In the debate among American biologists, especially Carl R. Woese, Ernst Mayr, and Lynn Margulis, whether there are two or three superkingdoms, domains, or empires of all life-forms – either only Prokarya (bacteria) and Eukarya (symbiosis-derived nucleated organisms), or Archaea, Bacteria (or Eubacteria), and Eukarya – all agree that it was the French protistologist Edouard Chatton (1883- 1947) who in the 1930’s divided life into two primary categories: prokaryotes and eukaryotes. (About Chatton’s life see four obituaries: Caullery 1947; Lwoff 1947, 1947-1948; Roubaud 1947). And all quote the same reference: “Chatton E. (1937 or 1938) Titres et Travaux Scientifiques [Titles and Scientific Works] (1906-1937). E. Sottano [the printer], Ste, France [sometimes wrongly Italy]”. However, no one recites the wording of the passage, nor gives the page of the book where the two fundamental terms are introduced.
This is namely one of the cases where most authors copy a footnote from another without having seen the original source. The book is extremely rare in public libraries, and it seems that in the USA, there is only one print copy and one microfilm copy, both in the Bioscience Library of the University of California in Berkeley. Probably, they are the only ones outside France. In the online catalogue of 22 of the largest university libraries in the UK plus the British Library (COPAC), you find only two other works of Chatton. And even in France, the Bibliothque Nationale does not possess the book nor is it to be found in the collective library catalogue of France or in the Pasteur Institute. Only an individual email inquiry brought two private (one in France, one in the USA), and four library copies to light, two in the small French sea coast places where Chatton had worked (Banyuls and Ste), and two in Paris: one in the library of the Acadmie des Sciences of which Chatton was a Correspondent, and one in the Central Library of the Musum National d’Histoire Naturelle.
The book has 407 pages. On the title page the professions of the author are stated, and the year of publication is 1937. However, after page 60, there is a second title page with the new position of Chatton which had changed in the meantime, and the year is 1938. (There are also copies only with the title page of 1938 at the beginning.) The one and only mention of the terms Eucaryote and Procaryote is on page 50. Here, for the first time, the French text and an English translation of the relevant paragraph is published:
Les protistologues s’accordent, aujourd’hui, considrer les Flagells autotrophes, comme les plus primitifs des Protozoaires noyau vrai, des Eucaryotes (ensemble qui embrasse aussi les Vgtaux et les Mtazoaires), parce qu’ils sont les seuls pouvoir faire la synthse totale de leur protoplasme partir du milieu minral. Les organismes htrotrophes sont donc subordonns leur existence, ainsi qu’ celle des Procaryotes chimiotrophes et autotrophes (Bactries nitrifiantes et sulfureuses, Cyanophyces).
The protistologists accord today to consider the autotrophic flagellates, being the most primitives of the protozoa with a true nucleus, Eucaryotes (assemblage that embraces also the plants and the metazoa [animals]) because they are the only ones capable to make the total synthesis of their protoplasm beginning from the mineral environment. The heterotrophic organisms are thus subordinated to their existence as well as to that of the chemotrophic and autotrophic Procaryotes (nitrifying and sulphurous bacteria, cyanophyceae [cyanobacteria]).
Chatton’s huge biological work was almost exclusively on protozoa. He was a specialist, not a generalist. Therefore, he probably was not aware of creating a fundamental dichotomy of the whole living world as was attributed to him in the scientific literature. Time was not yet ripe. Moreover, he had used the two terms already 12 years before.
In 1925, Chatton dedicated 81 pages of the “Annales des Sciences Naturelles: Zoologie” (Chatton 1925) to the description of an amoeboid protist he had already discovered in 1906: “Pansporella perplexa. Reflexions sur la Biologie et la Phylognie des Protozoaires”. Beginning on page 32, he tried to find the place of this protist within the systematics of protozoa. As he detected none on more than 40 pages, on page 75 he invented a special new group for Pansporella, the sporamoebas. In the whole text there is no mention of the two categories. However, on pages 76 and 77, there are “Synoptic tables [today we would call them dendrograms] of the place of Pansporella in the classification and the phylogeny of protists” (from the table of contents). And in both diagrams, the two main branches of the tree are named Procaryotes and Eucaryotes. The three twigs of the Procaryotes are Cyanophycae, Bacteriacae, and Spirochaetacae. The Eucaryotes have only protist twigs: Mastigiae (Flagellata, including chlorophyll-bearing flagellates, Rhizopoda, and Sporozoa), Ciliae, and Cnidiae. That means that at that time, Chatton did not think of plants and animals as Eucaryotes. He only considered eucaryotic protists.
