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Factors affecting glucose uptake by the ruminal bacterium Bacteroides ruminicola

  • Applied Microbial and Cell Physiology
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Summary

Glucose uptake by whole cells of Bacteroides ruminicola B14 is constitutive. Potassium concentrations between 10 and 150 mm stimulated uptake over fourfold, while sodium had little effect on uptake. The involvement of potassium in glucose uptake by B. ruminicola was supported by strong inhibition of uptake by the ionophores valinomycin, lasalocid, and monensin. The electron transport inhibitor antimycin A had little effect on uptake, but menadione and acriflavine inhibited uptake by 30 and 48%, respectively. Potent inhibitors of uptake included oxygen, p-chloromercuribenzoate, HgCl2, and o-phenanthroline. Sodium arsenate decreased uptake by 40%, suggesting that a high-energy phosphate compound and possibly a binding protein may be involved in glucose uptake. The protonophores carbonyl cyanide m-chlorophenylhydrazone and 2,4-dinitrophenol inhibited glucose uptake by 37 and 22%, respectively. Little change in uptake activity was observed at extracellular pH values between 4.0 and 8.0. Excess (10 mm) cellobiose, maltose, and sucrose inhibited glucose uptake less than 15%. High levels (0.15% w/v) of p-coumaric acid and vanillin decreased uptake by 32 and 37%, respectively, while 0.15% ferulic acid decreased uptake by 15%.

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References

  • Berger EA, Heppel LA (1974) Different mechanisms energy coupling for the shock-sensitive and shock-resistant amino acid permeases of Escherichia coli. J Biol Chem 249:7747–7755

    Google Scholar 

  • Borneman WS, Akin DE, VanEseltine WP (1986) Effect of phenolic monomers on ruminal bacteria. Appl Environ Microbiol 52:1331–1339

    Google Scholar 

  • Bryant MP (1959) Bacterial species of the rumen. Bacteriol Rev 23:125–153

    Google Scholar 

  • Bryant MP, Small N, Buoma C, Chu H (1958) Bacteroides ruminicola, sp. and Succinimonas amylolytica, the new genus and species of succinic-acid producing anaerobic bacteria of the bovine rumen. J Bacteriol 76:15–23

    Google Scholar 

  • Caldwell DR, Arcand C (1974) Inorganic and metal-organic growth requirements of the genus Bacteroides. J Bacteriol 120:322–333

    Google Scholar 

  • Chen G, Russell JB (1989) Sodium-dependent transport of branched-chain amino acids by a monensin-sensitive ruminal peptostreptococcus. Appl Environ Microbiol 55:2658–2663

    Google Scholar 

  • Chen M, Wolin MJ (1979) Effect of monensin and lasalocid-sodium on the growth of methanogenic and rumen saccharolytic bacteria. Appl Environ Microbiol 38:72–77

    Google Scholar 

  • Chesson A, Stewart CS, Wallace RJ (1982) Influence of plant phenolic acids on growth and cellulolytic activity of rumen bacteria. Appl Environ Microbiol 44:597–603

    Google Scholar 

  • Czerkawski JW (1986) An introduction to rumen studies. Pergamon Press, New York

    Google Scholar 

  • Dawson KA, Boling JA (1987) Effects of potassium ion concentrations on the antimicrobial activities of ionophores against ruminal anaerobes. Appl Environ Microbiol 53:2363–2367

    Google Scholar 

  • Dawson KA, Preziosi MC, Caldwell DR (1979) Some effects of uncouplers and inhibitors on growth and electron transport in rumen bacteria. J Bacteriol 139:384–392

    Google Scholar 

  • Durand M, Kawashima R (1980) Influence of minerals in rumen microbial digestion. In: Ruckebusch Y, Thivend P (eds) Digestive physiology and metabolism in ruminants. MTP Press, Lancaster, UK, pp 375–408

    Google Scholar 

  • Franklund CV, Glass TL (1987) Glucose uptake by the cellulolytic ruminal anaerobe Bacteroides succinogenes. J Bacteriol 169:500–506

    Google Scholar 

  • Helaszak CT, White BA (1991) Cellobiose uptake and metabolism by Ruminococcus flavefaciens. Appl Environ Microbiol 57:64–68

    Google Scholar 

  • Hungate RE (1966) The rumen and its microbes. Academic Press, New York

    Google Scholar 

  • Hylemon PB, Young JL, Roadcap RF, Phibbs PV Jr (1977) Uptake and incorporation of glucose and mannose by whole cells of Bacteroides thetaiotaomicron. Appl Environ Microbiol 34:488–494

    Google Scholar 

  • Jung HG, Fahey GC Jr (1983) Nutritional implications of phenolic monomers and lignin: a review. J Anim Sci 57:206–219

    Google Scholar 

  • Kaback HR, Reeves JP, Short SA, Lombardi FJ (1974) Mechanisms of active transport in isolated bacterial membrane vesicles. XVIII. The mechanism of action of carbonylcyanide m-chlorophenylhydrazone. Arch Biochem Biophys 160:215–222

    Google Scholar 

  • Kanapka JA, Hamilton IR (1971) Fluoride inhibition of enolase activity in vivo and its relationship to the inhibition of glucose-6-P formation in Streptococcus salivarius. Arch Biochem Biophys 146:167–174

