Plastid genome analysis of three Nemaliophycidae red algal species suggests environmental adaptation for iron limited habitats

PLoS One. 2018 May 8;13(5):e0196995. doi: 10.1371/journal.pone.0196995. eCollection 2018.

Abstract

The red algal subclass Nemaliophycidae includes both marine and freshwater taxa that contribute to more than half of the freshwater species in Rhodophyta. Given that these taxa inhabit diverse habitats, the Nemaliophycidae is a suitable model for studying environmental adaptation. For this purpose, we characterized plastid genomes of two freshwater species, Kumanoa americana (Batrachospermales) and Thorea hispida (Thoreales), and one marine species Palmaria palmata (Palmariales). Comparative genome analysis identified seven genes (ycf34, ycf35, ycf37, ycf46, ycf91, grx, and pbsA) that were different among marine and freshwater species. Among currently available red algal plastid genomes (127), four genes (pbsA, ycf34, ycf35, ycf37) were retained in most of the marine species. Among these, the pbsA gene, known for encoding heme oxygenase, had two additional copies (HMOX1 and HMOX2) that were newly discovered and were reported from previously red algal nuclear genomes. Each type of heme oxygenase had a different evolutionary history and special modifications (e.g., plastid targeting signal peptide). Based on this observation, we suggest that the plastid-encoded pbsA contributes to the iron controlling system in iron-deprived conditions. Thus, we highlight that this functional requirement may have prevented gene loss during the long evolutionary history of red algal plastid genomes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / genetics
  • Cell Nucleus / genetics
  • Ecosystem
  • Evolution, Molecular*
  • Genome, Plastid / genetics*
  • Iron / metabolism
  • Phylogeny*
  • Plastids / genetics
  • Rhodophyta / genetics*
  • Sequence Analysis, DNA

Substances

  • Iron

Grants and funding

This study was supported by the grants from the Collaborative Genome Program (20140428) funded by the Ministry of Oceans and Fisheries, the National Research Foundation of Korea (NRF-2017R1A2B3001923), the Next-generation BioGreen21 Program (PJ01389003) from the Rural Development Administration, Korea, and by a grant from the National Science Foundation Assembling the Tree of Life program (DEB-0937975, 1317114) to Hwan Su Yoon and Morgan Vis. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.