Figure 1. Lieutenant of the Tunisian Infantry Edouard Chatton in 1918 with the director of the Pasteur Institute in Tunis, Charles Nicolle (1866-1936), who in 1928, received the Nobel Prize in medicine “for his work on typhus” (In 1909 he had discovered that typhus fever is transmitted by the body louse.). Chatton was associate, and for one year the deputy of Nicolle (photograph courtesy of Family Chatton).
The paper of Chatton of 1925 is so specialized that only protistologists perused it. The book of 1937/38 undoubtedly also was no reading matter for non-protozoologists, and moreover, it is so rare that it is highly improbable that it would fall into the hands of a general biologist. Thus, the expressions procaryote and eucaryote (written today with k instead of c) would still slumber undetected on these esoteric pages if there had not been another way to propagate them and to make them common knowledge.
The French Nobel prize winner Andr Lwoff (1902-1994) is famous for his research on the lysogeny of bacteriophages; however, it is not so well known that he also was a studious protistologist, and beginning in 1921, worked first as a pupil and later as a close colleague and friend of Chatton (Soyer-Gobillard 2002; Soyer- Gobillard and Schrevel 2003). Together, they co-authored 55 papers. Since 1921, Lwoff had been interested in the nutrition of protozoa, and after having published 23 papers on this subject, he summed up his work and the results of other workers in 1932 in a Monograph of the Institut Pasteur (at the same time his thesis for Sc. D.): “Recherches Biochimiques sur la Nutrition des Protozoaires” (Lwoff 1932). He began it in the Introduction on page 3 with the words (the French translated into English):
We divide with E. Chatton (1926 ) the Protists into: 1 Procaryotic Protists, without a definite nucleus and individualised mitochondria: Bacteria and affined forms. 2 Eucaryotic Protists, equipped with a nucleus and mitochondria. These are the Protozoa in the largest acceptation of the term. For the ease of the expos which follows we divide the eucaryotic protists, or Eucaryotes, arbitrarily in two groups… In the monograph the terms Eucaryotes and Procaryotes are found several times. However, Eucaryote was used only for protists, not for plants or animals.
What Lwoff did in France with protozoa, the bacteriologist Paul Fildes (1882-1971) and the biochemist Bert Cyril James Gabriel Knight (1904-1981) did in England with bacteria. They studied their nutritional requirements, since 1929 together, and from 1934 to 1939 in a “Unit for Bacterial Chemistry”, established by the Medical Research Council, in the Middlesex Hospital in London. When Knight was composing the monograph “Bacterial Nutrition” (Knight 1936), he came across the treatise of Lwoff. he got in touch with his French colleague, and in the acknowledgements of his booklet (p. 175), he thanked him “for having read the MS, and offered valuable criticisms and emendations”.
Figure 2. Edouard Chatton in the gown of professor of the University of Strasbourg (1922-1932) (photograph courtesy of Family Chatton).
On page 156 of “Bacterial Nutrition”, Knight referred to A. Lwoff (1932) and wrote: Lwoff divides the protista into: Procaryotic Protista, without nucleus and individual mitochondria: bacteria and related forms. Eucaryotic Protista, having a nucleus and mitochondria. These Eucaryotes (protozoa in the widest sense) are further subdivided by Lwoff… Thus, for Knight, it was not Chatton but Lwoff who grouped the protists into procaryotes and eucaryotes. After page 158, the two words were not mentioned anymore.
