SELENOMONAS BOSKAMP, 1922-A GENUS THAT INCLUDES SPECIESSHOWING AN UNUSUAL TYPE OF FLAGELLATION

ERWIN F. LESSEL, JR. AND ROBERT S. BREEDCornell University, Geneva, New York

In revising the 6th edition of Bergey's Manual and they have been so reported by a few investi-(1), a study has been made of the validity of the gators. When examined by dark field microscopygenus Selenwmas Boskamp (2). This generic and as stained by Giemsa's stain, the attachmentname was introduced into the literature by von of the flagella in the center of the concave sideProwazek (3) in 1913. However, he did not name becomes clear. A highly refractive body withinany species as belonging in the genus, and the the cell absorbs nuclear stains and apparently isname did not have a valid status until Boskamp a nuclear body. The cell structure and unique(2) described the species Selenomonas palpitans form of flagellation fully justify the recognitionfrom the caecum of a guinea pig. This species of this species as the type species of a genushad been named earlier (1921) by Simons (4), distinct from Spirillum.but he failed to give a description so that the Because of the anaerobic nature of these or-organism did not receive a valid name until ganisms, investigators have not succeeded inBoskamp (2) published a description of it, cultivating them very readily, and their physio-ascribing the description to Simons. logical characteristics were not well known untilThe species mentioned above includes organ- Macdonald (5) succeeded in cultivating the

isms that are unique in their type of flagellation. mouth organism anaerobically in reduced bloodThese organisms have been generally over- agar and Difco thioglycolate broth.looked as they are strictly anaerobic and do not Selenomonas palpitans apparently occurs notgrow readily on the media that were used by only in the intestinal tract of guinea pigs, butearly investigators. It is little wonder that a also in the intestine of related rodents and her-poorly described genus and a species introduced bivorous mammals. It, or a closely relatedinto the literature with so little regard for the species, has been found by von Prowazek (3) inconventions established by codes of nomenclature examinations of blood contaminated with fecalhave been so generally ignored. matter of gazelles, giraffes and antelope shot inSet8nomor palpitans is, however, a species in Africa (3). It has also been found in Brazil (6)

which the organisms are sufficiently charac- in a rodent related to the guinea pig (Caviateristic in their appearance and habitat to sperea) and in a deer (Caryacus sp.).make even a microscopic description adequate The recognition of the genus Selenomonas isfor identification. The cells are of crescent form also indicated by the history of another specieswith blunt ends and are spirally twisted when of bacteria that has been known for an eventhey remain in chains. Thus they show the longer time than Selenomonas palpitans. In fact,normal appearance of organisms belonging to Dobell (7), in his book describing the work ofthe genus Spirillum. However, the cells are van Leeuwenhoek, feels confident that thismotile with a curious tumbling type of motility organism was one of those found in the humandifferent from that of the ordinary spirillum. mouth by this investigator in his original de-Staining with Giemsa's stain by von Prowazek scription of bacteria from the mouth. This

4,(3) revealed what appeared to be a single, red- species from the human mouth, which has beenstained, very heavy flagellum attached at the named Spirillum sputigenum since 1886 (8),middle of the concave side of the cell. Further shows a tumbling, rotary motion. Because ofstudies showed this stout flagellum to be in this characteristic movement van Leeuwenhoekreality a tuft of perhaps a dozen individual was led to draw the path of this organism in hisflagella. As shown in a related species from the original drawing as a curved, dotted line with ahuman mouth in separated form in electron loop in it (7).micrographs by Macdonald (5), the flagella may It has been difficult to determine who firstreadily be thought of as attached peritrichously, used the binomial Spirillum sputigenum. How-

