Simultaneous acclimation to nitrogen and iron scarcity in open ocean cyanobacteria revealed by sparse tensor decomposition of metatranscriptomes

Microbes respond to changes in their environment by adapting their physiology through coordinated adjustments to the expression levels of functionally related genes. To detect these shifts in situ, we developed a sparse tensor decomposition method that derives gene co-expression patterns from inherently complex whole community RNA-sequencing data. Application of the method to metatranscriptomes of the abundant marine cyanobacteria Prochlorococcus and Synechococcus identified responses to scarcity of two essential nutrients, nitrogen and iron, including increased transporter expression, restructured photosynthesis and carbon metabolism, and mitigation of oxidative stress. Further, expression profiles of the identified gene clusters suggest that both cyanobacteria populations experience simultaneous nitrogen and iron stresses in a transition zone between North Pacific oceanic gyres. The results demonstrate the power of our approach to infer organism responses to environmental pressures, hypothesize functions of uncharacterized genes, and extrapolate ramifications for biogeochemical cycles in a changing ecosystem.