The effects of fermentation acids on bacterial growth

Russell, James B.; Diez-Gonzalez, Francisco

doi:10.1016/s0065-2911(08)60017-x

Cited by 507Bacterial Genetics and BiotechnologyEscherichia coli research studiesProbiotics and Fermented Foods

The effects of fermentation acids on bacterial growth

Russell, James B., Diez-Gonzalez, Francisco·1997·Advances in Microbial Physiology

DOI 10.1016/s0065-2911(08)60017-x

Open this paper in CoChat — free account

Abstract

Anaerobic habitats often have low pH and high concentrations of fermentation acids, and these conditions can inhibit the growth of many bacteria. The toxicity of fermentation acids at low pH was traditionally explained by an uncoupling mechanism. Undissociated fermentation acids can pass across the cell membrane and dissociate in the more alkaline interior, but there is little evidence that they can act in a cyclic manner to dissipate protonmotive force. Fermentation acid dissociation in the more alkaline interior causes an accumulation of the anionic species, and this accumulation is dependent on the pH gradient (delta pH) across the membrane. Fermentation acid-resistant bacteria have low delta pH and are able to generate ATP and grow with a low intracellular pH. Escherichia coli O157:H7 is able to decrease its intracellular pH to 6.1 before growth ceases, but this modest decrease in delta pH can only partially counteract the toxic effect of fermentation anion accumulation. Fermentation acid-resistant bacteria are in most cases Gram-positive bacteria with a high intracellular potassium concentration, and even acid-sensitive bacteria like E. coli K-12 have increased potassium levels when fermentation acids are present. Intracellular potassium provides a counteraction for fermentation acid anions, and allows bacteria to tolerate even greater amounts of fermentation anions. The delta pH-mediated anion accumulation provides a mechanistic explanation for the effect of fermentation acids on microbial ecology and metabolism.

Integrity signals

Registry

Crossref · 10.1016/s0065-2911(08)60017-x

Cites

129 of 129 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

At low pH, increased acetic acid could create a stressful environment for most microorganisms because its higher pKa (4.76) compared to silage pH allows nearly all acetate to be undissociated.
“At low pH, an increase in acetic acid could create a stressful environment for most microorganisms, as the higher pKa of acetic acid (4.76) compared to the pH of the silage allows nearly all acetate to be in its undissociated form [67].”
From Dynamic succession of microbiota during ensiling of whole plant corn following inoculation with Lactobacillus buchneri and Lactobacillus hilgardii alone or in combination. (2019) · cites this paper as [67]
Acetic acid could enter microbial cells, dissociate, decrease intracellular pH, cause energy expenditure to maintain physiological pH, and eventually kill cells unable to adapt.
“Acetic acid could then easily enter microbial cells, dissociate, and decrease the intracellular pH associated with notable energy expenditure to maintain physiological pH values, eventually killing cells unable to adapt.”
From Dynamic succession of microbiota during ensiling of whole plant corn following inoculation with Lactobacillus buchneri and Lactobacillus hilgardii alone or in combination. (2019) · cites this paper as [67]

Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism
MITCHELL, P. (1961) · Nature · doi:10.1038/191144a0 · Cited by 4,704 · see citing works
The Rumen and Its Microbes
Hungate, R. E. (2013) · Elsevier eBooks · doi:10.1016/c2013-0-12555-x · Cited by 3,060 · see citing works
MICROBIAL ECOLOGY OF THE GASTROINTESTINAL TRACT
Savage, D. C. (1977) · Annual Review of Microbiology · doi:10.1146/annurev.mi.31.100177.000543 · Cited by 2,436 · see citing works
Modern Food Microbiology
Jay, J. M. (1995) · Food science text series · doi:10.1007/978-1-4615-7476-7 · Cited by 2,398 · see citing works
Chapter IV A Roll Tube Method for Cultivation of Strict Anaerobes
Hungate, R. E. (1969) · Methods in microbiology · doi:10.1016/s0580-9517(08)70503-8 · Cited by 1,355 · see citing works
Clostridium difficile Colitis
Kelly, C. P., Pothoulakis, C., & LaMont, J. T. (1994) · New England Journal of Medicine · doi:10.1056/nejm199401273300406 · Cited by 1,320 · see citing works
Digestion and metabolism in the ruminant : proceedings of the IV International Symposium on Ruminant Physiology, Sydney, Australia, August 1974
McDonald, I. W., & Warner, A. C. I. (1975) · Cited by 1,169 · see citing works
THE ANAEROBIC MESOPHILIC CELLULOLYTIC BACTERIA
Hungate, R. E. (1950) · Bacteriological Reviews · doi:10.1128/br.14.1.1-49.1950 · Cited by 1,094 · see citing works
Regulation of cytoplasmic pH in bacteria
Booth, I. R. (1985) · Microbiological Reviews · doi:10.1128/mr.49.4.359-378.1985 · Cited by 1,071 · see citing works
Regulation of cytoplasmic pH in bacteria.
Booth, I. R. (1985) · Microbiological reviews · doi:10.1128/mmbr.49.4.359-378.1985 · Cited by 1,044 · see citing works
Modern Food Microbiology
Jay, J. M. (1992) · Springer eBooks · doi:10.1007/978-94-011-6480-1 · Cited by 1,006 · see citing works
Digestion and metabolism in the ruminant
Ziołecki, A. (1976) · Livestock Production Science · doi:10.1016/0301-6226(76)90025-7 · Cited by 998 · see citing works
Microbiology of Fermented Foods
Wood, B. J. B. (1997) · Springer eBooks · doi:10.1007/978-1-4613-0309-1 · Cited by 970 · see citing works
A selective medium for the isolation and enumeration of oral and fecal lactobacilli
Rogosa, M., Mitchell, J. A., & Wiseman, R. F. (1951) · Journal of Bacteriology · doi:10.1128/jb.62.1.132-133.1951 · Cited by 653 · see citing works
Normal Indigenous Intestinal Flora
Finegold, S. M., Sutter, V. L., & Mathisen, G. E. (1983) · Elsevier eBooks · doi:10.1016/b978-0-12-341280-5.50007-0 · Cited by 618 · see citing works
Mechanisms of acid resistance in enterohemorrhagic Escherichia coli
Lin, J.-S., Smith, M. P., Chapin, K. C., Baik, H. S., Bennett, G. N., & Foster, J. W. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.9.3094-3100.1996 · Cited by 574 · see citing works
Another explanation for the toxicity of fermentation acids at low pH: anion accumulation versus uncoupling
Russell, J. B. (1992) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1992.tb04990.x · Cited by 573 · see citing works
Self-citation
Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli
Lin, J.-S., Lee, I. S., Frey, J., Slonczewski, J. L., & Foster, J. W. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.14.4097-4104.1995 · Cited by 569 · see citing works
The capacity of hydrogenotrophic anaerobic bacteria to compete for traces of hydrogen depends on the redox potential of the terminal electron acceptor.
Cord-Ruwisch, R., Seitz, H.-J., & Conrad, R. (1988) · Archives of Microbiology · doi:10.1007/bf00411655 · Cited by 549 · see citing works
Sulfate Reducers Can Outcompete Methanogens at Freshwater Sulfate Concentrations
Lovley, D. R., & Klug, M. J. (1983) · Applied and Environmental Microbiology · doi:10.1128/aem.45.1.187-192.1983 · Cited by 531 · see citing works
The fermentation pathways of Escherichia coli
Clark, D. P. (1989) · FEMS Microbiology Reviews · doi:10.1016/0168-6445(89)90033-8 · Cited by 506 · see citing works
Bacterial lactate dehydrogenases
Garvie, E. I. (1980) · Microbiological Reviews · doi:10.1128/mr.44.1.106-139.1980 · Cited by 497 · see citing works
Basic Food Microbiology
Banwart, G. J. (1989) · Springer eBooks · doi:10.1007/978-1-4684-6453-5 · Cited by 478 · see citing works
Osmoadaptation in Bacteria
Galinski, E. A. (1995) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/s0065-2911(08)60148-4 · Cited by 470 · see citing works
Effect of pH on the efficiency of growth by pure cultures of rumen bacteria in continuous culture
Russell, J. B., & Dombrowski, D. B. (1980) · Applied and Environmental Microbiology · doi:10.1128/aem.39.3.604-610.1980 · Cited by 459 · see citing works
Self-citation
pH homesstasis in bacteria
Padan, E., Zilberstein, D., & Schuldiner, S. (1981) · Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes · doi:10.1016/0304-4157(81)90004-6 · Cited by 435 · see citing works
Human intestinal microflora in health and disease
(1985) · Food and Chemical Toxicology · doi:10.1016/0278-6915(85)90079-1 · Cited by 429 · see citing works
Bioenergetics of lactic acid bacteria: cytoplasmic pH and osmotolerance
Kashket, E. R. (1987) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1987.tb02463.x · Cited by 412 · see citing works
The silage fermentation
Woolford, M. K., & Pahlow, G. (1998) · Springer eBooks · doi:10.1007/978-1-4613-0309-1_3 · Cited by 399 · see citing works
The Effect of Food Preservatives on pH Homeostasis in Escherichia coli
SALMOND, C. V., Kroll, R. G., & Booth, I. R. (1984) · Microbiology · doi:10.1099/00221287-130-11-2845 · Cited by 398 · see citing works
Human Intestinal Microflora in Health and Disease
(1983) · Elsevier eBooks · doi:10.1016/c2012-0-01555-4 · Cited by 395 · see citing works
Transient accumulation of potassium glutamate and its replacement by trehalose during adaptation of growing cells of Escherichia coli K-12 to elevated sodium chloride concentrations
Dinnbier, U., Limpinsel, E., Schmid, R., & Bakker, E. P. (1988) · Archives of Microbiology · doi:10.1007/bf00408306 · Cited by 392 · see citing works
THE ANAEROBIC MESOPHILIC CELLULOLYTIC BACTERIA 1
Hungate, R. E. (1950) · Bacteriological Reviews · doi:10.1128/mmbr.14.1.1-49.1950 · Cited by 369 · see citing works
Growth and survival of Escherichia coli O157:H7 under acidic conditions
Conner, D. E., & KOTROLA, J. S. (1995) · Applied and Environmental Microbiology · doi:10.1128/aem.61.1.382-385.1995 · Cited by 341 · see citing works
Influence of Acidosis on Rumen function
Slyter, L. L. (1976) · Journal of Animal Science · doi:10.2527/jas1976.434910x · Cited by 339 · see citing works
Cation Transport in Escherichia coli
Epstein, W., & Schultz, S. G. (1965) · The Journal of General Physiology · doi:10.1085/jgp.49.2.221 · Cited by 335 · see citing works