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166 ERWIN F. LESSEL, JR. AND ROBERT S. BREED [VOL. 18

ever, it seems probable that Miller, an American that they were like spirilla in many ways,dentist, originated the name during the course though they were doubtful whether they shouldof his work that resulted in the publication of his be regarded as bacteria. They concluded thatinaugural dissertation from the University of these flagellated crescents were an unusualBerlin. Apparently Flugge (8) knew of Miller's primitive type and listed them as a sort ofwork and used the name (without giving its "Pro-flagellate".origin) in the second edition of his textbook The crescents from the rumen are described(1886). This is the first use of the binomial in the foregoing papers as having a morphologySpirillum sputigenum that we have found, and like that of the organisms placed in the genusit is accompanied by a description of the species. Selnomonas. They normally have a stoutMiller's dissertation (9) was not published until flagellum attached in the center of the concave1887. No copy of this has been found, but he side of the crescent, and the organisms divide byprobably described SpiriUum sputigenum in it. transverse fission. When this happens, theAt least he uses this binomial and describes this flagellum divides lengthwise and for a time thespecies in the various editions of his book on two flagella are attached near the blunt ends ofmouth organisms (10) that is based on this the more or less pear-shaped young cells. Thethesis. In subsequent literature Miller is usually flagella stain red with Giemsa's stain and thengiven as the author of this binomial. show that they are divided into fibrils as if theMiller did not succeed in cultivating this stout flagellum really represented a tuft of

species from the human mouth, but he and flagella. The cells show several refractive bodiesvarious other investigators studied it micro- flattened against the cell membrane; thesescopically. It soon was established (11, 12, 13, granules stain with chromatin stains and may be14) that this crescent-shaped organism had a nuclear in character. Occasionally the granulestuft of flagella attached laterally. This mor- lie underneath the point where the flagella arephology is exactly similar to that described for attached as is also stated to be true in Seleno-Selenomonas palpitans, and therefore Dobell (7) monas palpitans.placed Spirillum sputigenum in the genus Because Woodcock and Lapage (17) build upSelenomonas in 1932. The latter species, however, a doubtful life cycle for the rumen organismswas not well described until Macdonald (5) pub- and because other characteristics are not exactlylished his thesis. Like Selenomonas palpitans it is like those of Selenomonas sputigena or of Seleno-a strict anaerobe. monas palpitans, the rumen species is accepted

Protozoologists have reported the presence of for the present as a third species in Selenomonas.still another organism in the rumen juice of The movements of the rumen organisms areherbivorous mammals (cattle, sheep, deer and described in terms similar to those used in de-especially goats) that is similar to Selenomonas scribing the movements of the species previouslysputigena and S. palpitans. Certes (15) observed placed in Selenomonas, and the body of the or-these in 1889 and, because of certain resem- ganism is reported to have the power of move-blances (S-form when in chains) to the protozoan ment independent of any action of the flagella.species Ancyromonas ides Kent, named On this account, the possibility that these or-these crescent-shaped forms Ancyromonas rumi- ganisms may have affinities with the spirochaetesnantium. is discussed (see next section).Kerandel (16) also found this so-called Ancy- Textbooks of protozoology by Wenyon (18)

romonas in the blood of an antelope (Cephalophus and by Neveu-LeMaire (19) describe these un-sp.) that was contaminated with stomach con- usual crescent-shaped organisms. Wenyontents. The animal was shot in the Congo Region placed them in the genus Selenomonas under theof Africa. name Selenomonas ruminantium (Certes) Wen-

Later Woodcock and Lapage (17) found these yon, and they are described under this name asorganisms in the rumen juice of various domestic recently as 1948 by McGaughey and Sellers (20).animals and placed them in a new genus Seleno-mastix under the name Selenomastix ruminantium DISCUSSION(Certes) Woodcock and Lepage. The latter From this review it is evident that three quiteauthors were confident that the organisms in different groups of workers, (a) students of oralquestion were not true protozoa and reported bacteriology, (b) investigators of intestinal

