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The role of zinc in the adaptive evolution of polar phytoplankton

Nature Ecology & Evolution volume 6, pages 965–978 (2022)Cite this article

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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.

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Fig. 1: The expansion and expression of transposable elements in Microglena sp.
Fig. 2: Expansion and evolution of zinc-finger proteins in polar microalgae.
Fig. 3: Comparison of protein copy numbers, cellular zinc concentrations and cell sizes between polar and non-polar green microalgae.
Fig. 4: The co-expression of zinc-finger genes and the expansion and expression of photosynthesis genes in Microglena sp.
Fig. 5: Zinc-dependent growth rates and photophysiology of polar versus non-polar green algal species.
Fig. 6: Eukaryotic phytoplankton metatranscriptomes and genomes with focus on zinc-binding domain-containing genes and their substitution rates (dN/dS) in relation to latitude and the estimated concentration of dissolved zinc in the surface ocean.

Data availability

The Microglena sp. genome assembly data were deposited in NCBI GenBank (under BioProject accession PRJNA787402 and genome accession JAJSRW000000000). All raw transcriptome sequencing data of Microglena sp. were deposited into the Sequence Read Archive (under BioProject accession PRJNA814737). The mass spectrometry proteomics data of Microglena sp. and C. reinhardtii have been deposited to the ProteomeXchange Consortium (http://proteomecentral.proteomexchange.org) via the iProX partner repository with the dataset identifier PXD032702. Source data are provided with this paper.

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Acknowledgements

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.

Author information

Author notes

  1. These authors contributed equally: Naihao Ye, Wentao Han.

Authors and Affiliations

  1. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, China

    Naihao Ye, Wentao Han, Yitao Wang, Xiao Fan, Dong Xu, Jian Zhang, Yan Zhang, Jian Ma & Xiaowen Zhang

  2. Function Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China

    Naihao Ye & Xiaowen Zhang

  3. School of Environmental Sciences, University of East Anglia, Norwich, UK

    Andrew Toseland, Cock van Oosterhout & Thomas Mock

  4. DOE Joint Genome Institute, Berkeley, CA, USA

    Igor V. Grigoriev

  5. Department of Plant and Molecular Biology, University of California Berkeley, Berkeley, CA, USA

    Igor V. Grigoriev

  6. School of Environmental Sciences, University of Liverpool, Liverpool, UK

    Alessandro Tagliabue

  7. US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    Kerrie Barry, Alicia Clum, Alex Copeland, Chris Daum, Emiley Eloe-Fadrosh, Brian Foster, Bryce Foster, Marcel Huntemann, Natalia N. Ivanova, Nikos C. Kyrpides, Supratim Mukherjee, Krishnaveni Palaniappan, T. B. K. Reddy, Simon Roux, Susannah G. Tringe, Neha Varghese & Huan Qiu

  8. Marine Science Research Institute of Shandong Province, Qingdao, China

    Youxun Li

  9. Department of Chemistry, Norwegian University of Science and Technology, Trondheim, Norway

    Shazia N. Aslam

  10. Department of Biology, University of Duisburg-Essen, Essen, Germany

    Bank Beszteri

  11. Royal Netherlands Institute for Sea Research, Texel, the Netherlands

    Corina Brussaard, Kara Martin & Klaas Timmermans

  12. School of Computing Sciences, University of East Anglia, Norwich, UK

    Anthony Duncan & Vincent Moulton

  13. Alfred-Wegener Institute for Polar and Marine Research, Bremerhaven, Germany

    Allison Fong, Michael Ginzburg & Klaus U. Valentin

  14. Earlham Institute, Norwich, United Kingdom

    Kara Martin

  15. School of Environmental Sciences, University of East Anglia, Norwich, UK

    Katrin Schmidt

  16. Ocean EcoSystems Biology Unit, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany

    Jan Strauss

  17. School of Life Sciences, University of Essex, Colchester, UK

    Graham J. C. Underwood

  18. Department of Ocean Ecosystems, Energy and Sustainability Research Institute Groningen, University of Groningen, Groningen, the Netherlands

    Willem H. van de Poll

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  1. Naihao Ye
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Consortia

Sea of Change Consortium

  • Shazia N. Aslam
  • , Kerrie Barry
  • , Bank Beszteri
  • , Corina Brussaard
  • , Alicia Clum
  • , Alex Copeland
  • , Chris Daum
  • , Anthony Duncan
  • , Emiley Eloe-Fadrosh
  • , Allison Fong
  • , Brian Foster
  • , Bryce Foster
  • , Michael Ginzburg
  • , Marcel Huntemann
  • , Natalia N. Ivanova
  • , Nikos C. Kyrpides
  • , Kara Martin
  • , Vincent Moulton
  • , Supratim Mukherjee
  • , Krishnaveni Palaniappan
  • , T. B. K. Reddy
  • , Simon Roux
  • , Katrin Schmidt
  • , Jan Strauss
  • , Klaas Timmermans
  • , Susannah G. Tringe
  • , Graham J. C. Underwood
  • , Klaus U. Valentin
  • , Willem H. van de Poll
  •  & Neha Varghese

