The bacterial origin of mitochondria: Incorrect phylogenies and the importance of metabolic traits

Contrary to other cellular organelles, mitochondria have several features of bacterial nature (Searcy, 2003), starting with their nude DNA (mtDNA). Since the popularization of the almost forgotten symbiotic hypothesis for the evolution of mitochondria (Martin, 2017a; Sagan, 1967), the bacterial origin of mitochondria has become a widely accepted notion in biomedical sciences (Fernandez-Vizarra and Zeviani, 2021; Martin, 2017a; Medini et al., 2020; Mills et al., 2022). Alphaproteobacteria are a large class of Proteobacteria primarily known for their photosynthetic, pathogenic and nitrogen-fixing members (Cevallos and Degli, 2022; Hördt et al., 2020; Williams et al., 2007). These bacteria have been considered the likely relatives to the ancestors of mitochondria, protomitochondria (Gray et al., 1999; Martin, 2017a; Martin et al., 2020; Mills et al., 2022; Roger et al., 2017; Searcy, 2003; Yang et al., 1985). However, it remains unclear, and controversial, from which lineage of extant alphaproteobacteria mitochondria evolved (Abhishek et al., 2011; Degli Esposti et al., 2014, Degli Esposti et al., 2018; Gray et al., 1999; Martin, 2017a; Muñoz-Gómez et al., 2022; Thiergart et al., 2012; Tria et al., 2021). Recently, it has been proposed that protomitochondria might have originated from an extinct lineage outside the core clade of alphaproteobacteria, presumably related to a group of metagenome assembled genomes, MAGs (Martijn et al., 2018; Muñoz-Gómez et al., 2022; Schön et al., 2022). The proposal is solely based on phylogenetic inference (Fan et al., 2020; Martijn et al., 2018; Muñoz-Gómez et al., 2022) and appears to gain traction among evolutionary biologists (for a recent review, see Verhoeve and Gillespie, 2022). However, is does not explain the large number of metabolic traits shared by extant alphaproteobacteria and mitochondria (Degli Esposti et al., 2018, Degli Esposti et al., 2022). This article presents additional evidence for the mitochondrial origin from alphaproteobacteria and therefore will maintain such opinion, supported by several previous studies (Degli Esposti et al., 2014, Degli Esposti et al., 2022; Fan et al., 2020; Gray et al., 1999; Thiergart et al., 2012; Tria et al., 2021).

The separation of alphaproteobacteria from other bacterial classes likely occurred after primordial cyanobacteria had established permanent levels of oxygen on Earth atmosphere (Degli Esposti et al., 2019; Lyons et al., 2018; Mills et al., 2022). This fundamental event, which transformed earth geochemistry and dramatically influenced life, occurred about 2300 million years (my, or Ga) ago and is called the Great Oxygenation Event, GOE (Fig. 1). Current consensus posits that the birth of the first eukaryotic cells, usually defined as LECA (Last Eukaryotic Common Ancestor), occurred 500 or 600 million years after the GOE (see Mills et al., 2022 and references therein). LECA was almost certainly a marine organism with ancestral mitochondria well adapted to the relatively low levels of oxygen that were present in marine environments after the GOE—less than 10% of current levels in the atmosphere (Cohen and Kodner, 2022; Lyons et al., 2018; Mills et al., 2022). The oxygen affinity of aa3 cytochrome c oxidase (COX IV) of extant eukaryotes allows some respiration under these conditions (Degli Esposti et al., 2019), which nowadays are considered to be hypoxic and unsuitable for most marine organisms (Mills et al., 2022; Sperling et al., 2015). Yet, there are contemporary multicellular organisms adapted to low levels of oxygen for extended periods of time without major changes in the physiology of their aerobic mitochondria. The living fossil Nautilus, a cephalopod with beautiful spiral shell (Neil and Askew, 2018), is probably the best known example of such marine organisms. It is therefore plausible that the descendants of LECA were able to thrive in poorly oxygenated marine environments, differentiating in major lineages of flagellates feeding on bacteria and autotrophic algae living photosynthetically in the photic strata of ancestral oceans (Burki et al., 2020; Cohen and Kodner, 2022). Eukaryotic life remained fundamentally unicellular until about 600 my ago, when oxygen levels significantly increased also in the depth of the oceans (Lenton et al., 2016), triggering the explosive phase of eukaryotic differentiation that is usually called Cambrian explosion (Briggs, 2015; Cohen and Kodner, 2022; Medini et al., 2020).

The Cambrian explosion was followed by the colonization of emerged land by plants and animals (Fig. 1). Primordial land plants rapidly differentiated in large organisms forming vast forest-like biota, leading to an enormous increase in oxygen (Lenton et al., 2016), as illustrated by the pale bluish background in the middle of Fig. 1. After several mass extinction events (Jablonski and Chaloner, 1994), atmospheric oxygen adjusted to current levels. The present review will examine the possible impact of mass extinction events on the mtDNA of extant animals and will then survey metabolic traits in the frame of syntrophic models for mitochondrial evolution (López-García and Moreira, 2020; Mills et al., 2022). The survey will finally examine the traits of aerobic metabolism that are shared between extant alphaproteobacteria and mitochondria in light of recent proposals for the origin of mitochondria, either outside (Martijn et al., 2018) or within core alphaproteobacteria (Degli Esposti et al., 2022).

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