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1954] SELENOMONAS BOSKAMP 167

bacteriology, and (c) protozoologists, have all Prowazek (3) in 1913 has priority over Seleno-found and named these flagellate organisms. The mastix that Woodcock and Lapage (17) proposedorganism found in the human mouth has been the same year, the fact that von Prowazek didnamed Selenomonas sputigena and has been not name a species as belonging in the genuscultured anaerobically on Difco thioglycolate gives Selenomonas the status of a nomen nudum.media by Macdonald (5) in a way that demon- Nevertheless, Selenomonas von Prowazek hasstrates that it should be regarded as a bacterium. been accepted by some as having priority (18,The organism found in the rumen juice of her- 19, 20), and general usage has favored its ac-bivorous mammals has been named Selenomonas ceptance. Therefore, Selenomonas has been usedruminantium; it has not been cultured and is not in this discussion, while awaiting a review of thewell known even to recent students of rumen status of the two names by the Internationalbacteriology though it is well known to pro- Judicial Commission on Bacteriological No-tozoologists. The organism found first in the menclature.caecum contents of guinea pigs (which is namedSelenomonas palpitans) has later been shown to REFERENCESbe common in the intestines of both rodents and 1. BREED, R. S., MURRAY, E. G. D., AND HIT-herbivorous mammals. As these bacteria swim CHENS, A. P. 1948 Bergey's manual ofby means of a tuft of flagella and have also been determinative bacteriology. 6th ed. Theclaimed to have the power to move independ- Williams & Wilkins Co., Baltimore, Md.ently of the flagella (2), they may well represent 2. BosKAmP, E. 1922 Ueber Bau, Lebensweiseorganisms intermediate between Spirillum and und systematische Stellung von SelenomonasSpirochaeta, thus indicating a close relationship pi taen (ioAb.n).CenI,Orakti Para-between the species placed in Sillaceae and . VON PROWAZEK, S. 1913 Zur Parasitologiethose placed in Spirochaetroeae. von Westafrika. Centr. Bakt. Parasitenk.,

In view of the similar morphology and the Abt. I, Orig., 70, 32-36.limited cultural studies that have been made on 4. SIMONs, H. 1921 Ueber Selenomonas pal-the three species included in this genus, it is, of pitans n. sp. Centr. Bakt. Parasitenk.,course, possible that all of these species are Abt. I, Orig., 87, 50.identical; but for the present it is believed de- 5. MACDONALD, J. S. 1953 The motile non-sirable to regard them as separate species. It sporulating anaerobic rods of the oralmay even be possible that further studies may cavity. Thesis. University of Toronto.show that additional species should be recog- 95 ppHnized. 6. DA CUNHA, A. M. 1915 Sobre apresenga de

"Selenomonas" no coecum dos roedores.CONCLUSIONS Brasil Medico, 29, No. 5, 33.

Selenomonas von Prowazek, 1913, emend. 7. DOBELL, C. 1932 Antony van LeeuwenhoekBoskamp, 1922, is a recognizable genus and and his "little animals", p. 245. Har-should be accepted as such, type species Seleno- court, Brace, & Co., New York.monas palpitans Simons ex Boskamp, 1922, the 8. FLtGGE, C. 1886 Die Mikroorganismen. 2

only species placed in the genus when it was Auf., Leipzig, 387-388.valdlyspubieshaed.mthis ienusw wasfirstd 9. MILLER, W. D. 1887 Ueber pathogenevalidly published. This species was first de- Mundpilze. Inaug. Diss., Berlin.scribed from the contents of the caecuml of 10. MILLER, W. D. 1888 Die Mikroorganismenguinea pigs. A second species that belongs in der Mundhohle. 1 AuO., Leipzig; Thethe genus is Seenomnas sputigena (Flugge, microorganisms of the human mouth. Eng.1886) Dobell, 1932. This species occurs in the ed., S. S. White Dental Mfg. Co., Philadel-human mouth and may even have been seen by phia, 1890; 2 Aufl., Leipzig, 1892.van Leeuwenhoek in his studies of mouth or- 11- LOEWENTHAL, W. 1906 Zur Kenntnis derganisms in 1683. Still a third species has been Mundspirochiten. Med. Klinik, 2, 278-described by protozoologists as Selonaso 12. 281.

