As an undergraduate, my interest in cell biology was spurred by a curiosity about the origins of life. I was particularly fascinated by the theory of endosymbiotic evolution, which holds that mitochondria and chloroplasts arose when a bacterium established a symbiotic relationship by taking up residence in a larger host cell. I naturally gravitated to this idea of cooperation leading to innovation and evolution. In contrast, I viewed Darwinism as all about competition and survival—all red in tooth and claw.

Some time ago, I visited Lester Park near Saratoga Springs, New York, where I stood on the fossilized remains of the mats of cyanobacteria (also called stromatolites) that grew on the bottom of the sea that covered much of North America 490 million years ago. This got me thinking about the idea of symbiogenesis again, so I decided to check the literature to see how things have developed.

Endosymbiotic theory was controversial when it was first proposed by Konstantin Mereschkowski and later championed by Lynn Margulis. Subsequent sequencing of the genome of mitochondria and chloroplasts confirmed the presence of the vestiges of the endosymbiont in the organellar genome. These evolutionary leftovers have given scientists enough information to understand what the bacterial endosymbiont may have looked like, but the nature of the archaeal host, sometimes called the last eukaryotic common ancestor (LECA), is unknown.

DNA sequencing is getting cheaper, easier, and faster, which allows sampling and sequencing of very diverse and complex environments (as evidenced by the increase in microbiome studies). Such metagenomics approaches permit the identification of new species of prokaryotes, even if they can't be cultured in the lab. An analysis of samples from Loki's Castle deep sea vents revealed the sequence of a new archaeal species that has a surprising number of homologs to proteins that are typically only found in eukaryotes. The species was named Candidatus Lokiarchaeum (a.k.a. Loki), and it is thought to be the closest living relative of LECA. Subsequent research has extended the species related to Loki to include Thor, Odin, and Heimdall as part of the aptly named Asgard superphylum of archaea.

A fascinating Opinion piece in Trends in Cell Biology imagines what this organism, which we've never actually seen and can't culture in the lab, could look like. Perhaps the most notable feature of the Asgard superphylum is the homology to GTPases, including a few that are similar to Rab- and Arf-type GTPases that are involved in intracellular membrane traffic. These results suggest that Loki and his clan express proteins that would allow them to develop the complex cellular features present in eukaryotes. The authors suggest that, by combining these components from the archaeal genome with a few genes and lipids from the bacteria, you could imagine the slow evolution of membrane trafficking and intracellular membrane compartments.

Although the Asgard archaea may help explain the evolution of parts of the endomembrane system, we’ve yet to discover intermediate species that could explain the complexity of the eukaryotic membrane system. An opinion in Trends in Microbiology suggests that secretion of outer membrane vesicles by the endosymbiont, rather than endocytosis by the host, led to the advent of the endomembrane system. This review includes an excellent Video Abstract where the authors explain their hypothesis clearly and with beautiful animations. The two models could both contribute, given that the complexity of the endomembrane system in eukaryotes likely requires elements that came from the host as well as the endosymbiont.



Although I always thought of the relationship of the early endosymbiont and host as beneficial for both parties (mutualistic), we don't really know if the relationship was mutualistic or exploitive. A recent paper in Current Biology (covered in a Dispatch) took advantage of a tractable, facultative (i.e., each can live with or without the other) microbial endosymbiosis between a ciliate and a green alga to perform a cost-benefit analysis of their relationship by comparing the growth of the two organisms in different levels of light for the alga and varying amounts of food for the bacteria. Interestingly, when light is plentiful, the host will cast off or digest the symbiont; when light is limited, the symbiont can escape the host, but the conditions are not ideal for it to survive on its own. Thus, stable endosymbiotic interactions may result from exploitive not mutualistic relationships. This result surprised me as it suggests that cooperation is not the only pressure at the heart of eukaryogenesis.

I'm sure there are more surprises in store. For example, a recent paper in Current Biology (covered in a Dispatch) performed a phylogenomic analysis of cyanobacterial genes in the nuclear and plastid genomes in a large number of algae and plants. The authors found that a freshwater cyanobacterium named Gloeomargartia lithophora is the closest living relative of the plastid ancestor. This result suggests that the first photosynthetic eukaryote evolved in freshwater biofilms or microbial mats, similar to the fossilized mats that I saw in Lester Park.

I look forward to seeing what scientists uncover next as they aim to unravel one of the biggest mysteries in evolution.