Competition between sulfate-reducing and methanogenic bacteria for H2 under resting and growing conditions
Robinson, J. A., & Tiedje, J. M. (1984) · Archives of Microbiology · doi:10.1007/bf00425803 · Cited by 310 · see citing works
Escherichia coli O157: H7 Infection in Humans
Su, C., & Brandt, L. J. (1995) · Annals of Internal Medicine · doi:10.7326/0003-4819-123-9-199511010-00009 · Cited by 309 · see citing works
THE PROTON MOTIVE FORCE IN BACTERIA: A CRITICAL ASSESSMENT OF METHODS
Kashket, E. R. (1985) · Annual Review of Microbiology · doi:10.1146/annurev.mi.39.100185.001251 · Cited by 302 · see citing works
Osmoregulation in Escherichia coli by accumulation of organic osmolytes: betaines, glutamic acid, and trehalose
Larsen, P. I., Sydnes, L. K., Landfald, B., & Str�m, A. R. (1987) · Archives of Microbiology · doi:10.1007/bf00492896 · Cited by 299 · see citing works
Factors Affecting the Cellulolytic Activity of Rumen Contents
Stewart, C. S. (1977) · Applied and Environmental Microbiology · doi:10.1128/aem.33.3.497-502.1977 · Cited by 291 · see citing works
Regulation of Lactate Production in Streptococcus bovis: A Spiraling Effect That Contributes to Rumen Acidosis
Russell, J. B., & Hino, T. (1985) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(85)81017-1 · Cited by 290 · see citing works
Self-citation
Proton/sodium ion antiport in Escherichia coli
West, I. C., & Mitchell, P. D. (1974) · Biochemical Journal · doi:10.1042/bj1440087 · Cited by 272 · see citing works
RESISTANCE OF THE MOUSE'S INTESTINAL TRACT TO EXPERIMENTAL SALMONELLA INFECTION
Bohnhoff, M., Miller, C. P., & Martin, W. R. (1964) · The Journal of Experimental Medicine · doi:10.1084/jem.120.5.805 · Cited by 246 · see citing works
Microbiology of food fermentations
Pederson, C. S. (1979) · Cited by 245 · see citing works
Livestock feeds and feeding
Orr, R. M. (1988) · Elsevier eBooks · doi:10.1016/b978-0-408-03060-1.50019-9 · Cited by 242 · see citing works
Bacterial lactate dehydrogenases.
Garvie, E. I. (1980) · Microbiological Reviews · doi:10.1128/mmbr.44.1.106-139.1980 · Cited by 241 · see citing works
The effect of pH on ruminal methanogenesis
Kessel, J. A. S. V., & Russell, J. B. (1996) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.1996.tb00319.x · Cited by 236 · see citing works
Self-citation
Livestock feeds and feeding
Church, D. C. (1977) · Andalas University Repository (Andalas University) · Cited by 235 · see citing works
Effects of lactulose and other laxatives on ileal and colonic pH as measured by a radiotelemetry device
Bown, R. L., Gibson, J., Sladen, G. E., Hicks, B. D., & Dawson, A. M. (1974) · Gut · doi:10.1136/gut.15.12.999 · Cited by 232 · see citing works
Transport of lactate and acetate through the energized cytoplasmic membrane of Escherichia coli
Axe, D. D., & Bailey, J. E. (1995) · Biotechnology and Bioengineering · doi:10.1002/bit.260470103 · Cited by 223 · see citing works
Influence of pH and undissociated butyric acid on the production of acetone and butanol in batch cultures of Clostridium acetobutylicum
Monot, F., Engasser, J., & Petitdemange, H. (1984) · Applied Microbiology and Biotechnology · doi:10.1007/bf00454381 · Cited by 216 · see citing works
Influence of temperature on energetics of hydrogen metabolism in homoacetogenic, methanogenic, and other anaerobic bacteria
Conrad, R., & Wetter, B. (1990) · Archives of Microbiology · doi:10.1007/bf00291281 · Cited by 214 · see citing works
The internal pH of Clostridium acetobutylicum and its effect on the shift from acid to solvent formation
Gottwald, M., & Gottschalk, G. (1985) · Archives of Microbiology · doi:10.1007/bf00414766 · Cited by 201 · see citing works
The effect of pH on ruminal methanogenesis
Kessel, J. V. (1996) · FEMS Microbiology Ecology · doi:10.1016/0168-6496(96)00030-x · Cited by 198 · see citing works
RESISTANCE OF THE MOUSE'S INTESTINAL TRACT TO EXPERIMENTAL SALMONELLA INFECTION
Bohnhoff, M., Miller, C. P., & Martin, W. R. (1964) · The Journal of Experimental Medicine · doi:10.1084/jem.120.5.817 · Cited by 196 · see citing works
Intracellular Conditions Required for Initiation of Solvent Production by Clostridium acetobutylicum
Terracciano, J., & Kashket, E. R. (1986) · Applied and Environmental Microbiology · doi:10.1128/aem.52.1.86-91.1986 · Cited by 186 · see citing works
Microbiological and physiological changes associated with acute indigestion in sheep.
Hungate, R. E., Dougherty, R. W., Bryant, M. P., & Cello, R. M. (1952) · PubMed · Cited by 176 · see citing works
The ability of Escherichia coli O157:H7 to decrease its intracellular pH and resist the toxicity of acetic acid
Diez‐Gonzalez, F., & Russell, J. B. (1997) · Microbiology · doi:10.1099/00221287-143-4-1175 · Cited by 168 · see citing works
Self-citation
A Proposed Mechanism of Monensin Action in Inhibiting Ruminant Bacterial Growth: Effects on Ion Flux and Protonmotive Force
Russell, J. B. (1987) · Journal of Animal Science · doi:10.2527/jas1987.6451519x · Cited by 163 · see citing works
Self-citation
Methane production in contrasting wetland sites: Response to organic‐chemical components of peat and to sulfate reduction
Yavitt, J. B., & Lang, G. E. (1990) · Geomicrobiology Journal · doi:10.1080/01490459009377876 · Cited by 160 · see citing works
The clostridia and biotechnology.
Woods, D. (1993) · PubMed · Cited by 155 · see citing works
Regulation of solute transport in streptococci by external and internal pH values.
Poolman, B., Driessen, A. J., & Konings, W. (1987) · Microbiological reviews · doi:10.1128/mmbr.51.4.498-508.1987 · Cited by 154 · see citing works
Generation of an electrochemical proton gradient in bacteria by the excretion of metabolic end products
Michels, P. A. M., Michels, J. P. J., Boonstra, J., & Konings, W. N. (1979) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1979.tb03339.x · Cited by 142 · see citing works
Role of volatile fatty acids in colonization resistance to Clostridium difficile
Rolfe, R. D. (1984) · Infection and Immunity · doi:10.1128/iai.45.1.185-191.1984 · Cited by 142 · see citing works
Organic Nutrition of Chemolithotrophic Bacteria
Matin, A. (1978) · Annual Review of Microbiology · doi:10.1146/annurev.mi.32.100178.002245 · Cited by 139 · see citing works
Generation of an electrochemical proton gradient in bacteria by the excretion of metabolic end products
Michels, P. A. M. (1979) · FEMS Microbiology Letters · doi:10.1016/0378-1097(79)90208-8 · Cited by 139 · see citing works
Fermentation by the human large intestine microbial community in an in vitro semicontinuous culture system
Miller, T. L., & Wolin, M. J. (1981) · Applied and Environmental Microbiology · doi:10.1128/aem.42.3.400-407.1981 · Cited by 136 · see citing works
