Plastomes of Hyalomonas oviformis and Hyalogonium fusiforme evolved dissimilar architecture after loss of photosynthesis

The loss of photosynthesis in land plants and algae is typically associated with parasitism but can also occur in free-living species, including chlamydomonadalean green algae. The plastid genomes (ptDNAs) of colorless chlamydomonadalean species are surprisingly diverse in architecture, including highly expanded forms (Polytoma uvella, Leontynka pallida) as well as outright genome loss (Polytomella species). Here, we explore the ptDNAs of Hyalomonas (Hm.) oviformis (SAG 62-27; formerly known as Polytoma oviforme) and Hyalogonium (Hg.) fusiforme (SAG 62-1c), each representing independent losses of photosynthesis within the Chlamydomonadales. The Hm. oviformis ptDNA is moderately sized (132 kb), smaller than that of its photosynthetic relative Hyalomonas chlamydogama SAG 11-48b (198.3 kb), with a reduced gene complement but still encoding the ATPase subunits. The Hg. fusiforme plastome, however, is the largest yet observed in colorless plants or algae (~463 kb) and has a coding repertoire that is almost identical to that of its photosynthetic relatives in the genus Chlorogonium. Furthermore, the ptDNA of Hg. fusiforme shows no clear evidence of pseudogenization, which is consistent with our analyses showing that Hg. fusiforme is the non-photosynthetic lineage of most recent origin among the known colorless Chlamydomonadales. Together, these new ptDNAs clearly show that, in contrast to parasitic algae, plastid genome compaction is not an obligatory route following the loss of photosynthesis in free-living algae, and that certain chlamydomonadalean algae have a remarkable propensity for genomic expansion, which can persist regardless of the trophic strategy. One sentence summaryThe plastid genomes of two free-living chlamydomonadalean algae, Hyalomonas oviformis and Hyalogonium fusiforme, reveal different evolutionary stages following the loss of photosynthesis.