In 1938, Lwoff published a paper in French in the German “Archiv fr Protistenkunde” (the precursor of “Protist”): “Remarques sur la physiologie compare des Protistes eucaryotes” (Lwoff 1938) in which he wrote again: We divide with E. Chatton (1926) the Protists into Procaryotes and Eucaryotes…
The morphological evolution of microbes was studied since the last third of the 19th century. However, it seems that Lwoff was the first to investigate consciously their physiological evolution. An important finding of Lwoff, enunciated already in 1932 and confirmed by Knight in 1936, was that a regressive physiological evolution can lead, especially among p\arasites, to the gradual irreversible diminution or disappearance of certain biosynthetic abilities, and consequently, to new accessory essential nutritional requirements (growth factors, vitamins). In 1944, Lwoff published a book, dedicated to Chatton, about this subject: “L’volution Physiologique. tude des Pertes de Fonctions chez les Microorganismes” (The Physiological Evolution. Study of the Losses of Functions among the Microorganisms) (Lwoff 1944). And here once more he repeated on page 71 : We divide with Chatton (1926) the protists into two great groups: a) The Procaryotes,… b) The Eucaryotes…
That means the two terms were propagated in 1932 and in 1944 in the French, in 1936 in the English, and in 1938 in the German microbial literature. However, they were still restricted to protozoa and bacteria. And it seems that only one American student followed Lwoff’s use of the designations prokaryotic and eukaryotic, though only “to clarify the phytogeny of primitive organisms”, not to divide all life-forms into two superkingdoms: Ellsworth Charles Dougherty (1921-1965).
In 1957, Dougherty published an abstract “Neologisms Needed for Structures of Primitive Organisms” in the Journal of Protozoology (Dougherty 1957) in which he proposed the terms “prokaryon”, plural “prokarya”, for the moneran (bacterial) nucleus enclosing the genomic DNA not by a nuclear membrane, “eukaryon”, plural “eukarya”, for the nucleus of higher organisms bounded by a nuclear membrane and containing true chromosomes, and the corresponding adjectives “prokaryotic” and “eukaryotic”, denoting, respectively, “the condition of possessing prokarya or eukarya”. Dougherty’s prokarya and eukarya were nuclei, not what they mean today. Furthermore, Dougherty did not use the term prokaryote for the organisms possessing a prokaryon within their cells or the term eukaryote for those with a eukaryon in their cells.
After the incomprehensible indifference to Lwoff’s multiple mention of Chatton’s terms procaryote and eucaryote, we owe their general use for all organisms in today’s sense mainly to the Canadian bacteriologist Roger Yates Stanier (1916-1982) who had already in the 1940s made an unsuccessful attempt to define “The Main Outlines of Bacterial Classification” (Stanier and Van Niel 1941). The professor of the University of California in Berkeley used his sabbatical year 1960/61 for a stay at the Pasteur Institute in Paris, and there in an exchange of ideas with Lwoff in January or February 1961, he came to know the two expressions. In the Foreword of the book “The Biology of Cyanobacteria” (Stanier 1982), Stanier wrote: It was Andr Lwoff who proposed these two names [eukaryotes and prokaryotes] during a discussion that I had with him in 1961. He revived these historically appropriate names from oblivion, citing as his authority an equally obscure and rare publication from the great French protozoologist Edouard Chatton (1938).
In his autobiography (Stanier 1980), Stanier wrote: Andr Lwoff drew my attention to Chatton’s taxonomic dichotomy, printed in a rare publication… I adopted these terms with enthusiasm…
Stanier used his new knowledge in a French lecture at the French Society of Microbiology on 2 March 1961 titled “La place des Bactries dans le Monde Vivant” (The place of bacteria in the world of living) (Stanier 1961), in which he said (translated from the French): …the cell of inferior protists, bacteria and blue algae [cyanobacteria], is organized in a manner different from the cell one knows among the superior protistsp, among the plants and among the animals. A specific designation for these two types of cells has become essential, and I will adopt the terminology proposed twenty years ago by Chatton. The cell of the type, which exists among the bacteria and the blue algae, is a procaryotic cell; the cell of the type, which exists among the other organisms, is a eucaryotic cell.