Comparison of Maintenance Energy Expenditures and Growth Yields Among Several Rumen Bacteria Grown on Continuous Culture
Russell, J. B., & Baldwin, R. L. (1979) · Applied and Environmental Microbiology · doi:10.1128/aem.37.3.537-543.1979 · Cited by 131 · see citing works
Self-citation
Regulation of solute transport in streptococci by external and internal pH values
Poolman, B., Driessen, A. J. M., & Konings, W. N. (1987) · Microbiological Reviews · doi:10.1128/mr.51.4.498-508.1987 · Cited by 130 · see citing works
Characterization of Methanosarcina barkeri MST and 227, Methanosarcina mazei S-6T, and Methanosarcina vacuolata Z-761T
Maestrojuan, G. M., & Boone, D. R. (1991) · International Journal of Systematic Bacteriology · doi:10.1099/00207713-41-2-267 · Cited by 130 · see citing works
Effects of potassium ions on the electrical and pH gradients across the membrane of Streptococcus lactis cells
Kashket, E. R., & Barker, S. L. R. (1977) · Journal of Bacteriology · doi:10.1128/jb.130.3.1017-1023.1977 · Cited by 125 · see citing works
Effect of Lactulose on the Composition and Metabolic Activity of the Human Faecal Flora
Terada, A., Hiroyoshi, H. A. R. A., Kataoka, M., & MITSUOKA, T. (1992) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v5i1.7768 · Cited by 123 · see citing works
Comparison of Substrate Affinities Among Several Rumen Bacteria: a Possible Determinant of Rumen Bacterial Competition
Russell, J. B., & Baldwin, R. L. (1979) · Applied and Environmental Microbiology · doi:10.1128/aem.37.3.531-536.1979 · Cited by 119 · see citing works
Self-citation
Volatile Fatty Acids and the Inhibition of Escherichia coli Growth by Rumen Fluid
Wolin, M. J. (1969) · Applied Microbiology · doi:10.1128/am.17.1.83-87.1969 · Cited by 118 · see citing works
Intestinal Flora of Infants
Cooperstock, M. S., & Zedd, A. J. (1983) · Elsevier eBooks · doi:10.1016/b978-0-12-341280-5.50010-0 · Cited by 117 · see citing works
Biochemistry and Genetics of Actinomycete Cellulases
Wilson, D. B. (1992) · Critical Reviews in Biotechnology · doi:10.3109/07388559209069187 · Cited by 113 · see citing works
Effects of pH and Repellent Tactic Stimuli on Protein Methylation Levels in Escherichia coli
Slonczewski, J. L., Macnab, R. M., Alger, J. R., & Castle, A. M. (1982) · Journal of Bacteriology · doi:10.1128/jb.152.1.384-399.1982 · Cited by 111 · see citing works
Effect of Lactulose on the Composition and Metabolic Activity of the Human Faecal Flora
Terada, A., Hiroyoshi, H. A. R. A., Kataoka, M., & MITSUOKA, T. (1992) · Microbial Ecology in Health and Disease · doi:10.3109/08910609209141303 · Cited by 111 · see citing works
Microbiology of foods
Ayres, J. C., Mundt, J. O., & Sandine, W. E. (1980) · W.H. Freeman eBooks · Cited by 109 · see citing works
The effects of spatial and temporal variations in acetate and sulfate on methane cycling in two Michigan peatlands
Shannon, R. D., & White, J. R. (1996) · Limnology and Oceanography · doi:10.4319/lo.1996.41.3.0435 · Cited by 109 · see citing works
Molecular Responses of Microbes to Environmental pH stress
Hall, H. K., Karem, K. L., & Foster, J. W. (1995) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/s0065-2911(08)60147-2 · Cited by 106 · see citing works
Role of the Intestinal Microflora in Host Defense against Infection
Hentges, D. J. (1983) · Elsevier eBooks · doi:10.1016/b978-0-12-341280-5.50020-3 · Cited by 105 · see citing works
The effect of absorption on the acidity of rumen contents
Ash, R. W., & Dobson, A. (1963) · The Journal of Physiology · doi:10.1113/jphysiol.1963.sp007240 · Cited by 104 · see citing works
Mu d-directed lacZ fusions regulated by low pH in Escherichia coli
Slonczewski, J. L., Gonzalez, T. N., Bartholomew, F. M., & Holt, N. J. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.7.3001-3006.1987 · Cited by 103 · see citing works
Construction of an Escherichia coli strain unable to synthesize putrescine, spermidine, or cadaverine: characterization of two genes controlling lysine decarboxylase
Tabor, H., Hafner, E. W., & Tabor, C. W. (1980) · Journal of Bacteriology · doi:10.1128/jb.144.3.952-956.1980 · Cited by 102 · see citing works
The relationship between intracellular pH, the pH gradient and potassium transport in Escherichia coli
Kroll, R. G., & Booth, I. R. (1983) · Biochemical Journal · doi:10.1042/bj2160709 · Cited by 97 · see citing works
FERMENTATION OF GLUCOSE BY SUSPENSIONS OF ESCHERICHIA COLI
Stokes, J. L. (1949) · Journal of Bacteriology · doi:10.1128/jb.57.2.147-158.1949 · Cited by 95 · see citing works
The Acetone-Butanol-Ethanol Fermentation
Awang, G., Jones, G. A., Ingledew, W. M., & Kropinski, A. M. (1988) · CRC Critical Reviews in Microbiology · doi:10.3109/10408418809104464 · Cited by 94 · see citing works
Microbial diversity of Minnesota peatlands
Williams, R. T., & Crawford, R. L. (1983) · Microbial Ecology · doi:10.1007/bf02097737 · Cited by 90 · see citing works
Lactic acid excretion by Streptococcus mutans
Dashper, S. G., & Reynolds, E. C. (1996) · Microbiology · doi:10.1099/13500872-142-1-33 · Cited by 90 · see citing works
Electrogenic L-malate transport by Lactobacillus plantarum: a basis for energy derivation from malolactic fermentation
Olsen, E., Russell, J. B., & Henick‐Kling, T. (1991) · Journal of Bacteriology · doi:10.1128/jb.173.19.6199-6206.1991 · Cited by 89 · see citing works
Self-citation
Isolation and Characterization of Methanobacterium espanolae sp. nov., a Mesophilic, Moderately Acidiphilic Methanogen
Patel, G. B., Sprott, G. D., & Fein, J. E. (1990) · International Journal of Systematic Bacteriology · doi:10.1099/00207713-40-1-12 · Cited by 88 · see citing works
Interactions between the bacterial species of the rumen
Wolin, M. J. (1975) · Medical Entomology and Zoology · Cited by 86 · see citing works
Carbohydrate Fermentation
Wolin, M. J., & Miller, T. L. (1983) · Elsevier eBooks · doi:10.1016/b978-0-12-341280-5.50013-6 · Cited by 85 · see citing works
The internal pH of Acetobacterium wieringae and Acetobacter aceti during growth and production of acetic acid
Menzel, U., & Gottschalk, G. (1985) · Archives of Microbiology · doi:10.1007/bf00414767 · Cited by 83 · see citing works
Acetone/butanol/ethanol fermentation
SPIVEY, M. J. (1978) · OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) · Cited by 80 · see citing works
Cloning of genes responsible for acetic acid resistance in Acetobacter aceti
Fukaya, M., Takemura, H., Okumura, H., Kawamura, Y., Horinouchi, S., & Beppu, T. (1990) · Journal of Bacteriology · doi:10.1128/jb.172.4.2096-2104.1990 · Cited by 79 · see citing works
Intracellular pH of acid-tolerant ruminal bacteria
