Why Environmental Biomarkers Work: Transcriptome-Proteome Correlations and Modeling of Multi-Stressor 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 through the use of metatranscriptomic and metaproteomic environmental biomarkers, despite ongoing uncertainty about the coherence between RNA and protein signals. Using published proteomes and transcriptomes from the abundant colony-forming cyanobacterium Trichodesmium (strain T. erythraeum IMS101) grown under varying Fe and/or P limitation and/or co-limitation in low and high CO2, we observed robust correlations of stress induced proteins and RNAs (i.e., those involved in transport and homeostasis) that can yield useful information on 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, can achieve large increases in fold-change units, as opposed to those with higher basal expression and inventory such as metabolic systems. Microbial cells, due to their close proximity to the environment, tend to show large adaptive responses to environmental stimuli in both RNA and protein that result in transcript-protein correlations. These observations and model results demonstrate a multi-omic coherence for environmental biomarkers and provide the underlying mechanism for those observations, supporting the promise for global application in detecting responses to environmental stimuli in a changing ocean.