Roles of motility, chemotaxis, and penetration through and growth in intestinal mucus in the ability of an avirulent strain of Salmonella typhimurium to colonize the large intestine of streptomycin-treated mice

Abstract

Previously, it had been shown that an avirulent strain of Salmonella typhimurium, SL5316, with wild-type lipopolysaccharide (LPS) was a far better colonizer of the streptomycin-treated CD-1 mouse large intestine, was far more motile, did not bind to mouse intestinal mucus nearly as well as, but penetrated through a layer of intestinal mucus in vitro far better than an almost isogenic LPS-deficient transductant, SL5325. In the present investigation, a nonflagellated transductant, SL5681, and a nonchemotactic transductant, SL5784, were isolated from SL5316 and tested for relative colonizing ability versus SL5316 (smooth) and SL5325 (rough) in streptomycin-treated mice. In addition, the Salmonella strains were tested for their ability to grow together in cecal intestinal mucus and in cecal luminal contents, for their tumbling and swimming activities after growth in cecal mucus, and for their ability to adhere to and travel through cecal mucus in vitro. The data show that the nonflagellated and nonchemotactic derivatives colonized large intestine nearly as well as their parent and were far better colonizers than the LPS-deficient mutant, that all the strains grew equally well in cecal mucus but did not grow in cecal luminal contents, and that cecal mucus-grown strains lost tumbling and swimming activities. Furthermore, the LPS-deficient strain adhered to cecal mucus far better but penetrated mucus far worse than did the nonflagellated transductant, the nonchemotactic transductant, and the parent. Thus, 2209

Growth of Salmonella typhimurium SL5319 and Escherichia coli F-18 in mouse cecal mucus: role of peptides and iron

“…If so, as S. typhimurium SL5319 penetrates the mucus layer and grows, it might effectively starve S. typhimurium SL5325 for iron, resulting in failure of S. typhimurium SL5325 to grow faster than the mucus is sloughed into the lumen. Since S. typhimurium SL5325 cannot grow in luminal contents [2], sloughed bacterial cells would be rapidly eliminated from the intestine in feces, resulting in the observed inability of S. typhimurium SL5325 to colonize when fed to mice along with S. typhimurium SL5319 [5]. In contrast, since E. coli F-18 cannot use enterochelin, when mice are fed E. coli F-18 and S. typhimurium SL5325, sufficient ferrienterochelin might be available tc the more slowly penetrating S. typhimurium SL5325 at all times, to allow ~ rowth and avoid washout in feces.…”

“…S. typhimurium SL5325, which colonizes the streptomycin-treated mouse large intestine when fed to mice alone, is a poor colotdzer when fed to mice together with either S. typhimurium SL5316 or S. typhimurium SL5319, a tetracycline resistant derivative of SL5316 which also contains wild-type LPS [1]. Recently, we reported that S. typhimurium SL5319 and SL5325 colonization requires growth in cecal mucus and that S. typhimurium SL5325 travels through cecal mucus very slowly relative to SL5319 [2]. Since mucus is in a dynamic state, constantly being synthesized by specialized goblet cells and sloughed into the lumen of the intestine [3], we hypothesized that S. typhimurium SL5319 is a better colonizer than S. typhimurium SL5325 because it quickly penetrates deep into the cecal mucus layer, depletes the nutrients that S. typhimurium SL5325 also needs for growth and thereby starves S. typhimurium SL5325, resulting in its rapid elimination.…”

Microbial biofilms and gastrointestinal diseases

“…Some bacteria can invade the mucus layer, and many intestinal microorganisms use these molecules as carbon, nitrogen, and energy sources (McCormick et al, 1988). The removal of carbohydrates and other components, such as sulfate, from the glycoprotein compromises its protective function (Schrager & Oates, 1978), particularly when the rate of mucus breakdown exceeds that of its synthesis and secretion.…”

Neither motility nor chemotaxis plays a role in the ability of Escherichia coli F-18 to colonize the streptomycin-treated mouse large intestine

“…Microscopic observation of E. coli F-18 grown in intestinal mucus in vitro. Jejunal, cecal, proximal colonic, midcolonic, and distal colonic mucus preparations (2 mg of protein per ml) were prepared from male CD-1 mice (5 to 8 weeks old) in HEPES-Hanks buffer, pH 7.4, as described previously (6,12,19 Spread of E. coli F-18 on L motility and mucus motility agars. Three E. coli F-18 colonies, isolated from the jejunum, cecum, proximal colon, midcolon, and distal colon of each streptomycin-treated mouse colonized for 8 days with E. coli F-18, were streaked on L agar containing streptomycin sulfate (100 ,ug/ml) and rifampin (50 ,ug/ml), incubated at 37°C for 18 h, transferred by toothpick to L motility agar, and incubated at 37°C for 18 h. At that time, the diameter of spread of each colony was measured in millimeters.…”

“…Moreover, motility also appears to be a colonization factor for Campylobacter jejuni in the lower small intestine, cecum, and colon of suckling mice (14) and in the conventional adult rabbit small intestine (3). However, motility/ chemotaxis does not appear to be important in the ability of Salmonella typhimurium to colonize the large intestines of conventional (4) or streptomycin-treated (12) mice, nor does motility appear to be important in the virulence of the organism (4,10). Here, we show that motility/chemotaxis also does not appear to be important in the ability of a human fecal Escherichia coli strain, F-18, to colonize the mouse large intestine.…”