Russell, J. B. (1991) · Applied and Environmental Microbiology · doi:10.1128/aem.57.11.3383-3384.1991 · Cited by 76 · see citing works
Self-citation
Resistance of Streptococcus bovis to acetic acid at low pH: relationship between intracellular pH and anion accumulation
Russell, J. B. (1991) · Applied and Environmental Microbiology · doi:10.1128/aem.57.1.255-259.1991 · Cited by 75 · see citing works
Self-citation
Lactic Acid Translocation: Terminal Step in Glycolysis by Streptococcus faecalis
Harold, F. M., & Levin, E. J. (1974) · Journal of Bacteriology · doi:10.1128/jb.117.3.1141-1148.1974 · Cited by 71 · see citing works
Cellobiose versus glucose utilization by the ruminal bacterium Ruminococcus albus
Thurston, B., Dawson, K. A., & Strobel, H. J. (1993) · Applied and Environmental Microbiology · doi:10.1128/aem.59.8.2631-2637.1993 · Cited by 71 · see citing works
Comparative assessment of bacterial inoculation and propionic acid treatment of aerobic stability and microbial populations of ensiled high-moisture ear corn.
Sebastian, S., Phillip, L. E., Fellner, V, & Idziak, E. S. (1996) · Journal of Animal Science · doi:10.2527/1996.742447x · Cited by 69 · see citing works
Shigella, indigenous flora interactions in mice
Maier, B. R., Onderdonk, A. B., Baskett, R. C., & Hentges, D. J. (1972) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/25.12.1433 · Cited by 65 · see citing works
The effect of extracellular pH and lactic acid on pH homeostasis inLactococcus lactis andStreptococcus bovis
Cook, G. M., & Russell, J. B. (1994) · Current Microbiology · doi:10.1007/bf01571059 · Cited by 63 · see citing works
Self-citation
Acetogenic capacities and the anaerobic turnover of carbon in a kansas prairie soil
Wagner, C., Griesshammer, A., & Drake, H. L. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.2.494-500.1996 · Cited by 61 · see citing works
Effect of extracellular pH on growth and proton motive force of Bacteroides succinogenes, a cellulolytic ruminal bacterium
Russell, J. B. (1987) · Applied and Environmental Microbiology · doi:10.1128/aem.53.10.2379-2383.1987 · Cited by 59 · see citing works
Self-citation
Toxicity of volatile fatty acids at rumen pH prevents enrichment ofEscherichia coli by sorbitol in rumen contents
Wallace, R. J., Falconer, M. L., & Bhargava, P. K. (1989) · Current Microbiology · doi:10.1007/bf01570101 · Cited by 58 · see citing works
Comparison between in vivo and in vitro enzyme activities in continuous and batch fermentations of Clostridium acetobutylicum
H�semann, M. W., & Papoutsakis, E. (1989) · Applied Microbiology and Biotechnology · doi:10.1007/bf00255364 · Cited by 51 · see citing works
Uncoupler-resistant mutants of bacteria.
Krulwich, T., Quirk, P. G., & Guffanti, A. (1990) · Microbiological reviews · doi:10.1128/mmbr.54.1.52-65.1990 · Cited by 51 · see citing works
Isolation and characterization of uncoupler-resistant mutants of Bacillus subtilis
Guffanti, A. A., Clejan, S., Falk, L. H., Hicks, D. B., & KRULWICH, T. A. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.10.4469-4478.1987 · Cited by 49 · see citing works
Uncoupler-resistant mutants of bacteria
KRULWICH, T. A., Quirk, P. G., & Guffanti, A. A. (1990) · Microbiological Reviews · doi:10.1128/mr.54.1.52-65.1990 · Cited by 49 · see citing works
ATPase-dependent energy spilling by the ruminal bacterium, Streptococcus bovis
Russell, J. B., & Strobel, H. J. (1990) · Archives of Microbiology · doi:10.1007/bf00249009 · Cited by 48 · see citing works
Self-citation
Evolution of a Microbial Ecologist
Hungate, R. E. (1979) · Annual Review of Microbiology · doi:10.1146/annurev.mi.33.100179.000245 · Cited by 45 · see citing works
Effects of carbonylcyanide-m-chlorophenylhydrazone (CCCP) and acetate on Escherichia coli O157:H7 and K-12: uncoupling versus anion accumulation
Diez‐Gonzalez, F. (1997) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(97)00140-7 · Cited by 42 · see citing works
Self-citation
Effects of carbonylcyanide-m-chlorophenylhydrazone (CCCP) and acetate on Escherichia coli O157:H7 and K-12: uncoupling versus anion accumulation
Diez‐Gonzalez, F., & Russell, J. B. (2006) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1997.tb10396.x · Cited by 37 · see citing works
Self-citation
Effects of potassium ions on proton motive force in Rhodobacter sphaeroides
Abee, T., Hellingwerf, K. J., & Konings, W. N. (1988) · Journal of Bacteriology · doi:10.1128/jb.170.12.5647-5653.1988 · Cited by 36 · see citing works
Microbial production of butanol acetone
Bahl, H., & Gottschalk, G. (1988) · Cited by 33 · see citing works
Role of volatile fatty acids in colonization resistance to Clostridium difficile in gnotobiotic mice
Su, W. J., Waechter, M., Bourlioux, P., Dolegeal, M., Fourniat, J., & Mahuzier, G. (1987) · Infection and Immunity · doi:10.1128/iai.55.7.1686-1691.1987 · Cited by 32 · see citing works
Carrier-mediated acetate transport in Acetobacterium woodii
Boenigk, R., D�rre, P., & Gottschalk, G. (1989) · Archives of Microbiology · doi:10.1007/bf00425492 · Cited by 28 · see citing works
Microbiology of animals and animal products
Hird, D. W. (1992) · Preventive Veterinary Medicine · doi:10.1016/0167-5877(92)90059-o · Cited by 23 · see citing works
Associations of Indigenous Microorganisms with Gastrointestinal Epithelial Surfaces
Savage, D. C. (1983) · Elsevier eBooks · doi:10.1016/b978-0-12-341280-5.50009-4 · Cited by 22 · see citing works
Mutants of Bacillus species isolated on the basis of protonophore resistance are deficient in fatty acid desaturase activity
Dunkley, E. A., Clejan, S., & KRULWICH, T. A. (1991) · Journal of Bacteriology · doi:10.1128/jb.173.24.7750-7755.1991 · Cited by 21 · see citing works
Active Transport: Membrane Vesicles, Bioenergetics, Molecules, and Mechanisms
Kaback, H. R. (1990) · Elsevier eBooks · doi:10.1016/b978-0-12-307212-2.50010-7 · Cited by 21 · see citing works
Microbiology of animals and animal products
Woolcock, J. B. (1991) · Cited by 14 · see citing works
The effect of ionophores on proton flux in the ruminal bacterium,streptococcus bovis
Kajikawa, H., & Russell, J. B. (1992) · Current Microbiology · doi:10.1007/bf01577229 · Cited by 8 · see citing works
Self-citation
[Effect of the activity of primary proton pumps on the growth of Escherichia coli in the presence of acetate].
Gv, S., & On, O. (1989) · PubMed · Cited by 8 · see citing works
Clostridium difficile
Eagle, K., & Phillips, D. M. (1994) · New England Journal of Medicine · doi:10.1056/nejm199401273300405 · Cited by 7 · see citing works
Electrochemical potential and membrane properties of methanogenic bacteria
Sprott, G., & Jarrell, K. (1984) · NPARC · Cited by 3 · see citing works