Contributions

N.Y., T.M. and X.Z. designed the study. X.Z., W.H., T.M., C.v.O., X.F., N.Y., A.T. and H.Q. analysed the data. Y.W., D.X., J.Z., Y.Z., J.M. and Y.L. conducted the laboratory experiments. Sea of Change Consortium collected the samples and did DNA and RNA extractions. The consortium also contributed to sequence data analysis. I.V.G. coordinated the project at JGI. T.M., X.Z., N.Y., A.T. and C.v.O. cowrote the manuscript.

Corresponding authors

Correspondence to Naihao Ye, Xiaowen Zhang or Thomas Mock.

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Nature Ecology & Evolution thanks Cheong Xin Chan and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Morphology and phylogenetic relationship of Microglena sp. YARC.

a, b, Optical microscope (a) and transmission electron microscopy (b) of Microglena sp. YARC. c, A maximum likelihood tree of green algae based on the five chloroplast protein-coding genes (atpB, psaA, psaB, psbC and rbcL) using maximum likelihood method. The tree with branches showing bootstrap support > 50.

Extended Data Fig. 2 Genome characters of Microglena sp. YARC.

a, Estimation of the genome size by flow cytometry. The maize diploid cells (genome size 2.3 Gb) were used as reference. The relative fluorescence values of maize diploid cells were 55.15 ± 2.43, and the relative fluorescence value of Microglena haploid cells were 15.11 ± 0.73. Based on the ratio of fluorescence values, the genome size of Microglena was estimated to be about 1.26 ± 0.02 Gb. b, K-mer estimation of the genome size of Microglena sp. YARC. c, Cytogenetic studies showed that Microglena sp. YARC has n = 6 chromosomes. d, The Hi-C assisted assembly of Microglena sp. pseudomolecules. Heatmap showing Hi-C interactions under the resolution of 200 kb, and the antidiagonal pattern for the intrachromosomal interactions may reflect the Rabl configuration of chromatins. e,f, Ks (e) and 4dtv (f) distribution of the whole Microglena sp. genome.

Extended Data Fig. 3 Comparison of total zinc-finger domains in bacteria and fish genomes.

a, Total zinc-finger domains comparison between psychrophillic (blue) and mesophilic bacteria (tawny). b, Zinc-finger comparison between two Antarctic fishes and four Mesophilic fishes. Statics analysis of two-sided Duncan’s test showed no significant difference between each species. For all boxplots, box bounds represent the first and third quartiles and whiskers 1.5× the interquartile range; the centre line represents the median.

Extended Data Fig. 4

Phylogenetic and expansion analysis of carbonic anhydrase encoding genes in green algae and diatoms.

Extended Data Fig. 5 Expansion of light-harvesting proteins in Microglena sp. YARC.

a, Expansion of chlorophyll A-B binding protein domains as a function of total annotated domains for green algal, diatom and dinoflagellate genomes. Solid for polar algae and hollow for non-polar algae. b, Unrooted genealogy of LHC genes in Microglena (Red), Chlamydomonas reinhardtii (blue), Chlamydomonas eustigma (green), Volvox carteri (yellow) and Gonium pectorale (purple).

Extended Data Fig. 6 Upper 100 m annually averaged dissolved zinc (nmol L-1) from the PISCES model with observations taken within the upper 100 m overlain as coloured circles.

Sampling locations for this study are indicated with red crosses.

Supplementary information

Supplementary Information

Supplementary Methods and Tables 1–7.

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Supplementary Data

Supplementary Data 1, PFAM and Interproscan annotation of zinc-finger-containing LTRs; 2, Protein copy number of Microglena sp. YARC; 3, Protein copy number of Chlamydomonas reinhardtii; 4, Copy number of zinc-binding proteins of Microglena sp. YARC; 5, Copy number of zinc-binding proteins of Chlamydomonas reinhardtii; 6 Co-expression gene pairs of Microglena sp. YARC.

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Ye, N., Han, W., Toseland, A. et al. The role of zinc in the adaptive evolution of polar phytoplankton. Nat Ecol Evol 6, 965–978 (2022). https://doi.org/10.1038/s41559-022-01750-x

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