Perspective a Units‐of‐evolution Perspective on the Endosymbiont Theory of the Origin of the Mitochondrion

Abstract

Discussions of mitochondria and their hosts often conceptualize this relationship in a more or less modern form, focusing on the metabolic benefits of mitochondria to the host cell or on the possibility of intragenomic conflict. A more inclusive units-of-evolution perspective recognizes that both costs and benefits must be viewed from the level of the cells that initiated this interaction, the protomitochondrion and the primitive host cell. From this perspective, ecological and physiological considerations become central to the characterization of initial and subsequent host-mitochondria associations. Foremost among these considerations is the generation of superoxide radicals by modern mitochondria and the deleterious effects of these endogenous oxidants on modern eukaryotic cells. Because of their photosynthetic and aerobic ecologies, protomitochondria likely were relatively tolerant of such oxidants; anaerobic, heterotrophic, primitive host cells, on the other hand, likely were not. In the initial association of host and symbiont, the latter may have manipulated the former's life history by means of both endogenous oxidants and a superabundance of ATP. A resolution of this units-of-evolution conflict was necessary to continue this association, and this resolution, in a ritualized form, may have shaped the evolution of many features of modern eukaryotic cells and mitochondria, for example, the messenger functions of calcium ions, the regulatory role of phosphorylation cascades in cell-division cycles, the absence from the mitochondrial genome of replication factors, transcription factors, and adenine nucleotide carrier genes. The initial host-mitochondria interaction may have further channeled the evolution of multicellular eukaryotes, particularly animals, resulting in the association of mitochondria and the germinal plasm and in the use of extracellular ATP and endogenous oxidants as developmental signals. Evolutionary explanations for "free-radical" theories of development and aging are thus suggested.

Primitive anaerobic protozoa: the wrong host for mitochondria and hydrogenosomes?

“…This hypothesis argues that the original eukaryote was derived from an association between a H 2 -producing proteobacterium and an autotrophic archaeon, describing how in some circumstances this association gave rise to hydrogenosomes whilst in others it gave rise to mitochondria. This prediction, however, is contrary to the simplest explanation that hydrogenosomes are an adaptation of preexisting mitochondria (3,13).…”

“…In some versions of the endosymbiont hypothesis, the host is envisaged as a prokaryote, but in most versions it is envisaged as a eukaryote that either arose autogenously (without symbiosis) or as the result of a symbiosis of cells that occurred prior to the origin of mitochondria (for a random sample see 3,6,9,11,12,15,18,19,22). But in all versions of the 'classical' endosymbiont hypothesis that make a statement on the issue (e.g.…”

A briefly argued case that mitochondria and plastids are descendants of endosymbionts, but that the nuclear compartment is not

“…Importantly, gene transfer from symbiont to host is not an ad hoc invention of the hypothesis that is designed to explain a particular pattern of genetic compartmentation. Rather, it is a logical consequence that ensues from the selective pressures that arguably would have confronted such an anaerobic, symbiotic pair of cells in the environment (see Blackstone (1995) for a good discussion of selective pressures in endosymbiotic theory). Furthermore, the earliest phases of gene transfer from symbiont to host would not have required the pre-existence of a protein import machinery that directs the products of translocated genes back into the compartment from which the gene was donated.…”

“…The backbone of such a cytoskeleton could easily be derived from pre-existing prokaryotic gene products: tubulin-like FtsZ and actin-like FtsA. However, as Blackstone (1995) lucidly argued, limiting factors and immediate selective pressures must be explicitly formulated to account for the ¢xation of cellular novelties in endosymbiotic theory. Thus, we have to face the di¤cult question of what sorts of selective pressures would be su¤cient to lead to the ¢xation of a primitive cytoskeleton and an endomembrane system during the phase of evolution before anything similar to what we observe today in eukaryotes (endocytosis, the endoplasmic reticulum and nucleus) arose.…”

Natural and human economies compared

“…Hosts were better at getting food, whereas the aerobic guests were better at getting energy from that food. There was accordingly a basis for mutualism between host and guest, whereby complementary abilities could be pooled for the common good (Blackstone 1995). Subsequent selection entwined the fates of the mitochondria so closely with that of the host that the mitochondria could only reproduce by helping their hosts (Leigh 2010b).…”