Decoupling between the genetic potential and the metabolic regulation and expression in microbial organic matter cleavage across microbiomes

Author(s)

Zihao Zhao, Federico Baltar, Gerhard J Herndl

Abstract

UNLABELLED: Metagenomics, metatranscriptomics, and metaproteomics are used to explore the microbial capability of enzyme secretion, but the links between protein-encoding genes and corresponding transcripts/proteins across ecosystems are underexplored. By conducting a multi-omics comparison focusing on key enzymes (carbohydrate-active enzymes [CAZymes] and peptidases) cleaving the main biomolecules across distinct microbiomes living in the ocean, soil, and human gut, we show that the community structure, functional diversity, and secretion mechanisms of microbial secretory CAZymes and peptidases vary drastically between microbiomes at metagenomic, metatranscriptomic, and metaproteomic levels. Such variations lead to decoupled relationships between CAZymes and peptidases from genetic potentials to protein expressions due to the different responses of key players toward organic matter sources and concentrations. Our results highlight the need for systematic analysis of the factors shaping patterns of microbial cleavage on organic matter to better link omics data to ecosystem processes.

IMPORTANCE: Omics tools are used to explore adaptive mechanism of microbes in diverse systems, but the advantages and limitations of different omics tools remain skeptical. Here, we reported distinct profiles in microbial secretory enzyme composition revealed by different omics methods. In general, the predicted function from metagenomic analysis decoupled from the expression of corresponding transcripts/proteins. Linking omics results to taxonomic origin, functional capability, substrate specificity, secretion preference, and enzymatic activity measurement suggested the substrate's source, concentration and stoichiometry impose strong filtering on the expression of extracellular enzymes, which may overwrite the genetic potentials. Our results present an integrated perspective on the need for multi-dimensional characterization of microbial adaptation in a changing environment.

Organisation(s)

Functional and Evolutionary Ecology

External organisation(s)

Universität Wien, Royal Netherlands Institute for Sea Research, Medizinische Universität Wien

Journal

Microbiology Spectrum

Pages

e0303623

ISSN

2165-0497

DOI

https://doi.org/10.1128/spectrum.03036-23

Publication date

2024

Peer reviewed

Yes

Austrian Fields of Science 2012

106021 Marine biology

Sustainable Development Goals

SDG 14 - Life Below Water

Portal url

https://ucris.univie.ac.at/portal/en/publications/decoupling-between-the-genetic-potential-and-the-metabolic-regulation-and-expression-in-microbial-organic-matter-cleavage-across-microbiomes(1b56defa-a04b-4e8d-89d8-b7bee2d06e78).html