Of more influence, especially in the English-speaking world, was an English paper Stanier wrote in 1962 together with his Dutch- American teacher and colleague Cornells Bernardus van Niel (1897- 1985) (Spath 1999) in a German journal, the “Archiv fr Mikrobiologie”, titled “The Concept of a Bacterium” (Stanier and Van Niel 1962): It is now clear that among organisms there are two different organizational patterns of cells, which Chatton (1937) called, with singular prescience, the eucaryotic and procaryotic type. This sentence and the following frequent use of the adjectives procaryotic and eucaryotic (cells, protists, etc.) introduced the fundamental bipartition of all living beings into the world of science for good. However, it is interesting that Stanier and van Niel did not use the nouns procaryotes and eucaryotes in their basic paper, but always spoke only of procaryotic and eucaryotic organisms (Stanier also helped in propagating “procaryotic” and “eucaryotic” – still with c – in the 2nd edition of the standard work “The Microbial World” by Stanier, Doudoroff, Adelberg 1963.). The footnote in Stanier’s French and English paper with the title of Chatton’s work, its printer, and the year of publication (1937) obviously is the source, which most authors copied without having seen the book itself.
“… the Chatton-Stanier concept of a kingdom (better, superkingdom) Prokaryota for bacteria (in the broadest sense) and a second superkingdom Eukaryota for all other organisms has been widely accepted with enthusiasm.” (Corliss 1986a).
“The work of Chatton was, with some few exceptions, devoted to the protozoa…” (Lwoff 1947-1948, p. 123). “He possessed also, allied to an almost violent and exclusive love for Protozoa, a peculiar sense which enabled him to recognize every known protozoon…” (Lwoff 1947). However, Chatton regarded himself less as a protozoologist, but primarily as a “protistologue” (protistologist). This is shown in a slip of his memory (or a deliberate act?) in his book (Chatton 1937/1938). On page 29, he wrote: “… I entered in 1907 at the Pasteur Institute into the Service of Protistology and Colonial Microbiology of Mr. F. Mesnil.” But Flix Mesnil (1869-1938) became in 1898 head of the Laboratory of Protozoology, and in 1907, also of the newly created Service de Microbiologie Coloniale (France had colonies until after the second World War with endemic infectious diseases, which were studied by the Pasteur Institutes.). In the annual reports of the Pasteur Institute of 1911 and 1912 it was called “Service de Protozoologie et de Zoologie Tropicale”.
In his book, Chatton also described his “Works of pathological protistology”, his “Works of protistology and marine zoology”, and “My works in the protistological literature”, and wrote: “During twelve annual volumes I gave analyses of French or foreign papers of protistology in the ‘Bulletin de l’Institut Pasteur'”. The French words “protozoologie” and “protozoologiste” (or “protozoologue”) are never used, only “protozoaires” (protozoa). However, it seems that the “protistologue” Chatton never defined what he understood by protists.
Probably, he agreed with Ernst Haeckel (1834-1919) who had introduced the term protist in 1866: “… we propose to sum up all those independent stocks of organisms, which cannot be ascribed with full certainty and without contradiction to the kingdoms of animals or plants, under the collective name of protists.” Footnote: “protiston, to (in Greek letters), the first of all, the primordial.” (Haeckel 1866, p. 203). Therefore, according to Haeckel, biology had three branches: A. Zoology, B. Protistology, C. Botany (Haeckel 1866, p. 21). (For a modern definition of protists, see the chapter “What is a Protist?” in Corliss 2000, pp. 131-132, and Corliss 1991.)
In 1735, the “father of taxonomy” Carolus Linnaeus (Carl von Linn 1707-1778) subdivided the Imperium Naturae (Empire of Nature) into three kingdoms: the Regnum Lapideum (Mineral Kingdom; lapideum, Latin, stony), the Regnum Vegetabile (Plant Kingdom), and the Regnum Animale (Animal Kingdom) (Linnaeus 1735). Parts of the varied history of taxonomy since then, especially concerning the search of the proper place for the microscopic living beings, and the changing number of kingdoms have been told by several authors (e.g., Corliss 1986 b, 1992, 1998; Rothschild 1989; Scamardella 1999). Here, only the most important milestones since 1938 are listed leaving out the many detours and wrong tracks, and outmoded terms like mychota or non-euphonic and unnecessary terms like protoctista.
