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

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.

红藻亚纲Nemaliophycidae涵盖海洋与淡水类群，其物种数占红藻门（Rhodophyta）淡水物种总量的半数以上。鉴于该类群栖息于多样生境，Nemaliophycidae是研究环境适应性的优质模式类群。为此，我们对两个淡水物种——Kumanoa americana（串珠藻目Batrachospermales）、Thorea hispida（索藻目Thoreales），以及一个海洋物种Palmaria palmata（海棕榈目Palmariales）的质体基因组（plastid genomes）进行了系统表征。比较基因组分析鉴定出7个基因（ycf34、ycf35、ycf37、ycf46、ycf91、grx及pbsA）在海洋与淡水物种间存在差异。在当前已公开的127个红藻质体基因组数据集中，多数海洋物种保留了pbsA、ycf34、ycf35、ycf37这4个基因。其中，编码血红素加氧酶（heme oxygenase）的pbsA基因拥有两个新发现的额外拷贝（HMOX1和HMOX2），这两个拷贝此前仅在红藻核基因组（nuclear genomes）中被报道过。两类血红素加氧酶各具独特的进化历史与特殊修饰（如质体靶向信号肽（plastid targeting signal peptide））。基于该发现，我们推测质体编码的pbsA基因在铁匮乏条件下参与铁调控系统。因此，我们指出，这一功能需求可能在红藻质体基因组的长期进化历程中阻止了该基因的丢失。