Abstract

Microbial biosynthetic gene clusters (BGCs) encoding secondary metabolites are thought to impact a plethora of biologically mediated environmental processes, yet their discovery and functional characterization in natural microbiomes remains challenging. Here we describe deep long-read sequencing and assembly of metagenomes from biological soil crusts, a group of soil communities that are rich in BGCs. Taking advantage of the unusually long assemblies produced by this approach, we recovered nearly 3,000 BGCs for analysis, including 712 full-length BGCs. Functional exploration through metatranscriptome analysis of a 3-day wetting experiment uncovered phylum-specific BGC expression upon activation from dormancy, elucidating distinct roles and complex phylogenetic and temporal dynamics in wetting processes. For example, a pronounced increase in BGC transcription occurs at night primarily in cyanobacteria, implicating BGCs in nutrient scavenging roles and niche competition. Taken together, our results demonstrate that long-read metagenomic sequencing combined with metatranscriptomic analysis provides a direct view into the functional dynamics of BGCs in environmental processes and suggests a central role of secondary metabolites in maintaining phylogenetically conserved niches within biocrusts.

Highlights

  • Microbial biosynthetic gene clusters (BGCs) encoding secondary metabolites are thought to impact a plethora of biologically mediated environmental processes, yet their discovery and functional characterization in natural microbiomes remains challenging

  • Previous work has demonstrated the potential for deep shotgun metagenomic sequencing to directly characterize BGCs from environmental samples[10,11], but the assembly of full-length BGCs from short reads is associated with major limitations[12]

  • We found 17 phenazines in our dataset, most of which belonged to cyanobacteria, and some of which may have functions in redox balance during anoxia[46], which frequently occurs in biocrust after intense rain events

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Summary

Introduction

Microbial biosynthetic gene clusters (BGCs) encoding secondary metabolites are thought to impact a plethora of biologically mediated environmental processes, yet their discovery and functional characterization in natural microbiomes remains challenging. Our results demonstrate that long-read metagenomic sequencing combined with metatranscriptomic analysis provides a direct view into the functional dynamics of BGCs in environmental processes and suggests a central role of secondary metabolites in maintaining phylogenetically conserved niches within biocrusts. Our results showed that thousands of gene clusters could be extracted from assembled long-read metagenomes which gave insight into the secondary metabolism of uncultivated microbial taxa Coupling these results to metatranscriptomics indicated that most BGCs were transcribed after a simulated rain event, and that cyanobacteria dominated secondary metabolism throughout the experiment

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