Strain-specific metabarcoding reveals rapid evolution of copper tolerance in populations of the coastal diatom Skeletonema marinoi

Björn Andersson, Olof Berglund, Helena L. Filipsson, Olga Kourtchenko, Anna Godhe, Kerstin Johannesson, Mats Töpel, Matthew I.M. Pinder, Lara Hoepfner, Karin Rengefors

Research output: Contribution to journalArticlepeer-review

Abstract

Phytoplankton have short generation times, flexible reproduction strategies, large population sizes and high standing genetic diversity, traits that should facilitate rapid evolution under directional selection. We quantified local adaptation of copper tolerance in a population of the diatom Skeletonema marinoi from a mining-exposed inlet in the Baltic Sea and in a non-exposed population 100 km away. We hypothesized that mining pollution has driven evolution of elevated copper tolerance in the impacted population of S. marinoi. Assays of 58 strains originating from sediment resting stages revealed no difference in the average tolerance to copper between the two populations. However, variation within populations was greater at the mining site, with three strains displaying hyper-tolerant phenotypes. In an artificial evolution experiment, we used a novel intraspecific metabarcoding locus to track selection and quantify fitness of all 58 strains during co-cultivation in one control and one toxic copper treatment. As expected, the hyper-tolerant strains enabled rapid evolution of copper tolerance in the mining-exposed population through selection on available strain diversity. Within 42 days, in each experimental replicate a single strain dominated (30%–99% abundance) but different strains dominated the different treatments. The reference population developed tolerance beyond expectations primarily due to slowly developing plastic response in one strain, suggesting that different modes of copper tolerance are present in the two populations. Our findings provide novel empirical evidence that standing genetic diversity of phytoplankton resting stage allows populations to evolve rapidly (20–50 generations) and flexibly on timescales relevant for seasonal bloom progressions.

Original languageEnglish
JournalMolecular Ecology
Early online date2023 Sept 11
DOIs
Publication statusE-pub ahead of print - 2023 Sept 11

Bibliographical note

Funding Information:
The Captain and the crew of r/v Electra af Askö and Johan Burman, and Kotaro Hirose for sediment sampling assistance. Jakob Walve for facilitating water collection at Askö B1 station. The project was funded by the Swedish Research Council FORMAS grant number 2016‐00594 and the Oscar and Lili Lamm Foundation grant number FO2018‐0042. The authors acknowledge support from the National Genomics Infrastructure in Stockholm funded by Science for Life Laboratory, the Knut and Alice Wallenberg Foundation and the Swedish Research Council, and SNIC/Uppsala Multidisciplinary Center for Advanced Computational Science for assistance with massively parallel sequencing and access to the UPPMAX computational infrastructure.

Publisher Copyright:
© 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

Subject classification (UKÄ)

  • Biochemistry and Molecular Biology
  • Environmental Sciences

Free keywords

  • adaptation
  • copper tolerance
  • diatoms
  • phytoplankton
  • strain metabarcoding
  • strain-selection

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