When Chatton died on 23 April 1947, it was a little more than eight years since Herbert F. Copeland (1902-1968) had written in December 1938: “This paper proposes the recognition of certain groups of living creatures as kingdoms in addition to the two which are conventionally regarded [animals and plants]” (Copeland 1938, p. 383). Copeland (who had forerunners in the 19th century) added two kingdoms: the Monera (bacteria) and the Protista. If Chatton had come to know Copeland’s paper, he probably would have been very happy that his beloved protists were raised to the rank of a kingdom at the same level as animals and plants.
In 1959, Robert H. Whittaker (1920-1980) split off the kingdom Fungi from the kingdom Plantae, but for him, the bacteria were included in the Protista as a subkingdom (Whittaker 1959). In 1981, Thomas Cavalier-Smith (born 1942) “treated the Chromophyta and Cryptophyta as subkingdoms of a newlydefined kingdom Chromista” because “…the Chromista are so different from both the Protista and the Plantae that to lump them with either would cause great confusion” (Cavalier-Smith 1981, pp. 462, 477). Thus, he had two superkingdoms, the Prokaryota and the Eukaryota, and six kingdoms: Bacteria, Fungi, Animalia, Protista, Plantae, and Chromista.
At the time of the death of Chatton, the biological applications of the electron microscope in the US had began only a few years ago (\1940), and the double helix of 1953 and the wonders of molecular biology were still in the future. In the meantime, these revolutionary new methods to study the ultrastructure of organisms have enormously deepened our understanding of biodiversity, and changed fundamentally our conceptions also in the field of taxonomy. Because of the kingdom Protista being “immensely too heterogeneous” and “too diverse”, and because of “the arbitrariness of its boundaries” with the kingdoms Plantae, Fungi, and Animalia, in 1993 Cavalier-Smith split it into the three major kingdoms Archezoa, Protozoa, and Chromista (Cavalier-Smith 1993, p. 956). That is, he used the older and more familiar name Protozoa, rather than Protista, for the basal eukaryotic kingdom. In 1998, he reduced the Archezoa to a subkingdom of Protozoa, and thus, we now have besides the kingdom Bacteria two zoological kingdoms, Protozoa and Animalia, and three botanical kingdoms, Plantae, Fungi, and Chromista (Cavalier-Smith 1998).
“…the diversity of the protists is too great to be confined to a single kingdom and, thus, … their species require dispersal throughout all of the several kingdoms of the eukaryotic biotic world that are becoming widely recognized today.” (Corliss 1998, p. 85). Therefore, the problem was to distribute the great motley variety of more than 200,000 species of protists to the five eukaryotic kingdoms. That was done mainly by Cavalier-Smith and John O. Corliss (born 1922). Corliss specifies 35 phyla containing all known species of protists, and distributes 14 of them to the kingdom Protozoa, 11 to the kingdom Chromista, 6 to the kingdom Plantae, 2 to the kingdom Fungi, and 2 to the kingdom Animalia (Corliss 1998, 2000). The protistan megasystematics will remain in a state of flux, but if this taxonomy of Corliss is accepted, only minor modifications are to be expected in the future.
If Edouard Chatton could see the taxonomical scene of today, he might possibly be disappointed that the protists do not constitute a kingdom of nature anymore and are scattered in all other eukaryotic kingdoms; however, he probably would be consoled by the fact that his favorite field of research and life-long great love and passion, protistology, is, nevertheless, still very much alive and active. The most convincing proof is this journal which, more than half a century after Chatton’s death, is continuing to prosper. In his country the “Groupement des Protistologues de Langue Franaise” (Grouping of Protistologists of French Language), founded in 1962, is busy.
Among the huge tasks of protistology in the future is the answering of two major questions: How did eukaryogenesis, the coming- into-being of the eukaryotic cell, occur, and what protistan groups may have served as progenitors of the “higher” eukaryotic kingdoms? (Corliss 1989).
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