Genome-Wide Adaptation to a Complex Environmental Gradient in a Keystone Phytoplankton Species

  • Eveline Pinseel
  • , Elizabeth C Ruck
  • , Teofil Nakov
  • , Per R Jonsson
  • , Olga Kourtchenko
  • , Anke Kremp
  • , Matthew I M Pinder
  • , Wade R Roberts
  • , Conny Sjöqvist
  • , Mats Töpel
  • , Anna Godhe
  • , Matthew W Hahn
  • , Andrew J Alverson

Research output: Contribution to journalArticleScientificpeer-review

3 Citations (Scopus)
31 Downloads (Pure)

Abstract

Marine phytoplankton play essential roles in global primary production and biogeochemical cycles. Yet, the evolutionary genetic underpinnings of phytoplankton adaptation to complex marine and coastal environments, where many environmental variables fluctuate and interact, remain unclear. We combined population genomics with experimental transcriptomics to investigate the genomic basis underlying a natural evolutionary experiment that has played out over the past 8000 years in one of the world's largest brackish water bodies: the colonisation of the Baltic Sea by the ancestrally marine diatom Skeletonema marinoi. To this end, we combined target capture of the entire nuclear genome with pooled shotgun sequencing, and showed that the method performs well on both cultures and single cells. Genotype-environment association analyses identified > 1000 genes with signals of selection in response to major environmental gradients in the Baltic Sea, which apart from salinity, include marked differences in temperature and nutrient supply. Locally adapted genes were related to diverse metabolic processes, including signal transduction, cell cycle, DNA methylation and maintenance of homeostasis. The locally adapted genes showed significant overlap with salinity-responsive genes identified in a laboratory common garden experiment, suggesting the Baltic salinity gradient contributes to local adaptation of S. marinoi. Taken together, our data show that local adaptation of phytoplankton to complex coastal environments, which are characterised by a multitude of environmental gradients, is driven by widespread changes in diverse metabolic pathways and functions.

Original languageEnglish
Article numbere17817
Pages (from-to)e17817
JournalMolecular Ecology
Volume34
Issue number13
DOIs
Publication statusPublished - 10 Jun 2025
MoE publication typeA1 Journal article-refereed

Funding

This work was supported by grants from the Simons Foundation (403249 to A.J.A. and 725407 to E.P.), grants from the National Science Foundation (1651087 to A.J.A. and DBI\u20102146866 to M.W.H.), and a grant from the Science Foundation Flanders, FWO (1221323N to E.P.). This research used resources available through the Arkansas High Performance Computing Center, which is funded through multiple NSF grants and the Arkansas Economic Development Commission. We thank Geoffrey House for help with the sampling design, and we are grateful to Sirje Sildever (Tallinn University of Technology, Estonia), Bj\u00F6rn Andersson (University of Gothenburg, Sweden), Andrzej Witkowski (University of Szczecin, Poland), J\u00F6rg Dutz (Leibniz Institute for Baltic Sea Research Warnemuende, Germany), Justyna Kobos (University of Gdansk, Poland) and Anu Vehmaa (University of Helsinki, Finland) for sample collection. This work was supported by grants from the Simons Foundation (403249 to A.J.A. and 725407 to E.P.), grants from the National Science Foundation (1651087 to A.J.A. and DBI\u20102146866 to M.W.H.), and a grant from the Science Foundation Flanders, FWO (1221323N to E.P.). This research used resources available through the Arkansas High Performance Computing Center, which is funded through multiple NSF grants and the Arkansas Economic Development Commission. Funding:

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