Collaborative Research: Evolutionary, biochemical and biogeochemical responses of marine cyanobacteria to warming and iron limitation interactions

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The oceans absorb much of the heat generated by human activities, and this warming of the surface ocean has consequences for important groups of marine organisms. Marine cyanobacteria are one such key group of organisms, since they supply much of the essential carbon and nitrogen that supports nearly all the rest of the marine food web. Currently, the growth of cyanobacteria is mostly constrained by scarce supplies of the micronutrient element iron, but they are also very sensitive to the ongoing increases in seawater temperature. Preliminary results suggest that warming could partly mitigate the negative effects of iron limitation on marine cyanobacteria. This project examines in depth how these interactions between warming and iron limitation will affect the future ocean carbon and nitrogen cycles, using laboratory culture experiments showing how cyanobacteria respond to simultaneously changing temperature and iron supplies. Both short-term response studies and long-term evolutionary experiments testing for adaptation use a comprehensive set of molecular biology tools targeting genes to proteins. The final goal is to apply the results of these experiments to improve quantitative models predicting how the ocean's carbon and nitrogen cycles, biological productivity, and living resources will respond to a warming future climate. Two graduate students, a postdoc and 3-4 underrepresented undergraduate researchers are supported, and the investigators also mentor summer science interns from largely Hispanic local high schools. The physiology, biochemistry and biogeography of nitrogen-fixing cyanobacteria and unicellular picocyanobacteria are strongly influenced by temperature, subjecting them to intense selective pressure as the modern ocean steadily warms up. These groups have likewise been rigorously selected under chronic iron (Fe) scarcity, and the availability of this crucial micronutrient is also changing with a shifting climate. This project examines short-term acclimation and long-term evolutionary responses of Fe-stressed marine cyanobacteria to a warmer environment. Preliminary data show that Iron Use Efficiencies (IUE, mols N fixed.hr-1 mol cellular Fe-1) of Fe-limited Trichodesmium increase 4 to 5-fold with a 5oC temperature increase, allowing the cells to much more efficiently leverage scarce available Fe supplies to grow and fix nitrogen. This means that warming can to a large degree mitigate the negative effects of Fe limitation on Trichodesmium, resulting in a modelled 22% increase in global nitrogen fixation by 2100 in a warmer climate. This project aims to uncover the cellular biochemical mechanisms involved in this Fe-limitation/thermal IUE effect in a four-year experimental evolution study of the diazotrophs Trichodesmium and Crocosphaera and the picocyanobacteria Synechococcus and Prochlorococcus, under a multi-variate selection matrix of temperature and Fe availability. The objectives are to 1) Assess the long-term adaptive responses of fitness, IUE and physiology to Fe limitation and warming interactions in these four major cyanobacterial groups; 2) Determine the molecular and biochemical mechanisms behind the surprising Fe/warming interactive effect on IUE using genomics, transcriptomics and quantitative proteomics coupled with 'metalloproteomics' determinations of Fe content in critical proteins; 3) Compare and contrast acclimation and adaptation responses to Fe limitation and warming in key cyanobacteria taxa, and 4) Integrate results using a published biogeochemical modeling approach to assess global consequences for marine productivity and nitrogen fixation. This project offers a mechanistic and predictive understanding of adaptation to Fe and warming co-stressors in a rapidly changing future ocean environment for some of the most important photoautotrophic functional groups in the ocean.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.