Eukaryotic cellular intricacies shape mitochondrial proteomic complexity

Abstract

Mitochondria have been fundamental to the eco‐physiological success of eukaryotes since the last eukaryotic common ancestor (LECA). They contribute essential functions to eukaryotic cells, above and beyond classical respiration. Mitochondria interact with, and complement, metabolic pathways occurring in other organelles, notably diversifying the chloroplast metabolism of photosynthetic organisms. Here, we integrate existing literature to investigate how mitochondrial metabolism varies across the landscape of eukaryotic evolution. We illustrate the mitochondrial remodelling and proteomic changes undergone in conjunction with major evolutionary transitions. We explore how the mitochondrial complexity of the LECA has been remodelled in specific groups to support subsequent evolutionary transitions, such as the acquisition of chloroplasts in photosynthetic species and the emergence of multicellularity. We highlight the versatile and crucial roles played by mitochondria during eukaryotic evolution, extending from its huge contribution to the development of the LECA itself to the dynamic evolution of individual eukaryote groups, reflecting both their current ecologies and evolutionary histories.

How mitochondria showcase evolutionary mechanisms and the importance of oxygen

“…Far from diminishing, step by step, towards oblivion upon sustained anoxia, mitochondria in these groups retain “normal” aerobic potential, but also have to alter their unicellular metabolism in highly diverse ways in response to abrupt changes in both nutrient and O 2 availability. If we further take into account that they often have to engage in very elaborate mechanisms (such as RNA pan‐editing) to be able to express mitochondrial genes from complex networks, it is not surprising in the least, that such cells have enormously complex mitochondrial proteomes 100,101 . However, the mitochondrial proteome of a member of the third (free‐living) sister group, which retained is phototrophic ability, Euglena gracilis , turns out to be surprisingly complex as well 102 .…”

“…If we further take into account that they often have to engage in very elaborate mechanisms (such as RNA pan-editing) to be able to express mitochondrial genes from complex networks, it is not surprising in the least, that such cells have enormously complex mitochondrial proteomes. 100,101 However, the mitochondrial proteome of a member of the third (free-living) sister group, which retained is phototrophic ability, Euglena gracilis, turns out to be surprisingly complex as well. 102 This indicates that mitochondrial proteome complexity was already present in the common ancestor of all three groups, and, just like glycosomes, arose independent of parasitism.…”

The development of intracytoplasmic membranes in alphaproteobacteria involves the conserved mitochondrial crista-developing protein Mic60

“…), the mitochondrion evolved from an endosymbiont most closely related to extant alphaproteobacteria (Muñoz-Gómez et al 2022; Martijn et al 2018; Fan et al 2020). In aerobic eukaryotes, mitochondria produce most of the ATP of the cell through aerobic respiration, i.e., the harnessing of energy through the coupling of electron transport to chemiosmosis with oxygen as a terminal electron acceptor, in addition to compartmentalizing other metabolic pathways (Roger et al 2017; Hammond et al 2022). Because aerobic respiration occurs at internalized membranes that can expand greatly, mitochondria allow for the proportional increase (or linear scaling) of respiration with cell volume across eukaryotes (Schavemaker and Muñoz-Gómez 2022).…”

“…In aerobic eukaryotes, mitochondria produce most of the ATP of the cell through aerobic respiration, i.e., the harnessing of energy through the coupling of electron transport to chemiosmosis with oxygen as a terminal electron acceptor. Mitochondria also compartmentalize other metabolic pathways 1,5 . Because aerobic respiration occurs at internalized membranes that can expand greatly, mitochondria allow for the proportional increase (or linear homologues of Mic60, many alphaproteobacteria also develop either lamellar or vesicular intracytoplasmic membranes (ICMs) that house diverse electron transport chains involved in methanotrophy, nitrification, and anoxygenic photosynthesis [21][22][23][24][25] .…”