A novel mechanism explaining the temperature dependence of marine unicellular nitrogen-fixing cyanobacteria

Abstract

The major marine nitrogen-fixing cyanobacterium, Crocosphaera watsonii, is restricted to warm tropical and subtropical oceans, while the underlying mechanisms remain unclear. C. watsonii fixes nitrogen (oxygen-sensitive) and carbon (oxygen-evolving) during night and day, respectively. By diel analyses of physiological rates and transcriptome at its optimal (28 degrees C) and a lower temperature (23 degrees C), we found that the low temperature delayed the enhancement of respiration (oxygen-consuming) and the onset of nitrogen fixation during nighttime. Transcription of the master regulator of circadian gene expression, circadian genes, and major metabolic pathways (e.g., respiration, nitrogen fixation, and photosynthesis) was delayed at the low temperature, suggesting that low temperature might decouple intracellular and environmental diurnal cycles and cause resource limitation and reduced growth. We propose that temperature might mediate the circadian clock, thereby regulating diurnal rhythm of nitrogen and carbon fixation, explaining the temperature dependence (particularly the lower thermal limit) and biogeography of C. watsonii.