A deep-sea microorganism and the origin of eukaryotes

By Masashi Yamaguchi and Cedric Worman

There are only two kinds of organisms on Earth: prokaryotes and eukaryotes. Prokaryotes include the Bacteria and Archaea and consist of structurally simple cells that are generally a few micrometers (1 µm= 1/1,000 mm) in size and lack a nucleus. Eukaryotes include animals, plants, fungi, etc. and consist of structurally complex cells that are nearly 10,000 times the volume of prokaryotic cells and have a nucleus enclosed by a double membrane in addition to various organelles such as mitochondria and chloroplasts.

Although eukaryotes are considered to have evolved from prokaryotes, there were no previously known examples of intermediate forms between prokaryotic and eukaryotic organization. In fact, the differences in cellular structure between prokaryotes and eukaryotes are so vast that the problem of how eukaryotes could have evolved from prokaryotes is one of the greatest enigmas in biology. One way to address this question is to find an organism with intermediate organization and examine its ultrastructure, DNA, and molecular machinery in detail. The deep sea is one of the most likely environments in which to find such organisms because it exhibits the extreme environmental stability that allows for the survival of morphologically stable organisms over long periods of time, such as the coelacanth fish, which has changed little morphologically in the past 400 million years.

Last year, we discovered a unique organism with cellular structures appearing to have intermediate features between prokaryotes and eukaryotes from the deep sea off the coast of Japan using electron microscopy. The organism was 10 μm long and 3 μm in diameter, having more than 100 times the volume of Escherichia coli, a common bacterium. It had a large ‘nucleoid’, consisting of naked DNA fibers (unlike eukaryotes, whose DNA is tightly organized with proteins) surrounded by a single nucleoid membrane (unlike both prokaryotes, which have no nucleoid membrane, and eukaryotes, which have a double nuclear membrane) and endosymbionts that resemble bacteria, but no mitochondria. Because this organism appears to be a life form distinct from both prokaryotes and eukaryotes, but similar to eukaryotes, we named this unique microorganism the ‘Myojin parakaryote’ with the scientific name of Parakaryon myojinensis (‘next to (eu)karyote from Myojin’) after the discovery location and its intermediate morphology.

There are two major hypotheses regarding the origin of eukaryotes. The symbiotic theory, initially proposed by Lynn Margulis in 1970, supposes that eukaryotes evolved from symbiotic relationships established between anaerobic archaeans and aerobic bacteria that began to live inside the larger archaeans. On the other hand, the autogenesis theory supposes that the structures and functions of eukaryotic cells developed gradually from simple rudiments in prokaryotic cells. The cellular structure of Parakaryon myojinensis suggests that stable endosymbiosis is maintained between the host and the engulfed bacteria, and thus supports the plausibility of the symbiotic theory.

We have found only one P. myojinensis so far, and need to collect more individuals to obtain molecular data, including sequences of ribosomal RNA genes, to establish the evolutionary relationships between this microorganism and the prokaryotic and eukaryotic branches of life.

We believe that life is a continuum and there might be a multitude of organisms in the deep sea that demonstrate many possible pathways from prokaryotes to eukaryotes, either because they are relatively stable descendents of the intermediates themselves or because they are unrelated lineages that chanced upon similar adaptations. Also, unusual prokaryotic life forms which never evolved or are extinct on the Earth’s surface might survive in the deep sea where the selective pressures are relatively stable and competition from other types of organisms is low. The extremely long generation times of deep-sea microorganisms due to low temperatures (1-2 °C) and poor nutrition would also favor the survival of ancient morphologies. Thus, the deep sea might be regarded as a huge living museum that may still hold a variety of the basic forms life has evolved in the 3.8 billion years since the first cell appeared on Earth.

Masashi Yamaguchi is an Associate Professor of Cell Biology at the Medical Mycology Research Center, Chiba University, Japan, and the Editor of the Journal of Electron Microscopy (becoming Microscopy in 2013). Cedric Worman is an Assistant Professor of Biology at Francis Marion University, South Carolina, USA. They are the authors of “Prokaryote or eukaryote? A unique microorganism from the deep sea” in the latest issue of the Journal of Electron Microscopy, which is available to read for free for a limited time.

The Journal of Electron Microscopy, the official publication of the Japanese Society of Microscopy, promotes research combined with any type of microscopy techniques, not limited to electron microscopy, by publishing informative articles on their theories, methods, techniques and instrumentation as well as their applications to life and material sciences.

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