Proteomic responses to ocean acidification of the marine diazotroph Trichodesmium under iron-replete and iron-limited conditions

Growth and dinitrogen (N2) fixation of the globally important diazotrophic cyanobacteria Trichodesmium are often limited by iron (Fe) availability in surface seawaters. To systematically examine the combined effects of Fe limitation and ocean acidification (OA), T. erythraeum strain IMS101 was acclimated to both Fe-replete and Fe-limited concentrations under ambient and acidified conditions. Proteomic analysis showed that OA affected a wider range of proteins under Fe-limited conditions compared to Fe-replete conditions. OA also led to an intensification of Fe deficiency in key cellular processes (e.g., photosystem I and chlorophyll a synthesis) in already Fe-limited T. erythraeum. This is a result of reallocating Fe from these processes to Fe-rich nitrogenase to compensate for the suppressed N2 fixation. To alleviate the Fe shortage, the diazotroph adopts a series of Fe-based economic strategies (e.g., upregulating Fe acquisition systems for organically complexed Fe and particulate Fe, replacing ferredoxin by flavodoxin, and using alternative electron flow pathways to produce ATP). This was more pronounced under Fe-limited-OA conditions than under Fe limitation only. Consequently, OA resulted in a further decrease of N2- and carbon-fixation rates in Fe-limited T. erythraeum. In contrast, Fe-replete T. erythraeum induced photosystem I (PSI) expression to potentially enhance the PSI cyclic flow for ATP production to meet the higher demand for energy to cope with the stress caused by OA. Our study provides mechanistic insight into the holistic response of the globally important N2-fixing marine cyanobacteria Trichodesmium to acidified and Fe-limited conditions of future oceans.