Why Environmental Biomarkers Work: Transcriptome-Proteome Correlations and Modeling of Multistressor Experiments in the Marine Bacterium Trichodesmium

Ocean microbial communities are important contributors to the global biogeochemical reactions that sustain life on Earth. The factors controlling these communities are being increasingly explored using metatranscriptomic and metaproteomic environmental biomarkers. Using published proteomes and transcriptomes from the abundant colony-forming cyanobacterium Trichodesmium (strain IMS101) grown under varying Fe and/or P limitation in low and high CO2, we observed robust correlations of stress induced proteins and RNAs (i.e., involved in transport and homeostasis) that yield useful information on the nutrient status under low and/or high CO2. Conversely, transcriptional and translational correlations of many other central metabolism pathways exhibit broad discordance. A cellular RNA and protein production/degradation model demonstrates how biomolecules with small initial inventories, such as environmentally responsive proteins, achieve large increases in fold-change units as opposed to those with a higher basal expression and inventory such as metabolic systems. Microbial cells, due to their immersion in the environment, tend to show large adaptive responses in both RNA and protein that result in transcript-protein correlations. These observations and model results demonstrate multi-omic coherence for environmental biomarkers and provide the underlying mechanism for those observations, supporting the promise for global in to environmental stimuli in a ocean.

Automated summary

Ocean microbial communities play a crucial role in sustaining life on Earth, and researchers are using metatranscriptomic and metaproteomic environmental biomarkers to study the factors influencing these communities. By analyzing proteomes and transcriptomes of the cyanobacterium Trichodesmium grown under different nutrient limitations and CO2 concentrations, the study found strong correlations between stress-induced proteins and RNAs, providing valuable insights into the nutrient status under different CO2 conditions. However, there were broader discrepancies in the correlations of transcriptional and translational pathways related to central metabolism. The findings also showed how environmental biomarkers exhibit coherence across multiple omics levels, supporting the potential for studying global responses to environmental stimuli in the ocean.