    Google Scholar 

  • Klein WL, Boyer PD (1972) Energization of active transport by Escherichia coli. J Biol Chem 247:7257–7265

    Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurements with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Martin SA, Akin DE (1988) Effect of phenolic monomers on the growth and β-glucosidase activity of Bacteroides ruminicola and on the carboxymethylcellulase, β-glucosidase, and xylanase activities of Bacteroides succinogenes. Appl Environ Microbiol 54:3019–3022

    Google Scholar 

  • Martin SA, Russell JB (1986) Phosphoenolpyruvate-dependent phosphorylation of hexoses by ruminal bacteria: evidence for the phosphotransferase transport system. Appl Environ Microbiol 52:1348–1352

    Google Scholar 

  • Martin SA, Russell JB (1987) Transport and phosphorylation of disaccharides by the ruminal bacterium Streptococcus bovis. Appl Environ Microbiol 53:2388–2393

    Google Scholar 

  • Martin SA, Russell JB (1988) Mechanisms of sugar transport in the rumen bacterium Selenomonas ruminantium. J Gen Microbiol 134:819–827

    Google Scholar 

  • Matin A, Veldkamp H (1978) Physiological basis of the selective advantage of a Spirillum sp. in a carbon-limited environment. J Gen Microbiol 105:187–197

    Google Scholar 

  • Nicholls DG (1982) Bioenergetics. An introduction to the chemiosmotic theory. Academic Press, New York, pp 25–39

    Google Scholar 

  • Poolman B, Hellingwerf KJ, Konings WN (1987) Regulation of the glutamate-glutamine transport system by intracellular pH in Streptococcus lactis. J Bacteriol 169:2272–2276

    Google Scholar 

  • Romano AH, Eberhard SJ, Dingle SL, McDowell TD (1970) Distribution of the phosphoenolpyruvate: glucose phosphotransferase system in bacteria. J Bacteriol 104:808–813

    Google Scholar 

  • Romano AH, Trifone JD, Brustolon M (1979) Distribution of the phosphoenolpyruvate: glucose phosphotransferase system in fermentative bacteria. J Bacteriol 139:93–97

    Google Scholar 

  • Russell JB (1985) Fermentation of cellodextrins by cellulolytic and noncellulolytic rumen bacteria. Appl Environ Microbiol 49:572–576

    Google Scholar 

  • Russell JB, Baldwin RL (1978) Substrate preferences in rumen bacteria: evidence of catabolite regulatory mechanisms. Appl Environ Microbiol 36:319–329

    Google Scholar 

  • Russell JB, Baldwin RL (1979) Comparison of substrate affinities among several rumen bacteria: a possible determinant of rumen bacterial competition. Appl Environ Microbiol 37:531–536

    Google Scholar 

  • Russell JB, Dombrowski DB (1980) Effect of pH on the efficiency of growth by pure cultures of rumen bacteria in continuous culture. Appl Environ Microbiol 39:604–610

    Google Scholar 

  • Russell JB, Strobel HJ (1989) Effect of ionophores on ruminal fermentation. Appl Environ Microbiol 55:1–6

    Google Scholar 

  • Russell JB, Wilson DB (1988) Potential opportunities and problems for genetically altered rumen microorganisms. J Nutr 118:271–279

    Google Scholar 

  • Russell JB, Sharp WM, Baldwin RL (1979) The effect of pH on maximum bacterial growth rate and its possible role as a determinant of bacterial competition in the rumen. J Anim Sci 48:251–255

    Google Scholar 

  • Russell JB, Strobel HJ, Driessen AJM, Konings WN (1988) Sodium-dependent transport of neutral amino acids by whole cells and membrane vesicles of Streptococcus bovis, a ruminal bacterium. J Bacteriol 170:3531–3536

    Google Scholar 

  • Sato Y, Noji S, Suzuki R, Taniguchi S (1989) Dual mechanism for stimulation of glutamate transport by potassium ions in Streptococcus mutants. J Bacteriol 171:4963–4966

    Google Scholar 

  • Shah HN, Collins MD (1983) Genus Bacteroides: a chemotaxonomical perspective. J Appl Bacteriol 55:403–416

    Google Scholar 

  • Shah HN, Collins MD (1990) Prevotella, a new genus to include Bacteroides melaninogenicus and related species formedly classified in the genus Bacteroides. Int J Syst Bacteriol 40:205–208

    Google Scholar 

  • Stewart CS, Bryant MP (1988) The rumen bacteria. In: Hobson PN (ed) The rumen microbial ecosystem. Elsevier Science Publishing Co, New York, pp 21–75

    Google Scholar 

  • Welsch CA, Lachance PA, Wasserman BP (1989) Dietary phenolic compounds: inhibition of Na+-dependent d-glucose uptake in rat intestinal brush border membrane vesicles. J Nutr 119:1698–1704

    Google Scholar 

  • Williams DK, Martin SA (1990) Xylose uptake by the ruminal bacterium Selenomonas ruminantium. Appl Environ Microbiol 56:1683–1688

    Google Scholar 

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Martin, S.A. Factors affecting glucose uptake by the ruminal bacterium Bacteroides ruminicola . Appl Microbiol Biotechnol 37, 104–108 (1992). https://doi.org/10.1007/BF00174212

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