Novel soil bacteria possess diverse genes for secondary metabolite biosynthesis View Full Text


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Article Info

DATE

2018-06-13

AUTHORS

Alexander Crits-Christoph, Spencer Diamond, Cristina N. Butterfield, Brian C. Thomas, Jillian F. Banfield

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 taxa3, and the biosynthetic potential of the vast majority of bacteria in soil has rarely been investigated4. 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 biomes5. 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. More... »

PAGES

440-444

References to SciGraph publications

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  • 2014-07-08. Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology in THE ISME JOURNAL: MULTIDISCIPLINARY JOURNAL OF MICROBIAL ECOLOGY
  • 2008-12-29. WGCNA: an R package for weighted correlation network analysis in BMC BIOINFORMATICS
  • 2015-06-15. Unusual biology across a group comprising more than 15% of domain Bacteria in NATURE
  • 2014-01-29. An environmental bacterial taxon with a large and distinct metabolic repertoire in NATURE
  • 2014-09-14. Binning metagenomic contigs by coverage and composition in NATURE METHODS
  • 2018-05-28. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy in NATURE MICROBIOLOGY
  • 2014-12-05. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 in GENOME BIOLOGY
  • 2013-09-22. Identifying producers of antibacterial compounds by screening for antibiotic resistance in NATURE BIOTECHNOLOGY
  • 2016-04-04. Near-optimal probabilistic RNA-seq quantification in NATURE BIOTECHNOLOGY
  • 2016-10-24. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system in NATURE COMMUNICATIONS
  • 2016-02-01. Assembly and clustering of natural antibiotics guides target identification in NATURE CHEMICAL BIOLOGY
  • 2016-04-11. A new view of the tree of life in NATURE MICROBIOLOGY
  • 2012-03-04. Fast gapped-read alignment with Bowtie 2 in NATURE METHODS
  • 2015-08-18. Minimum Information about a Biosynthetic Gene cluster in NATURE CHEMICAL BIOLOGY
  • 2005-01. Bioactive Microbial Metabolites in THE JOURNAL OF ANTIBIOTICS
  • 2009-11-30. Bacterial competition: surviving and thriving in the microbial jungle in NATURE REVIEWS MICROBIOLOGY
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1038/s41586-018-0207-y

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    DIMENSIONS

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    30 schema:description 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 taxa3, and the biosynthetic potential of the vast majority of bacteria in soil has rarely been investigated4. 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 biomes5. 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.
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    38 Gemmatimonadetes
    39 Rokubacteria
    40 Verrucomicobia
    41 abundant bacterial phyla
    42 acidobacterial genomes
    43 activation
    44 antibiotics
    45 antifungals
    46 antimicrobial resistance
    47 bacteria
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    50 biosynthesis
    51 biosynthetic gene cluster
    52 biosynthetic genes
    53 biosynthetic locus
    54 biosynthetic potential
    55 candidate phylum Rokubacteria
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    58 communication
    59 competition
    60 complete genome
    61 compounds
    62 confidence
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