Evolutionary interactions between ocean acidification and iron/phosphorus co-limitation in the marine nitrogen-fixing cyanobacterium Trichodesmium

Chair: Alistair Hobday

David A. Hutchins (1)*, Feixue Fu (1), Eric A. Webb (1), Mak A. Saito (2), Dawn Moran (2), Matthew R. McIlvin (2), Michael D. Lee (1), Nathan G. Walworth (1)

1 Marine and Environmental Biology, Department of Biological Sciences, University of Southern California, Los Angeles, California, 90089, USA.
2 Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA

Long-term adaptive responses of marine primary producers to ocean acidification will be modulated by interactions with other environmental variables that are simultaneously changing in the anthropogenically-perturbed ocean, such as nutrient limitation. Iron (Fe) and phosphorus (P) are known to sometimes be individually limiting to marine nitrogen-fixers such as the keystone nitrogen-fixing cyanobacterium Trichodesmium, but the most relevant and biogeochemically-significant situation may be simultaneous co-limitation by both Fe and P. Both Fe and P are also likely to be even scarcer in the future acidified oligotrophic ocean, due to projected intensification of surface stratification. However, we currently lack the ability to predict the evolutionary responses of Trichodesmium to the combination of rising ocean acidification and increased Fe/P co-limitation stress.

We examined interactive adaptation to high CO2 and nutrient (co)-limitation using experimental evolution cultures of Trichodesmium selected for ~7 years under both present day (380 uatm) and elevated (750 uatm) CO2. These high and low CO2-adapted cultures were then selected for a further ~1 year under Fe-limitation, P-limitation, or Fe/P co-limitation. We evaluated adaptive changes under these multiple factor selection regimes using physiological measurements coupled with proteomics.

Physiological, morphological and proteomic results all demonstrate the existence of complex feedbacks between adaptation to ocean acidification and multiple nutrient limitation. Fe/P co-limited cell lines have increased growth rates and reduced cell sizes relative to cell lines limited by either Fe or P alone, while the global Trichodesmium proteome exhibits three distinctive sets of responses to Fe-limited, P-limited, and Fe/P co-limited growth, with large, treatment-specific shifts in protein abundance under all three conditions as a function of adaptation to high CO2. This restructured high CO2, Fe/P co-limited proteome includes fundamental changes in the abundance of many proteins involved in cellular core metabolism, photosynthesis, cell size regulation, and growth.

The results of our long-term evolutionary study suggest that diazotrophs such as Trichodesmium already possess a set of unique, adaptive biochemical and morphological strategies that may allow them to optimize their fitness under expected conditions of widespread multiple nutrient stress in the future high CO2 ocean.