There are only two known ways of being a living cell: the prokaryotic and the eukaryotic. Prokaryotes include the Bacteria and Archaea. Prokaryotic cells are generally only a few micrometers in size, have simple cellular structures including cytoplasm with a fibrous nucleoid, ribosomes, a plasma membrane, and a cell wall (Fig. 1a). Eukaryotic cells are much more complex and include multi-cellular organisms; e.g., animals, plants, and fungi. Eukaryotic cells have a nucleus enclosed by a double membrane and show complex membranous cellular structures: endoplasmic reticula, Golgi apparatuses, peroxisomes, lysosomes, endosomes, and various sizes and types of vacuoles. Additionally, eukaryotic cells have either one or both of two distinct types of organelles that contain their own DNA: mitochondria and chloroplasts. Eukaryotic cells also have various types of cytoskeletal structures: centrioles, microtubules and microfilaments (Fig. 1b). Eukaryotic cells typically have nearly 10000 times the volume of prokaryotic cells.
Fig. 1. Schematic diagrams of a prokaryotic cell (colon bacillus, a) and a eukaryotic cell (rat pancreas, b). (Reprinted from Yamaguchi M, Kembikyo 48, 124-127, 2013).
Eukaryotes are thought to have evolved from prokaryotes, and the problem of how eukaryotes could have evolved from prokaryotes is one of the greatest puzzles 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 to find such an organism 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.
In 2010, Dr. Masashi Yamaguchi and his research team took a vessel to the Myojin Knoll, which is located about 100 km south of Hachijo Island off the coast of Japan. Samples were collected at a depth of 1200 m and fixed with glutaraldehyde on board, and transported to the laboratory in Chiba University. A total of 420 blocks were prepared by newly developed method that preserved close-to-native images of cell ultrastructure, and serially cut and observed in electron microscope. After one year of patient observation, Dr. Yamaguchi found a yeast-like microorganism several microns in size with a cell wall.
However, this microorganism was found to lack a nucleus enclosed by a double membrane typical for eukaryotes (Fig. 2). The ‘nucleoid’ of the host cell had a highly irregular shape and occupied most of the host cytoplasm (Fig. 3b). It consisted of fibrous material (DNA) and ribosomes. Interestingly, the ‘nucleoid’ was different from both the true nucleoids of prokaryotes and the true nuclei of eukaryotes in that it was enclosed by single-layer membrane (Fig. 2).
Fig. 2. An ultrathin section of Parakaryon myojinensis. Note the large irregular ‘nucleoid’ (N) with single layer ‘nucleoid membrane’ (NM), the presence of endosymbionts (E), and the absence of mitochondria. Also labeled are the cell wall (CW) and plasma membrane (PM). (Reprinted from Yamaguchi et al., J Electron Microsc, 61, 423-431, 2012).
The nucleoid membrane was not a closed membrane system but was interrupted by gaps through which the nucleoid region was connected to the cytoplasm. It had no mitochondria, but had ‘endosymbionts’ with bacteria-like morphology consisting of ribosomes and fibrous nucleoids but no cell wall (Fig.2). By 3D reconstruction from the 67 complete serial sections (Cover page) and structome analysis, they found a total of three endosymbionts in the cell (Fig. 3d). The ‘nucleoid’ of the host occupied 40 % of the cell volume (Fig. 3b) and was surrounded by a complicated cytomembrane system (Fig. 3c). The cell lacked chloroplasts, a nucleolus, plastids, Golgi apparatuses, peroxisomes, centrioles, spindle pole bodies, and microtubules (Table 1). These features show that the microorganism does not belong to a prokaryote nor eukaryote, and may be an intermediate form between them. Therefore, Dr. Yamaguchi named the microorganism ‘Parakaryon myojinensis’.
Fig. 3. The three dimensional reconstruction of P. myojinensis. a The whole cell. b The nucleiod. c The cytomembrane system of the host cell. d The endosymbionts. e The distribution of vacuoles in the host cell. f The distribution of the small granulated electron-transparent materials in the host cell. g Trace image of one ultrathin section. (Reprinted from Yamaguchi et al., J Electron Microsc, 61, 423-431, 2012).
Table 1. Features of Parakaryon myojinensis
The generic name, ‘Parakaryon’ comes from Greek para (next to) and karyon (kernel, nucleus) and reflects its position between eu- and prokaryotes. The specific name, ‘myojinensis’ reflects the locality where the samples have been collected i.e. the hydrothermal vents at the Myojin Knoll off the coast of Japan. This organism exemplifies a potential evolutionary path between prokaryotes and eukaryotes, and the presence of the organism supports the endosymbiotic theory for the origin of mitochondria and the karyogenetic hypothesis for the origin of the nucleus.
The discovery of Parakaryon myojinensis is discussed in detail in the book of Dr. Nick Lane ‘The Vital Question: Why is the Life the Way it is (2015)’. P. myojinensis is also appear in ‘Wikipedia’.
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Grand Fellow Masashi Yamaguchi, Ph. D.Medical Mycology Research Center,Chiba University,Japan.
Dr. Masashi Yamaguchi was born in Yamagata, Japan, in 1948. He graduated from Yamagata University, in 1971. In 1978, Dr. Yamaguchi was awarded Ph. D. from Tokyo Metropolitan University. Throughout his career, Dr. Yamaguchi held various positions in research and academic fields such as Researcher at Memorial Sloan-Kettering Cancer Center in New York (1975-1980) and Monell Chemical Senses Center in Philadelphia (1980-1981), Assistant Professor-Lecturer at Jikei University School of Medicine in Tokyo (1981-1996), and Associate Professor at Chiba University (1996-2014).
Dr. Yamaguchi has done significant research studies based on electron microscopy of microorganisms. In 2006, he coined a word ‘structome’, and defined it as the ‘quantitative and three-dimensional structural information of a whole cell at the electron microscopic level’. In 2011, he succeeded in structome analysis of Saccharomyces cerevisiae (a species of yeast) by freeze-substitution and serial ultrathin sectioning. Back in 2010, he also started the study on deep-sea microorganisms, and observed that conventional chemical fixation severely distorted the cell structure of microorganisms. Based on this study, Dr. Yamaguchi developed a new method to preserve the exquisite close-to-native cell structure by applying rapid freeze-freeze substitution after glutaraldehyde fixation. Using this new fixation method and structome analysis, in 2012, he discovered Parakaryon myojinensis from the deep sea.
Presently, Dr. Yamaguchi is the Grand Fellow at Chiba University (2014-current year).
Dr. Yamaguchi is a member of the Japanese Society of Microscopy and also the editor of the book named ‘Guide Book for Electron Microscopy’, written in Japanese.
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