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Integration of time-series meta-omics data reveals how microbial ecosystems respond to disturbance.

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.

SUBMITTER: Herold M

PROVIDER: S-EPMC7572474 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Integration of time-series meta-omics data reveals how microbial ecosystems respond to disturbance.

Herold Malte M Martínez Arbas Susana S Narayanasamy Shaman S Sheik Abdul R AR Kleine-Borgmann Luise A K LAK Lebrun Laura A LA Kunath Benoît J BJ Roume Hugo H Bessarab Irina I Williams Rohan B H RBH Gillece John D JD Schupp James M JM Keim Paul S PS Jäger Christian C Hoopmann Michael R MR Moritz Robert L RL Ye Yuzhen Y Li Sujun S Tang Haixu H Heintz-Buschart Anna A May Patrick P Muller Emilie E L EEL Laczny Cedric C CC Wilmes Paul P

Nature communications 20201019 1

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 ge ...[more]

PMID: 33077707

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Project description:BackgroundMicrobe-microbe interactions between members of the plant rhizosphere are important but remain poorly understood. A more comprehensive understanding of the molecular mechanisms used by microbes to cooperate, compete, and persist has been challenging because of the complexity of natural ecosystems and the limited control over environmental factors. One strategy to address this challenge relies on studying complexity in a progressive manner, by first building a detailed understanding of relatively simple subsets of the community and then achieving high predictive power through combining different building blocks (e.g., hosts, community members) for different environments. Herein, we coupled this reductionist approach with high-resolution mass spectrometry-based metaproteomics to study molecular mechanisms driving community assembly, adaptation, and functionality for a defined community of ten taxonomically diverse bacterial members of Populus deltoides rhizosphere co-cultured either in a complex or defined medium.ResultsMetaproteomics showed this defined community assembled into distinct microbiomes based on growth media that eventually exhibit composition and functional stability over time. The community grown in two different media showed variation in composition, yet both were dominated by only a few microbial strains. Proteome-wide interrogation provided detailed insights into the functional behavior of each dominant member as they adjust to changing community compositions and environments. The emergence and persistence of select microbes in these communities were driven by specialization in strategies including motility, antibiotic production, altered metabolism, and dormancy. Protein-level interrogation identified post-translational modifications that provided additional insights into regulatory mechanisms influencing microbial adaptation in the changing environments.ConclusionsThis study provides high-resolution proteome-level insights into our understanding of microbe-microbe interactions and highlights specialized biological processes carried out by specific members of assembled microbiomes to compete and persist in changing environmental conditions. Emergent properties observed in these lower complexity communities can then be re-evaluated as more complex systems are studied and, when a particular property becomes less relevant, higher-order interactions can be identified.

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Integration of time-series meta-omics data reveals how microbial ecosystems respond to disturbance.

Publications

Integration of time-series meta-omics data reveals how microbial ecosystems respond to disturbance.

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