Flagged first, then by citations

1 of the 130 references couldn’t be matched to a known paper.

Sorted by citations

Probiotic Mechanisms of Action
Bermúdez-Brito, M., Plaza‐Díaz, J., Muñoz‐Quezada, S., Gómez‐Llorente, C., & Gil, Á. (2012) · Annals of Nutrition and Metabolism · doi:10.1159/000342079 · Cited by 1,276 · see citing works
The Acetate Switch
Wolfe, A. J. (2005) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.69.1.12-50.2005 · Cited by 1,233 · see citing works
The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women
Romero, R., Hassan, S. S., Gajer, P., Tarca, A. L., Fadrosh, D. W., Nikita, L., Galuppi, M., Lamont, R. F., Chaemsaithong, P., Miranda, J., et al. (2014) · Microbiome · doi:10.1186/2049-2618-2-4 · Cited by 852 · see citing works
From the gut to the peripheral tissues: the multiple effects of butyrate
Guilloteau, P., Martin, L., Eeckhaut, V., Ducatelle, R., Zabielski, R., & Immerseel, F. V. (2010) · Nutrition Research Reviews · doi:10.1017/s0954422410000247 · Cited by 813 · see citing works
Beneficial effects of probiotic consumption on the immune system
Maldonado Galdeano, C., Cazorla, S. I., Lemme Dumit, J. M., Vélez, E., & Perdigón, G. (2019) · Annals of Nutrition and Metabolism · doi:10.1159/000496426 · Cited by 729 · see citing works
Vaginal Microbiome: Rethinking Health and Disease
Ma, B., Forney, L. J., & Ravel, J. (2012) · Annual Review of Microbiology · doi:10.1146/annurev-micro-092611-150157 · Cited by 722 · see citing works
Cytoplasmic pH Measurement and Homeostasis in Bacteria and Archaea
Slonczewski, J. L., Fujisawa, M., Dopson, M., & KRULWICH, T. A. (2009) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/s0065-2911(09)05501-5 · Cited by 541 · see citing works
A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: From biofuels and chemicals, to biocatalysis and bioremediation
Nicolaou, S. A., Gaida, S. M., & Papoutsakis, E. T. (2010) · Metabolic Engineering · doi:10.1016/j.ymben.2010.03.004 · Cited by 537 · see citing works
RUMINANT NUTRITION SYMPOSIUM: Role of fermentation acid absorption in the regulation of ruminal pH12
Aschenbach, J. R., Penner, G. B., Stumpff, F., & Gäbel, G. (2010) · Journal of Animal Science · doi:10.2527/jas.2010-3301 · Cited by 500 · see citing works
pH Regulates Genes for Flagellar Motility, Catabolism, and Oxidative Stress in Escherichia coli K-12
Maurer, L. M., Yohannes, E., BonDurant, S. S., Radmacher, M. D., & Slonczewski, J. L. (2004) · Journal of Bacteriology · doi:10.1128/jb.187.1.304-319.2005 · Cited by 454 · see citing works
The use of organic acids to combat Salmonella in poultry: a mechanistic explanation of the efficacy
Immerseel, F. V., Russell, J. B., Flythe, M. D. D., Gantois, I., Timbermont, L., Pasmans, F., Haesebrouck, F., & Ducatelle, R. (2006) · Avian Pathology · doi:10.1080/03079450600711045 · Cited by 434 · see citing works
Self-citation
Role of Volatile Fatty Acids in Development of the Cecal Microflora in Broiler Chickens during Growth
van der Wielen, P. W. J. J., Biesterveld, S., Notermans, S. H. W., Hofstra, H., Urlings, H. A. P., & Knapen, F. V. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.6.2536-2540.2000 · Cited by 426 · see citing works
Fluoride and organic weak acids as modulators of microbial physiology
Marquis, R. E., Clock, S. A., & Mota‐Meira, M. (2003) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2003.tb00627.x · Cited by 384 · see citing works
In vaginal fluid, bacteria associated with bacterial vaginosis can be suppressed with lactic acid but not hydrogen peroxide
O'Hanlon, D. E., Moench, T. R., & Cone, R. A. (2011) · BMC Infectious Diseases · doi:10.1186/1471-2334-11-200 · Cited by 375 · see citing works
Acidogenic fermentation of food waste for volatile fatty acid production with co-generation of biohydrogen
Dahiya, S., Sarkar, O., Swamy, Y. V., & Mohan, S. V. (2015) · Bioresource Technology · doi:10.1016/j.biortech.2015.01.007 · Cited by 372 · see citing works
pH of the Cytoplasm and Periplasm of Escherichia coli : Rapid Measurement by Green Fluorescent Protein Fluorimetry
Wilks, J. C., & Slonczewski, J. L. (2007) · Journal of Bacteriology · doi:10.1128/jb.00615-07 · Cited by 371 · see citing works
Inhibition of Escherichia coli growth by acetic acid: a problem with methionine biosynthesis and homocysteine toxicity
Roe, A. J., O'Byrne, C. P., McLaggan, D., & Booth, I. R. (2002) · Microbiology · doi:10.1099/00221287-148-7-2215 · Cited by 355 · see citing works
Alternatives to antibiotics for organic poultry production: types, modes of action and impacts on bird's health and production
El-Hack, M. E. A., El‐Saadony, M. T., Salem, H. M., El-Tahan, A. M., Soliman, M. M., Youssef, G. B. A., Taha, A. E.-S., Soliman, S. M., Ahmed, A. E., El-kott, A. F., et al. (2022) · Poultry Science · doi:10.1016/j.psj.2022.101696 · Cited by 397 · see citing works
Molecular insights into probiotic mechanisms of action employed against intestinal pathogenic bacteria
van Zyl, W. F., Deane, S. M., & Dicks, L. M. T. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1831339 · Cited by 348 · see citing works
The utilization and mode of action of organic acids in the feeds of cultured aquatic animals
Ng, W., & Koh, C.-B. (2016) · Reviews in Aquaculture · doi:10.1111/raq.12141 · Cited by 339 · see citing works
Recent advances in the role of organic acids in poultry nutrition
Khan, S. H., & Iqbal, J. (2015) · Journal of Applied Animal Research · doi:10.1080/09712119.2015.1079527 · Cited by 333 · see citing works
Targeting gut microbiota and metabolism as the major probiotic mechanism - An evidence-based review
Ma, T., Shen, X., Shi, X., Sakandar, H. A., Quan, K., Li, Y., Jin, H., Kwok, L., Zhang, H., & Sun, Z. (2023) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2023.06.013 · Cited by 344 · see citing works
Salmonella Pathogenicity and Host Adaptation in Chicken-Associated Serovars
Foley, S. L., Johnson, T. J., Ricke, S. C., Nayak, R., & Danzeisen, J. (2013) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00015-13 · Cited by 330 · see citing works
