MOTILE ENTEROCOCCI (STREPTOCOCCUS FAECIUM VAR. MOBILIS VAR. N.) ISOLATED FROM GRASS SILAGE

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1 MOTILE ENTEROCOCCI (STREPTOCOCCUS FAECIUM VAR. MOBILIS VAR. N.) ISOLATED FROM GRASS SILAGE C. W. LANGSTON, JOYCE GUTIERREZ, AND CECELIA BOUMA Dairy Cattle Research Branch, Agricultural Research Center, Beltsville, Maryland Hugh (1959) recently reported on motile enterococci isolated from human sources. He pointed out that motile strains in the genus Streptococcus are considered rare, and suggested that they have gone unrecognized simply because investigators have failed to examine for motility and flagella. Actually many strains of motile streptococci have been isolated and studied and the reader is referred to Hugh's paper for a rather extensive review of this group. vmotile streptococci previously examined have been of animal or human origin, and have been identified as Streptococcus faecalis or varieties of this species. The results reported here describe the cultural, morphological, and physiological characteristics of motile streptococci isolated from silage fermentations. The strains studied showed some resemblance to S. faecalis, but the majority of characteristics place them in the species Streptococcus faecium (Orla-Jensen, 1919). MATERIALS AND METHODS The work reported here describes 11 motile strains isolated during the screening of several hundred streptococci from early stages of silage fermentations. They are representative of about 40 motile strains obtained and account for a rather small percentage of the total isolates screened. Isolation techniques and methods used in studying the organisms have been reported elsewhere (Langston and Bouma, 1960a, b, and Langston, Gutierrez, and Bouma, 1960). RESULTS The strains were isolated from small subsurface colonies which were whitish in color and lensshaped with entire edges. Cells were oval and occurred singly, in pairs and short chains. They averaged 0.8 by 1.1 IA. They were gram-positive, facultative for oxygen, and motile. M1otility was observed in semisolid agar tubes and by the hanging-drop technique. Flagella were observed when young cultures (8 to 10 hr old) were stained Received for publication April 25, 1960 by the method of O'Toole (1942). Difficulties were encountered in early attempts to stain the flagella by the technique of Leifson (1951). Similar difficulties were encountered by Auerbach and Felsenfeld (1948), but Hugh (1959) showed excellent flagella stains by this method. It was unusual to see more than three or four flagella attached to a single cell, and they originated either terminally or laterally (figures 1 to 4). The cultures grew abundantly in glucose broth (final ph 4.2 to 4.6) and produced acetylmethylcarbinol. They grew at 10 and 45 C, in 6.5 per cent sodium chloride, at ph 9.6, and in broth containing 40 per cent bile. They grew in the presence of 0.1 per cent methylene blue in milk and caused early and complete reduction of the indicator. Five of the cultures gave a gamma reaction on blood agar, and six gave an alpha reaction. Ten of the 11 strains showed moderate growth on agar containing potassium tellurite at a final concentration of 1:2,500. At 24 hr, small gray colonies were observed in contrast to the larger dark black typical strains of S. faecalis. At 48 hr, the colonies were dark gray and of moderate size. The strains varied in their sensitivity to heat. Some showed good growth after heating at 60 C for 30 min and others responded slowly. All but one of the cultures reduced tetrazolium (Barnes, 1956). Since the strains showed strong reduction after 12 hr incubation, reduction was followed and compared with S. faecalis at 2-hr intervals over an 8-hr period. At 4 hr, S. faecalis showed a 3+ reaction, and the motile strains showed either no change or a 1 to 2 + reaction. At 6 hr, S. faecalis gave a 4 + reaction and the motile cultures varied from 1 to 3 +. All cultures gave a 4 + reaction at 8 hr. This test was repeated and essentially the same results were obtained. The organisms gave a bright red layer after extraction with butanol. The majority of the strains caused a reduced acid reaction in litmus milk at 24 hr, but only two produced enough acid for curd formation. 714

