Chemiosmosis and the Origin of Eukaryotes

Abstract

Because their energy-converting membranes are on the outside of the cell, surface-to-volume constraints limit the size and complexity of prokaryotic cells. Eukaryotes transcend these constraints by having energy-converting symbionts within a larger cell. This clever engineering solution to surface-to-volume constraints, however, results in a levels-of-selection nightmare. For instance, defecting protomitochondria could use ATP for their own replication rather than export it to the cytoplasm. Mediating such conflicts was likely a crucial part of eukaryogenesis. Remarkably, the process of chemiosmosis favors conflict mediation. Chemiosmosis proceeds rapidly and conserves a large proportion of the energetic input, quickly generating products. These products can be stored in various ways, but storage mechanisms are slow relative to chemiosmosis and in any event storage capacity is usually limited. When conditions are opportune, chemiosmotic cells and organisms face the possibility of “end-product inhibition.” In the presence of molecular oxygen, this enhances the formation of reactive oxygen species. Such partially reduced forms of oxygen can have a variety of detrimental effects. To avoid blocking electron flow, the abundant products of chemiosmotic energy conversion must be consumed, stored, or simply gotten rid of. While mechanisms that modulate chemiosmosis are available, an alternative solution is simply to disperse excess product into the environment. This “no-cost” sharing—the free lunch you are forced to make—facilitates interspecific groups, and such groups can lead to cooperative symbioses. Chemiosmosis may thus have been one of the key drivers of the origin of eukaryotes, e.g., if their own replication was constrained, protomitochondria were forced to export ATP.

Life arose around half a billion years after the earth’s formation, but then got stuck at the bacterial level of complexity for more than 2 billion years, half the age of our planet. Indeed, bacteria have remained simple in their morphology (but not their biochemistry) throughout 4 billion years. In stark contrast, all morphologically complex organisms—all plants, animals, fungi, seaweeds and single-celled ‘protists’ such as amoeba—descend from that singular ancestor about 1.5–2 billion years ago.

Nick Lane [1]