pH-Dependent Expression of Periplasmic Proteins and Amino Acid Catabolism in Escherichia coli
Stancik, L. M., Stancik, D. M., Schmidt, B. F., Barnhart, D. M., Yoncheva, Y. N., & Slonczewski, J. L. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.15.4246-4258.2002 · Cited by 318 · see citing works
Achievements and perspectives to overcome the poor solvent resistance in acetone and butanol-producing microorganisms
Ezeji, T. C., Milne, C. B., Price, N. D., & Blaschek, H. P. (2009) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-009-2390-0 · Cited by 297 · see citing works
Acetate Metabolism and the Inhibition of Bacterial Growth by Acetate
Pinhal, S., Ropers, D., Geiselmann, J., & de Jong, H. (2019) · Journal of Bacteriology · doi:10.1128/jb.00147-19 · Cited by 278 · see citing works
International Society of Sports Nutrition Position Stand: Probiotics
Jäger, R., Mohr, A. E., Carpenter, K. C., Kerksick, C. M., Purpura, M., Moussa, A., Townsend, J. R., Lamprecht, M., West, N. P., Black, K., et al. (2019) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-019-0329-0 · Cited by 277 · see citing works
Fermented and nonfermented liquid feed to growing pigs: Effect on aspects of gastrointestinal ecology and growth performance
Canibe, N., & Jensen, B. B. (2003) · Journal of Animal Science · doi:10.2527/2003.8182019x · Cited by 267 · see citing works
Engineering Central Metabolic Pathways for High-Level Flavonoid Production in Escherichia coli
Leonard, E., Lim, K. H., Saw, P.-N., & Koffas, M. A. G. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00200-07 · Cited by 262 · see citing works
Immune boosting functional foods and their mechanisms: A critical evaluation of probiotics and prebiotics
Ashaolu, T. J. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110625 · Cited by 269 · see citing works
In vitro investigations of the effect of probiotics and prebiotics on selected human intestinal pathogens
Fooks, L. J., & Gibson, G. R. (2002) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2002.tb00907.x · Cited by 268 · see citing works
Weak Organic Acids: A Panoply of Effects on Bacteria
Hirshfield, I. N., Terzulli, S., & O'Byrne, C. (2003) · Science Progress · doi:10.3184/003685003783238626 · Cited by 245 · see citing works
Physiology of Acetic Acid Bacteria and Their Role in Vinegar and Fermented Beverages
Lynch, K. M., Zannini, E., Wilkinson, S., Daenen, L., & Arendt, E. K. (2019) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12440 · Cited by 258 · see citing works
Global Analysis of Escherichia coli Gene Expression during the Acetate-Induced Acid Tolerance Response
Arnold, C. N., McElhanon, J., Lee, A., Leonhart, R., & Siegele, D. A. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.7.2178-2186.2001 · Cited by 238 · see citing works
Nutritional influences on some major enteric bacterial diseases of pig
Pluske, J. R., Pethick, D. W., Hopwood, D. E., & Hampson, D. J. (2002) · Nutrition Research Reviews · doi:10.1079/nrr200242 · Cited by 237 · see citing works
Acetate and Formate Stress: Opposite Responses in the Proteome of Escherichia coli
Kirkpatrick, C. A., Maurer, L. M., Oyelakin, N. E., Yoncheva, Y. N., Maurer, R., & Slonczewski, J. L. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.21.6466-6477.2001 · Cited by 235 · see citing works
Metabolite stress and tolerance in the production of biofuels and chemicals: Gene‐expression‐based systems analysis of butanol, butyrate, and acetate stresses in the anaerobe Clostridium acetobutylicum
Alsaker, K. V., Paredes, C. J., & Papoutsakis, E. T. (2009) · Biotechnology and Bioengineering · doi:10.1002/bit.22628 · Cited by 213 · see citing works
Effect of Fermented Feed on the Microbial Population of the Gastrointestinal Tracts of Pigs
van Winsen, R. L., Urlings, H. A. P., Lipman, L. J. A., Snijders, J. M. A., Keuzenkamp, D., Verheijden, J. H. M., & Knapen, F. V. (2001) · Applied and Environmental Microbiology · doi:10.1128/aem.67.7.3071-3076.2001 · Cited by 212 · see citing works
Salmonella versus the Microbiome
Rogers, A. W. L., Tsolis, R. M., & Bäumler, A. J. (2020) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00027-19 · Cited by 202 · see citing works
Quantitative analysis of cellulose degradation and growth of cellulolytic bacteria in the rumen
Russell, J. B., Muck, R. E., & Weimer, P. J. (2008) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2008.00633.x · Cited by 204 · see citing works
Self-citation
The Energy Spilling Reactions of Bacteria and Other Organisms
Russell, J. B. (2007) · Microbial Physiology · doi:10.1159/000103591 · Cited by 204 · see citing works
Self-citation
Clostridium cellulolyticum: model organism of mesophilic cellulolytic clostridia
Desvaux, M. (2004) · FEMS Microbiology Reviews · doi:10.1016/j.femsre.2004.11.003 · Cited by 201 · see citing works
Role of acidifiers in livestock nutrition and health: A review
Pearlin, B. V., Shanmathy, M., Govidasamy, P., Manojkumar, V., Alagawany, M. M., Farag, M. R., Dhama, K., & Gopi, M. (2020) · Journal of Animal Physiology and Animal Nutrition · doi:10.1111/jpn.13282 · Cited by 200 · see citing works
Hydrogen production from sugars and sweet sorghum biomass using Ruminococcus albus
Ντάϊκου, Ι., Gavala, H. N., Kornaros, M. E., & Lyberatos, G. (2008) · International Journal of Hydrogen Energy · doi:10.1016/j.ijhydene.2007.10.053 · Cited by 194 · see citing works
Dynamics of Genomic-Library Enrichment and Identification of Solvent Tolerance Genes for Clostridium acetobutylicum
Borden, J. R., & Papoutsakis, E. T. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.02296-06 · Cited by 190 · see citing works
Diet,Escherichia coliO157:H7, and Cattle: A Review After 10 Years
Callaway, T. R., Carr, M. A., Edrington, T. S., Anderson, R. C., & Nisbet, D. J. (2009) · Current Issues in Molecular Biology · doi:10.21775/cimb.011.067 · Cited by 190 · see citing works
Effect of oxygen limitation and medium composition on Escherichia coli fermentation in shake-flask cultures.
