Abstract

The development of reliable, mixed-culture biotechnological processes hinges on understanding how microbial ecosystems respond to disturbances. Here we reveal extensive phenotypic plasticity and niche complementarity in oleaginous microbial populations from a biological wastewater treatment plant. We perform meta-omics analyses (metagenomics, metatranscriptomics, metaproteomics and metabolomics) on in situ samples over 14 months at weekly intervals. Based on 1,364 de novo metagenome-assembled genomes, we uncover four distinct fundamental niche types. Throughout the time-series, we observe a major, transient shift in community structure, coinciding with substrate availability changes. Functional omics data reveals extensive variation in gene expression and substrate usage amongst community members. Ex situ bioreactor experiments confirm that responses occur within five hours of a pulse disturbance, demonstrating rapid adaptation by specific populations. Our results show that community resistance and resilience are a function of phenotypic plasticity and niche complementarity, and set the foundation for future ecological engineering efforts.

Highlights

  • The development of reliable, mixed-culture biotechnological processes hinges on understanding how microbial ecosystems respond to disturbances

  • Gene expression, and activity of individual microbial populations over time, we dereplicated[29] the metagenome-assembled genomes (MAGs) across samples to generate 220 representative MAGs. We further selected those with the highest completeness resulting in 78 rMAGs (76.2% mean completeness, 2.2% mean contamination) (Supplementary Data 2)

  • Per time-point, on average 1.5 × 104 ± 4.5 × 103 (s.d.) spectral matches, i.e., on average 94% of all rMAG-associated matches could be assigned to genes with predicted functions, i.e., assigned KEGG ortholog groups (KOs)

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Summary

Introduction

The development of reliable, mixed-culture biotechnological processes hinges on understanding how microbial ecosystems respond to disturbances. Integrated meta-omics approaches hold the potential to resolve the fundamental niches and realized niches of microbial populations in situ[15]. The reconstruction of the fundamental niches is possible by linking functional potential to metagenome-assembled genomes (MAGs)[16] obtained through metagenomic (MG) sequencing Functional omics data, such as metatranscriptomics (MT) or metaproteomics (MP), allow the resolution of realized niches[16]. Resolving the functions of coexisting microbial populations is of particular interest in the context of the extensive functional redundancy within microbial ecosystems[21,22] Based on their emergent properties[23], microbial communities are characterized by composite metabolic capabilities and increased robustness compared to individual strains[24,25]. Steering these complex systems towards a desired endpoint, e.g., increased lipid accumulation, requires in-depth understanding of niche space and stability

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