A SUF Fe-S Cluster Biogenesis System in the Mitochondrion-Related Organelles of the Anaerobic Protist Pygsuia

Abstract

Many microbial eukaryotes have evolved anaerobic alternatives to mitochondria known as mitochondrion-related organelles (MROs). Yet, only a few of these have been experimentally investigated. Here we report an RNA-seq-based reconstruction of the MRO proteome of Pygsuia biforma, an anaerobic representative of an unexplored deep-branching eukaryotic lineage. Pygsuia's MRO has a completely novel suite of functions, defying existing "function-based" organelle classifications. Most notable is the replacement of the mitochondrial iron-sulfur cluster machinery by an archaeal sulfur mobilization (SUF) system acquired via lateral gene transfer (LGT). Using immunolocalization in Pygsuia and heterologous expression in yeast, we show that the SUF system does indeed localize to the MRO. The Pygsuia MRO also possesses a unique assemblage of features, including: cardiolipin, phosphonolipid, amino acid, and fatty acid metabolism; a partial Kreb's cycle; a reduced respiratory chain; and a laterally acquired rhodoquinone (RQ) biosynthesis enzyme. The latter observation suggests that RQ is an electron carrier of a fumarate reductase-type complex II in this MRO. The unique functional profile of this MRO underscores the tremendous plasticity of mitochondrial function within eukaryotes and showcases the role of LGT in forging metabolic mosaics of ancestral and newly acquired organellar pathways.