Zinc and the productivity and biodiversity of polar oceans

It is well known that zinc is an essential trace metal for almost all life on Earth. Our research has revealed that marine phytoplankton have evolved to exploit the abundance of zinc in surface polar oceans to thrive under low temperatures and the strong seasonality in solar irradiance.

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Despite the harsh polar environment, microalgae thrive and play a fundamental role in supporting complex and productive polar ecosystems. Their success is rooted in the unifying concept of adaptive evolution. To extend the list of polar species for which genomic resources are available, Naihao Ye, Wentao Han, and Xiaowen Zhang from the Yellow Sea Fisheries Research Institute in Qingdao (China) isolated the green alga Microglena sp. YARC from the Southern Ocean and sequenced its genome to reveal further insights into what drives the adaptation of microalgae to the polar environment. At approximately the same time, an international group of researchers led by myself together with close colleagues such as Cock van Oosterhout and Igor V. Grigoriev published the genome of the Antarctic diatom Fragilariopsis cylindrus [1]. Naihao and Xiaowen got in touch and shared their preliminary results with us. After comparing these two polar algal genomes, we found something interesting: gene families with zinc-binding domains (e.g., zinc fingers) expanded in both algal genomes. These results were soon confirmed by polar dinoflagellate genomes, which were published only a little later [2]. As all of these new genome data from polar microalgae converged on the idea that zinc plays an important role in the adaptive evolution of microalgae to the harsh polar environment, the foundation was laid for this paper [3]. Over subsequent years, we have built on it by extending the genome data with meta-omics data from pole to pole [4, 5], biochemical, and physiological studies using Microglena sp. YARC as our model system. 

However, when it comes to ocean sciences, research on essential trace metals is dominated by literature on iron. Dissolved iron limits oceanic primary productivity in approximately 30-40% of the global surface ocean including the Southern Ocean surrounding the Antarctic continent [6]. Although different species from diverse phytoplankton groups have adapted to iron scarcity, none of these adaptations appear to be polar specific. Adaptation to zinc, however, shows a different trend – this adaptation is polar specific across phytoplankton species from different lineages. Remarkably, however, species have evolved to exploit the abundance of zinc in surface polar oceans, especially in the Southern Ocean. We found that these elevated zinc concentrations are matched by a higher demand for this trace metal in diverse polar microalgae including diatoms, green algae and dinoflagellates but not their non-polar counterparts.

This elevated zinc demand appears to be required to regulate photosynthetic processes in algae under polar growth conditions because we did not find expanded zinc-binding protein families in polar heterotrophic organisms such as bacteria and fish. The polar environment is characterised by overall low temperatures in combination with strong seasonality in solar irradiance. Many different zinc-binding protein families such as regulatory zinc-finger families (e.g., zf-MYND) and some key proteins families involved in photosynthesis have expanded in F. cylindrus and Microglena sp. YARC. Both algal species show gene family expansions that appear to have evolved shortly after the formation of the Southern Ocean. Altogether, this suggests that the expanded zinc-binding protein families helped these algae to thrive under polar growth conditions, which therefore enabled them to successfully conquer polar oceans, making them to some of the most productive ecosystems on Earth. 

The Antarctic green alga Microglena sp. YARC under an optical microscope (Left) and a transmission electron microscope (Right).

Yet, we still don’t know how these regulatory zinc-finger proteins and other zinc-binding proteins contribute to sustaining photosynthesis in polar oceans. Their biochemistry is complex because some of the zinc-finger proteins appear to bind to DNA and RNA, whereas others contribute to protein-protein interactions. Hence, our study is only providing the first clue to their biological role in the context of regulating photosynthesis, including the acquisition of dissolved inorganic carbon such as CO2 and HCO3.  Thus, we hope that our paper will generate interest in revealing the biological functions of these regulatory zinc-binding proteins in microalgae. Those insights might help to link the adaptive evolution of key organism groups to environmental conditions (e.g., low temperatures, strong seasonality) with the cycling of essential trace elements in the oceans. In the case of zinc in polar oceans at least, not its scarcity drove adaptive processes but its abundance. And the latter might therefore be responsible for much of the biodiversity in polar oceans including crustaceans (e.g. krill), fish, and whales because polar phytoplankton form the base of the productive and diverse polar food web. 

References:

[1] https://www.nature.com/articles/nature20803

[2] https://bmcbiol.biomedcentral.com/articles/10.1186/s12915-020-00782-8

[3] https://www.nature.com/articles/s41559-022-01750-x

[4] https://www.nature.com/articles/s41467-021-25646-9

[5] https://microbiomejournal.biomedcentral.com/articles/10.1186/s40168-022-01254-7

[6] https://agupubs.onlinelibrary.wiley.com/doi/full/10.1029/2004JC002601    

    

 

Thomas Mock

Professor, University of East Anglia

Marine Microbiology, Evolution, Adaptation, Algae, Phytoplankton, Reverse Genetics, Genomics