2 1960] MOTILE ENTEROCOCCI FROM GRASS SILAGE 715 'C_ 10-A vl I.. S Us 3 Figure 1. Motile Streptococcus faecium var. mobilis var. n. Pair of cocci showing 2 lateral flagella. Figure 2. Motile Streptococcus faecium. var. mobilis var. n. Single coccus showing 3 terminal and 1 lateral flagella. Figure S. Motile Streptococcus faecium var. mobilis var. n. Pair of cocci showing a single lateral flagellum. Figure 4. Motile Streptococcus faecium var. mobilis var. n. Pair of cocci showing 3 or more lateral flagella. Three strains showed curd at 48 hr, 6 at 1 week and 10 after 1 month. Ammonia was produced from arginine and slight hydrolysis was observed in esculin. Eight of the strains hydrolyzed starch on plates. The amount of hydrolysis varied, but visibly clear zones surrounding streaked areas were evident after plates were flooded with iodine. The reaction was much slower and weaker than that observed with Streptococcus bovis. None of the strains hydrolyzed sodium hippurate or gelatin. They failed to produce dextran on 10 per cent sucrose agar, nitrite was not produced from nitrate, and no indole or catalase was formed. Only 1 of the 11 strains showed tyrosine decarboxylase activity. The organisms were rather uniform in their ability to ferment carbohydrates (table 1). All strains fermented arabinose, xylose, ribose, rhamnose, glucose, fructose, mannose, galactose, maltose, lactose, sucrose, trehalose, cellobiose, melibiose, dextrin, glycerol (aerobic), and mannitol. The majority fermented raffinose, melezitose, starch, and salicin. One strain fermented sorbitol and none fermented glycerol (anaerobic) or inositol. Two strains tested produced lactic acid; over 89 per cent of the glucose fermented was converted to lactic acid. Optical rotation and water of crystallization showed that the lactic acid produced was the dextro form. DISCUSSION The motile streptococci described in this study conform to the enterococcus grouping established by Sherman (1937). They grew at 10 and 45 C, in 6.5 per cent sodium chloride and 40 per cent bile, and at ph 9.6. They reduced 0.1 per cent methylene blue in milk. During the last few years work has been reported which suggests that S. faecium (Orla- Jensen, 1919) should be given species rank distinct from that of S. faecalis and its variants (Skadhauge, 1950; Shattock, 1955; Barnes,

3 716 LANGSTON, GUTIERREZ, AND BOUMA [VOL. 80 TABLE 1 Final ph of broth cultures after 14 days'-incubation at 30 C* Culture ph Basal Substrate Reaction (Range) MpeHdu Arabinose Xylose Ribose Rhamnose Glucose Fructose Mannose Galactose Maltose Lactose Sucrose Trehalose Cellobiose Melibiose Raffinose ; Melezitose ; Starch ; Dextrin Salicin ; Glycerol (aerobic) Mannitol Sorbitol... 1+; * None of the strains fermented glycerol (anaerobically) or inositol. 1956; Lake, Deibel, and Niven, 1957). Distinguishing characteristics which separate the species are based upon various physiological tests, some of which are not too clear-cut. S. faecium has been shown to differ from S. faecalis by giving less reduction and acid in litmus milk, failing to grow on potassium tellurite agar with a final concentration of 1:2,500, showing weak or no reduction of tetrazolium, and giving variable or no fermentative reactions in mannitol, sorbitol, melezitose, a-methyl-d-glycoside, and glycerol (anaerobic), but always fermenting arabinose. The results of this study showed that the 11 motile strains are similar to S. faecium based upon many of the properties already established. When they were compared to typical strains of S. faecalis, it was found that they differed in their ability to ferment arabinose, xylose, melibiose, rhamnose, raffinose, and inulin and in their failure to ferment sorbitol. The fermentation of arabinose, melibiose, and mannitol is in general agreement with the work of Mundt et al., 1958; Mundt and Johnson, 1959; Lake et al., 1957; Barnes, 1956; and Orla-Jensen, 1919, although Mundt and Johnson's cultures showed some variations on all these substrates. All our strains fermented melibiose but none of those studied by Lake et al., and the majority of Mundt and Johnson's cultures failed to ferment this compound. The ability of our strains to ferment raffinose, inulin, and a-methyl-d-glucoside was consistent with the findings of Mundt and Johnson, although fewer of their strains gave positive reactions. Orla-Jensen (1919) reported that his strains of S. faecium usually failed to ferment inulin and those studied by Lake et al. (1957) failed to ferment a-methyl-d-glucoside. Our cultures showed greater tolerance to potassium tellurite than those studied by other workers. The concentration of tellurite employed is reported to inhibit completely the growth of S. faecium. The motile strains grew at the level used (1:2,500) but did not produce colonies as dark or as large as strains of S. faecalis. Mundt and Johnson's (1959) cultures also varied on this compound. Ten of their strains of S. faecalis failed to grow, and some of their strains of S. faecium gave weak growth. In our hands the test for reduction of tetrazolium appeared to be of little value in differentiating between S. faeciutm and S. faecalis unless close observations were made during the first few hours of incubation. Typical strains of S. faecalis showed faster reducing abilities until about 8 hr, at which time no differences in color were observed. Since Eh values were not obtained, it is possible that a greater amount of tetrazolium had been reduced to formazan, but this was not apparent when the cultures were extracted with butanol. All but one of the motile strains gave a bright red butanol layer. Seeley and Dain (1960) in a study of starch hydrolyzing streptococci pointed out that hydrolysis of starch, which usually refers to plates, and starch fermentation, which measures lactic acid from starch, are not necessarily correlated with the iodine test. That this is true was shown recently by Langston et al. (1960) who reported two strains of streptococci that fermented starch but failed to hydrolyze starch on plates. The results of the present study revealed that some of the motile strains were capable of fermenting starch and also hydrolyzing starch on

