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

Abstract

<div><p>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, <i>Kumanoa americana</i> (Batrachospermales) and <i>Thorea hispida</i> (Thoreales), and one marine species <i>Palmaria palmata</i> (Palmariales). Comparative genome analysis identified seven genes (<i>ycf</i>34, <i>ycf</i>35, <i>ycf</i>37, <i>ycf</i>46, <i>ycf</i>91, <i>grx</i>, and <i>pbs</i>A) that were different among marine and freshwater species. Among currently available red algal plastid genomes (127), four genes (<i>pbs</i>A, <i>ycf</i>34, <i>ycf</i>35, <i>ycf</i>37) were retained in most of the marine species. Among these, the <i>pbs</i>A gene, known for encoding heme oxygenase, had two additional copies (<i>HMOX1</i> and <i>HMOX2</i>) 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 (<i>e</i>.<i>g</i>., plastid targeting signal peptide). Based on this observation, we suggest that the plastid-encoded <i>pbs</i>A 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.</p></div