The role of zinc in the adaptive evolution of polar phytoplankton

Ye, Naihao, Han, Wentao, Toseland, Andrew, Wang, Yitao, Fan, Xiao, Xu, Dong, van Oosterhout, Cock ORCID: https://orcid.org/0000-0002-5653-738X, Grigoriev, Igor V., Tagliabue, Alessandro, Zhang, Jian, Zhang, Yan, Ma, Jian, Qiu, Huan, Li, Youxun, Zhang, Xiaowen and Mock, Thomas ORCID: https://orcid.org/0000-0001-9604-0362 and Sea of Change Consortium (2022) The role of zinc in the adaptive evolution of polar phytoplankton. Nature Ecology & Evolution, 6 (7). pp. 965-978. ISSN 2397-334X

[thumbnail of Figure5]
Preview
PDF (Figure5) - Accepted Version
Download (236kB) | Preview
[thumbnail of Figure1]
Preview
PDF (Figure1) - Accepted Version
Download (4MB) | Preview
[thumbnail of Figure3]
Preview
PDF (Figure3) - Accepted Version
Download (327kB) | Preview
[thumbnail of Ye_for_re_resubmission_NATECOLEVOL-210212798_NO_tracked_changes_180322]
Preview
PDF (Ye_for_re_resubmission_NATECOLEVOL-210212798_NO_tracked_changes_180322) - Accepted Version
Download (395kB) | Preview
[thumbnail of Figure2]
Preview
PDF (Figure2) - Accepted Version
Download (612kB) | Preview
[thumbnail of Figure6]
Preview
PDF (Figure6) - Accepted Version
Download (1MB) | Preview
[thumbnail of Figure4]
Preview
PDF (Figure4) - Accepted Version
Download (3MB) | Preview

Abstract

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.

Item Type: Article
Additional Information: Funding Information: This work was supported by the national key research and development programme of China (2018YFD0900305), the Marine S&T Fund of Shandong Province for the Pilot National Laboratory for Marine Science and Technology (Qingdao) (2021QNLM050103-1), National Natural Science Foundation of China (41676145, 32000404), Central Public-interest Scientific Institution Basal Research Fund, YSFRI, CAFS (20603022020019, 20603022021019), China Agriculture Research System (CARS-50), Taishan Scholars Funding of Shandong Province, Young Taishan Scholars Program (tsqn202103136). The metatranscriptome sequencing was conducted by the US Department of Energy (DOE)–Joint Genome Institute, a DOE Office of Science User Facility, which is supported by the Office of Science of the DOE under contract no. DE-AC02-05CH1123. A.T. was supported by the European Research Council under the European Union’s Horizon 2020 research and innovation programme (grant no. 724289). T.M. acknowledges funding from the US DOE–Joint Genome Institute (grant no. 532, Community Science Program) and the Natural Environment Research Council (grant nos. NE/K004530/1 and NE/R000883/1). T.M. and C.v.O. acknowledge partial funding from the School of Environmental Sciences at the University of East Anglia, Norwich Research Park, United Kingdom.
Uncontrolled Keywords: ecology, evolution, behavior and systematics,ecology ,/dk/atira/pure/subjectarea/asjc/1100/1105
Faculty \ School: Faculty of Science > School of Environmental Sciences
Faculty of Science > School of Computing Sciences
Faculty of Science
University of East Anglia Research Groups/Centres > Theme - ClimateUEA
UEA Research Groups: Faculty of Science > Research Centres > Centre for Ecology, Evolution and Conservation
Faculty of Science > Research Groups > Norwich Epidemiology Centre
Faculty of Medicine and Health Sciences > Research Groups > Norwich Epidemiology Centre
Faculty of Science > Research Groups > Computational Biology
Faculty of Science > Research Groups > Centre for Ocean and Atmospheric Sciences
Faculty of Science > Research Groups > Environmental Biology
Related URLs:
Depositing User: LivePure Connector
Date Deposited: 18 Nov 2022 16:30
Last Modified: 07 Oct 2023 01:16
URI: https://ueaeprints.uea.ac.uk/id/eprint/89938
DOI: 10.1038/s41559-022-01750-x

Actions (login required)

View Item View Item