1.HOFFMANN, E., AND VON PROWAZEK, S. 1906ruminantium (Certes, 1889) Wenyon, 1926. It is 12 HOFAN E. AN VO RWZK .10

foundminantieum(Certesc18 Wenyon, 1926 Untersuchungen uber die Balanitis- undfound i the ruinen jueie of herbivorous mam- MundspirochAten. Centr. Bakt. Parasi-inals. The genus clearly belongs in the family tenk., Abt. I, Orig., 41, 817-821.Spirillaceae Migula. 13. MUHLENS, P. 1909 Ueber Zuchtung vonAlthough Selenomonas as proposed by von anaeroben Mikroorganismen der Mundhohle

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168 ERWIN F. LESSEL, JR. AND ROBERT S. BREED [VOL. 18

(u. a. Spirillum 8putigenum). Centr. Bakt. 17. WOODCOCK, H. M., AND LAPAGE, G. 1913 OnParasitenk., Abt. I, Orig., 48, 523-528. a remarkable type of protisten parasite.

14. YAMAMOTO, JUN31 1909 Ueber den Lo- Quart. J. Micro. Sci., N.S., 59, 431-458.komotionsapparat der Protistenzellen. 18. WENYON, C. M. 1926 Protozoology, p. 311.Centr. Bakt. Parasitenk., Abt. I, Orig., 5S, Vol. 1. Bailliere, Tindall and Cox, London.38-42. ~~~~~~~19.NEvEu-LEMAIRE, M. 1942 TraitM de proto-15. CERTES, A. 1889 Note sur les micro-or- 1Nole M. 14 traide proto-' . ~~~~~~~~~zoologieme~dicale et vdtdrinaire, p. 291.ganismes de la panse des ruminants. Bull. VigotFr.res, Paris, 1943.

soc. zool. France, 14, 70-73.20

oM EY, Pa., 1943.

16. KERANDEL, J. 1909 Sur quelques h6mato- 20. McGAUGHE, C. A., AND SELLERS, K. C.zaires observes au Congo. Bull. soc. path. 1948 Microflora of the rumen. Nature,exotique., 2, 208. 161, 1014-1015.

ADDENDUM

The pictures on Plate I are photomicrographs of Selenomonas palpitans. They show flagella arisingfrom the middle of the concave side of the organism and suggest that their insertion lies very close to,perhaps inside, the nucleus. The photographs reinforce the information contained in drawings of Seleno-monas in the first detailed account of this species by Boskamp (1922).

All figures are from preparations of the contents of the caecum of healthy guinea pigs.Figures 1-8. From caecum contents suspended in 5% formalin, washed by centrifugation and stained

by Loeffler's method. The cells in figures 2 and 3 are preparing to divide.Figures 4-8. From wet films on coverslips fixed for 7 minutes in Schaudinn's fixative (without acetic

acid). Stained with Giemsa solution. Figures 4 and 5 from films that had been treated for 10 minuteswith N/1 HCl at 60 C before staining. Figures 6, 7 and 8 from directly stained films that had been differ-entiated in 20% alcohol (Dobell, 1911). All Giemsa preparations were photographed mounted in water.

BOSKAMP, E. 1922 Ueber Bau, Lebensweise und systematische Stellung von Selenomonas palpitans(Simons). Centr. Bakt. Parasitenk., Abt. I, Orig., 88, 58-73.

DOBELL, C. C. 1911 Contributions to the cytology of the bacteria. Quart. J. Microscop. Sci., 56,395.

C. F. ROBINOW,Department of Bacteriology and Immunology,University of Western Ontario,London, Ontario, Canada.

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PLATE I

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