages, each of which encodes an unusually large repertoire of biosynthetic genes with up to fifteen large polyketide and nonribosomal peptide biosynthetic loci per genome. To track gene expression of genes encoding polyketide synthases and nonribosomal peptide synthetases in the soil ecosystem that we studied, we sampled 120 time points in a microcosm manipulation experiment and, using metatranscriptomics, found that gene clusters were differentially co-expressed in response to environmental perturbations. Transcriptional co-expression networks for specific organisms associated biosynthetic genes with two-component systems, transcriptional activation, putative antimicrobial resistance and iron regulation, linking metabolite biosynthesis to processes of environmental sensing and ecological competition. We conclude that the biosynthetic potential of abundant and phylogenetically diverse soil microorganisms has previously been underestimated. These organisms may represent a source of natural products that can address needs for new antibiotics and other pharmaceutical compounds.

Suggested Citation

  • Alexander Crits-Christoph & Spencer Diamond & Cristina N. Butterfield & Brian C. Thomas & Jillian F. Banfield, 2018. "Novel soil bacteria possess diverse genes for secondary metabolite biosynthesis," Nature, Nature, vol. 558(7710), pages 440-444, June.
  • Handle: RePEc:nat:nature:v:558:y:2018:i:7710:d:10.1038_s41586-018-0207-y
    DOI: 10.1038/s41586-018-0207-y
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    Cited by:

    1. Alexander Bogdanov & Mariam N. Salib & Alexander B. Chase & Heinz Hammerlindl & Mitchell N. Muskat & Stephanie Luedtke & Elany Barbosa Silva & Anthony J. O’Donoghue & Lani F. Wu & Steven J. Altschuler, 2024. "Small molecule in situ resin capture provides a compound first approach to natural product discovery," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Xiaoqian Lin & Tongyuan Hu & Jianwei Chen & Hewei Liang & Jianwei Zhou & Zhinan Wu & Chen Ye & Xin Jin & Xun Xu & Wenwei Zhang & Xiaohuan Jing & Tao Yang & Jian Wang & Huanming Yang & Karsten Kristian, 2023. "The genomic landscape of reference genomes of cultivated human gut bacteria," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Bin Ma & Caiyu Lu & Yiling Wang & Jingwen Yu & Kankan Zhao & Ran Xue & Hao Ren & Xiaofei Lv & Ronghui Pan & Jiabao Zhang & Yongguan Zhu & Jianming Xu, 2023. "A genomic catalogue of soil microbiomes boosts mining of biodiversity and genetic resources," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Liming Xia & Youzhi Miao & A’li Cao & Yan Liu & Zihao Liu & Xinli Sun & Yansheng Xue & Zhihui Xu & Weibing Xun & Qirong Shen & Nan Zhang & Ruifu Zhang, 2022. "Biosynthetic gene cluster profiling predicts the positive association between antagonism and phylogeny in Bacillus," Nature Communications, Nature, vol. 13(1), pages 1-11, December.

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