ALBERT

Description: Zinc is an essential trace metal for oceanic primary producers with the highest concentrations in polar oceans. However, its role in the biological functioning and adaptive evolution of polar phytoplankton remains enigmatic. Here, we have applied a combination of evolutionary genomics, quantitative proteomics, co-expression analyses and cellular physiology to suggest that model polar phytoplankton species have a higher demand for zinc because of elevated cellular levels of zinc-binding proteins. We propose that adaptive expansion of regulatory zinc-finger protein families, co-expanded and co-expressed zinc-binding proteins families involved in photosynthesis and growth in these microalgal species and their natural communities were identified to be responsible for the higher zinc demand. The expression of their encoding genes in eukaryotic phytoplankton metatranscriptomes from pole-to-pole was identified to correlate not only with dissolved zinc concentrations in the upper ocean but also with temperature, suggesting that environmental conditions of polar oceans are responsible for an increased demand of zinc. These results suggest that zinc plays an important role in supporting photosynthetic growth in eukaryotic polar phytoplankton and that this has been critical for algal colonization of low-temperature polar oceans.

Description: Microbial rhodopsins are photoreceptor proteins that convert light into biological signals or energy. Proteins of the xanthorhodopsin family are common in eukaryotic photosynthetic plankton including diatoms. However, their biological role in these organisms remains elusive. Here we report on a xanthorhodopsin variant (FcR1) isolated from the polar diatom Fragilariopsis cylindrus. Applying a combination of biophysical, biochemical and reverse genetics approaches, we demonstrate that FcR1 is a plastid-localized proton pump which binds the chromophore retinal and is activated by green light. Enhanced growth of a Thalassiora pseudonana gain-of-function mutant expressing FcR1 under iron limitation shows that the xanthorhodopsin proton pump supports growth when chlorophyll-based photosynthesis is iron-limited. The abundance of xanthorhodopsin transcripts in natural diatom communities of the surface oceans is anticorrelated with the availability of dissolved iron. Thus, we propose that these proton pumps convey a fitness advantage in regions where phytoplankton growth is limited by the availability of dissolved iron.

Description: Marine phytoplankton are responsible for ~50% of the CO2 that is fixed annually, worldwide, and contribute massively to other biogeochemical cycles in the oceans1. Their contribution depends significantly on the interplay between dynamic environmental conditions and metabolic responses that underpin resource allocation and hence biogeochemical cycling in the oceans. However, these complex environment-biome interactions have not been studied on a larger scale. Here we use a novel set of integrative approaches that combine metatranscriptomes, biochemical data, cellular physiology and emergent phytoplankton growth strategies in a global ecosystems model, to show that temperature significantly affects eukaryotic phytoplankton metabolism with consequences for biogeochemical cycling under global warming. In particular, the rate of protein synthesis strongly increases under high temperatures even though the numbers of ribosomes and their associated rRNAs decreases. Thus, at higher temperatures, eukaryotic phytoplankton seem to require a lower density of ribosomes to produce the required amounts of cellular protein. The reduction of P-rich ribosomes2 in warmer oceans will tend to produce higher organismal N:P ratios, in turn increasing demand for N with consequences for the marine carbon cycle due to shifts toward N-limitation. Our integrative approach suggests that temperature plays a previously unrecognized, critical role in resource allocation and marine phytoplankton stoichiometry with implications for the biogeochemical cycles that they drive.