4 1960] MOTILE ENTEROCOCCI FROM GRASS SILAGE 717 plates. It should be stressed, however, that the ability of these strains to hydrolyze starch on plates was much weaker and slower than that of S. bovis. Although weak reactions were observed surrounding streaks, it is possible that the extent of hydrolysis would have been greater if a more favorable medium had been used. Other workers have reported strains of S. faecalis which ferment and hydrolyze starch (Mann, Masson, and Oxford, 1954; Auerbach and Felsenfeld, 1948). The strain studied by Auerbach and Felsenfeld, incidently, was a motile streptococcus isolated from human origin. S. faecalis has been shown to have greater tyrosine decarboxylase activity than S. faecium. When our strains were tested for decarboxylase activity, it was found that only one contained this enzyme system, and it is interesting to note that this strain also failed to ferment raffinose, a result which is in agreement with the work of Sharpe (1948). The motile cocci studied appear to constitute a rather well defined species and were different from S. faecalis in several characteristics. They differed in their ability to ferment arabinose, xylose, melibiose, rhamnose, raffinose, and inulin, failure to ferment sorbitol, generally slower acid production in litmus milk, rapid reduction of 0.1 per cent methylene blue in milk, slight differences in growth response on potassium tellurite, and ability to reduce tetrazolium and usual lack of active tyrosine decarboxylase systems. From the results obtained in this study and the published work of other investigators, it appears that S. faecium should be given species rank. Since motile strains in the genus Streptococcus have not been previously isolated from other than human and animal sources and none has been described that conforms to the S. faecium grouping, and because motility is an important taxonomic criterion, the authors suggest that the motile strains be given variety status and propose the name Streptococcusfaecium var. mobilis var. n. According to the International Code of Nomenclature of Bacteria and Viruses (Editorial Board, 1958), whenever a species is divided into varieties, the name of the species must also be reduced to a variety to include the type of species. Based on this ruling the type species should be designated as Streptococcus faecium var. faeciur var. n. SUMMARY A detailed description of motile streptococci isolated from grass silage fermentations has been presented. Interrelationships between Streptococcus faecalis and Streptococcus faecium were discussed. The authors concluded that S. faecium should be given species rank distinct from S. faecalis, and that motile streptococci which conform to the S. faecium grouping be given variety status and named Streptococcus faecium var. mobilis var. n., and the type species designated as Streptococcus faecium var. faecium var. n. REFERENCES AUERBACH, H., AND 0. FELSENFELD 1948 An unusual strain of Streptococcus isolated from subacute bacterial endocarditis. J. Bacteriol., 56, BARNES, E. M Tetrazolium reduction as a means of differentiating Streptococcus faecalis from Streptococcus faecium. J. Gen. Microbiol., 14, EDITORIAL BOARD 1958 International code of nomenclature of bacteria and viruses. Iowa State College Press, Ames, Iowa. HUGH, R Motile streptococci isolated from the oropharyngeal region. Can. J. Microbiol., 5, LAKE, D. E., R. H. DEIBEL, AND C. F. NIVEN, JR The identity of Streptococcus faecium. Bacteriol. Proc., 1957, 13. LANGSTON, C. W., AND C. BOUMA 1960a A study of the microorganisms from grass silage. I. The cocci. Appl. Microbiol., 8, LANGSTON, C. W., AND C. BOUMA 1960b A study of the microorganisms from grass silage. II. The lactobacilli. Appl. Microbiol., 8, LANGSTON, C. W., J. GUTIERREZ, AND C. BOUMA 1960 Catalase-producing strains of Streptococci. J. Bacteriol., 80, LEIFSON, E Staining, shape, and arrangement of bacterial flagella. J. Bacteriol., 62, MANN, S. O., F. M. MASSON, AND A. E. OXFORD 1954 Facultative anaerobic bacteria from the sheep's rumen. J. Gen. Microbiol., 10, MUNDT, J. O., AND A. H. JOHNSON 1959 Physiological properties of group D streptococci isolated from plants. Food Research, 24, MUNDT, J. O., A. H. JOHNSON, AND R. KHATCHIKIAN 1958 Incidence and nature

5 718 LANGSTON, GUTIERREZ, AND BOUMA [VOL. 80 of enterococci on plant material. Food Research, 23, ORLA-JENSEN, S The lactic acid bacteria. Mem. acad. roy. sci. Danemark, 5. O'TooLE, E Flagella staining of anaerobic bacilli. Stain Technol., 17, SEELEY, H. W., AND J. A. DAIN 1960 Starch hydrolyzing streptococci. J. Bacteriol., 79, SHARPE, M. E Some biochemical characteristics of group D streptococci isolated from infant faeces, with special reference to their decarboxylase activity. Proc. Soc. Appl. Bacteriol., 19th Ann. Conf., pp SHATTOCK, P. M. F The identification and classification of Streptococcus faecalis and some associated streptococci. Ann. inst. Pasteur, Lille, 7, SHERMAN, J. M The streptococci. Bacteriol. Rev., 1, SKADHAUGE, K Studies on the enterococci with special reference to the serological properties. Copenhagen: Einer Munksgaards. (Cited by Barnes (1956).)

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