Mitochondrial genome reduction and accelerated evolution in planktonic foraminiferans

Abstract

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 calcifyers that are widely distributed across global oceans and important paleoenvironmental proxies. Through single-cell genomic sequencing, here we report a 22-kb complete mitogenome of a planktonic foraminiferan from tropical seawater, which is the smallest known to date among all sequenced mitogenomes of Rhizaria, a major lineage of eukaryotes. It contains only six protein-coding genes and fragmented ribosomal RNA genes, and has lost most genes in oxidative phosphorylation and all genes in mitochondrial translation. 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 the unique trajectory of mitogenome reduction during rhizarian evolution and the use of single-cell approaches for recovering microbial eukaryotic genomes and expanding our understanding of mitochondrial evolution.