TY - JOUR
T1 - The role of zinc in the adaptive evolution of polar phytoplankton
AU - Ye, Naihao
AU - Han, Wentao
AU - Toseland, Andrew
AU - Wang, Yitao
AU - Fan, Xiao
AU - Xu, Dong
AU - van Oosterhout, Cock
AU - Sea of Change Consortium
AU - Aslam, Shazia N.
AU - Barry, Kerrie
AU - Beszteri, Bank
AU - Brussaard, Corina
AU - Clum, Alicia
AU - Copeland, Alex
AU - Daum, Chris
AU - Duncan, Anthony
AU - Eloe-Fadrosh, Emiley
AU - Fong, Allison
AU - Foster, Brian
AU - Foster, Bryce
AU - Ginzburg, Michael
AU - Huntemann, Marcel
AU - Ivanova, Natalia N.
AU - Kyrpides, Nikos C.
AU - Martin, Kara
AU - Moulton, Vincent
AU - Mukherjee, Supratim
AU - Palaniappan, Krishnaveni
AU - Reddy, T. B. K.
AU - Roux, Simon
AU - Schmidt, Katrin
AU - Strauss, Jan
AU - Timmermans, Klaas
AU - Tringe, Susannah G.
AU - Underwood, Graham J. C.
AU - Valentin, Klaus U.
AU - Van De Poll, Willem H.
AU - Varghese, Neha
AU - Grigoriev, Igor V.
AU - Tagliabue, Alessandro
AU - Zhang, Jian
AU - Zhang, Yan
AU - Ma, Jian
AU - Qiu, Huan
AU - Li, Youxun
AU - Zhang, Xiaowen
AU - Mock, Thomas
N1 - 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.
PY - 2022/7
Y1 - 2022/7
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85131400092&partnerID=8YFLogxK
U2 - 10.1038/s41559-022-01750-x
DO - 10.1038/s41559-022-01750-x
M3 - Article
VL - 6
SP - 965
EP - 978
JO - Nature Ecology & Evolution
JF - Nature Ecology & Evolution
SN - 2397-334X
IS - 7
ER -