Mitochondrial Genome Reduction and Accelerated Evolution in Planktonic Foraminiferans

The evolution of mitochondria provides crucial insights into the diversification of eukaryotes, with complex events of gene losses revealed through comparative analyses of mitochondrial genomes (mitogenomes) across eukaryotic lineages. However, the mitogenomes of many microbial eukaryotes remain underexplored due to challenges in their isolation and cultivation. Particularly understudied are Foraminifera (Rhizaria, SAR), unicellular calcifiers that are widely distributed across global oceans and important paleoenvironmental proxies. Using single-cell genomic sequencing, we report a 22-kb mitogenome from a planktonic foraminiferan in tropical seawater, the smallest known to date among sequenced mitogenomes of Rhizaria, a major lineage of eukaryotes. It contains only six protein-coding genes (including reduced versions of nad1 and cox2) and fragmented ribosomal RNA genes, and has lost most genes in oxidative phosphorylation and all genes encoding mitochondrial ribosomal proteins. Such genome reduction is associated with accelerated evolutionary rates and a lower GC content than that of benthic foraminiferan and other rhizarian mitogenomes. These findings highlight a unique trajectory of mitogenome reduction during rhizarian evolution and the use of single-cell approaches to recover microbial eukaryotic genomes and expand our understanding of mitochondrial evolution.