Losen, M. H., Frölich, B., Pohl, M., & Büchs, J. (2004) · Biotechnology Progress · doi:10.1021/bp034282t · Cited by 188 · see citing works
Microencapsulated Short-Chain Fatty Acids in Feed Modify Colonization and Invasion Early After Infection with Salmonella Enteritidis in Young Chickens
Immerseel, F. V., Fievez, V., Buck, J. D., Pasmans, F., Martel, A., Haesebrouck, F., & Ducatelle, R. (2004) · Poultry Science · doi:10.1093/ps/83.1.69 · Cited by 186 · see citing works
Effects of Physical Properties of Feed on Microbial Ecology and Survival of Salmonella enterica Serovar Typhimurium in the Pig Gastrointestinal Tract
Mikkelsen, L. L., NAUGHTON, P. J., Hedemann, M. S., & Jensen, B. B. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.6.3485-3492.2004 · Cited by 184 · see citing works
Vaginal concentrations of lactic acid potently inactivate HIV
Aldunate, M., Tyssen, D. P., Johnson, A., Zakir, T., Sonza, S., Moench, T. R., Cone, R. A., & Tachedjian, G. (2013) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkt156 · Cited by 184 · see citing works
Fermented liquid feed—Microbial and nutritional aspects and impact on enteric diseases in pigs
Canibe, N., & Jensen, B. B. (2012) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2011.12.021 · Cited by 183 · see citing works
Nondigestible Oligosaccharides Enhance Bacterial Colonization Resistance against Clostridium difficile In Vitro
Hopkins, M. J., & Macfarlane, G. T. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.4.1920-1927.2003 · Cited by 183 · see citing works
The diversity of the fecal bacterial community and its relationship with the concentration of volatile fatty acids in the feces during subacute rumen acidosis in dairy cows
Mao, S., Zhang, R., Wang, D., & Zhu, W. (2012) · BMC Veterinary Research · doi:10.1186/1746-6148-8-237 · Cited by 181 · see citing works
Synthetic microbial consortia for biosynthesis and biodegradation: promises and challenges
Che, S., & Men, Y. (2019) · Journal of Industrial Microbiology and Biotechnology · doi:10.1007/s10295-019-02211-4 · Cited by 177 · see citing works
TheEscherichia coliProteome: Past, Present, and Future Prospects
Han, M., & Lee, S. Y. (2006) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00036-05 · Cited by 179 · see citing works
Intestinal microbiology in early life: specific prebiotics can have similar functionalities as human-milk oligosaccharides
Oozeer, R., van Limpt, K., Ludwig, T., Amor, K. B., Martı́n, R., Wind, R. D., Boehm, G., & Knol, J. (2013) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.038893 · Cited by 177 · see citing works
External Concentration of Organic Acid Anions and pH: Key Independent Variables for Studying How Organic Acids Inhibit Growth of Bacteria in Mildly Acidic Foods
Carpenter, C. E., & Broadbent, J. R. (2008) · Journal of Food Science · doi:10.1111/j.1750-3841.2008.00994.x · Cited by 175 · see citing works
Dynamic Changes of Intracellular pH in Individual Lactic Acid Bacterium Cells in Response to a Rapid Drop in Extracellular pH
Siegumfeldt, H., Rechinger, K. B., & Jakobsen, M. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.6.2330-2335.2000 · Cited by 173 · see citing works
Enrichment, Performance, and Microbial Diversity of a Thermophilic Mediatorless Microbial Fuel Cell
Jong, B. C., Kim, B. H., Chang, I. S., Liew, P. W. Y., Choo, Y. F., & Kang, G. S. (2006) · Environmental Science & Technology · doi:10.1021/es0613512 · Cited by 172 · see citing works
Probiotics interaction with foodborne pathogens: a potential alternative to antibiotics and future challenges
Wan, M. L. Y., Forsythe, S. J., & El-Nezami, H. S. (2018) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2018.1490885 · Cited by 180 · see citing works
LuxS and Autoinducer-2: Their Contribution to Quorum Sensing and Metabolism in Bacteria
Winzer, K., Hardie, K. R., & Williams, P. M. (2003) · Advances in applied microbiology · doi:10.1016/s0065-2164(03)53009-x · Cited by 169 · see citing works
Feed physical form and formic acid addition to the feed affect the gastrointestinal ecology and growth performance of growing pigs
Canibe, N., Højberg, O., Højsgaard, S., & Jensen, B. B. (2005) · Journal of Animal Science · doi:10.2527/2005.8361287x · Cited by 158 · see citing works
The Immunomodulatory Properties of Extracellular Vesicles Derived from Probiotics: A Novel Approach for the Management of Gastrointestinal Diseases
Molina‐Tijeras, J. A., Gálvez, J., & Rodríguez‐Cabezas, M. E. (2019) · Nutrients · doi:10.3390/nu11051038 · Cited by 156 · see citing works
Probiotics and Their Potential Preventive and Therapeutic Role for Cancer, High Serum Cholesterol, and Allergic and HIV Diseases
Nazir, Y., Hussain, S. A., Hamid, A. A., & Song, Y. (2018) · BioMed Research International · doi:10.1155/2018/3428437 · Cited by 163 · see citing works
Invasion of Salmonella enteritidis in avian intestinal epithelial cells in vitro is influenced by short-chain fatty acids
Immerseel, F. V. (2003) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(02)00542-1 · Cited by 156 · see citing works
From Acidifiers to Intestinal Health Enhancers: How Organic Acids Can Improve Growth Efficiency of Pigs
Tugnoli, B., Giovagnoni, G., Piva, A., & Grilli, E. (2020) · Animals · doi:10.3390/ani10010134 · Cited by 158 · see citing works
Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling
Pieterse, B., Leer, R. J., Schuren, F. H. J., & WERF, M. J. V. D. (2005) · Microbiology · doi:10.1099/mic.0.28304-0 · Cited by 154 · see citing works
The in vitro inhibition of Gram-negative pathogenic bacteria by Bifidobacteria is caused by the production of organic acids
Makras, L., & De Vuyst, L. (2006) · International Dairy Journal · doi:10.1016/j.idairyj.2005.09.006 · Cited by 147 · see citing works
Eubiotic effect of a dietary acidifier (potassium diformate) on the health status of cultured Oreochromis niloticus
Abu‐Elala, N. M., & Ragaa, N. M. (2014) · Journal of Advanced Research · doi:10.1016/j.jare.2014.02.008 · Cited by 142 · see citing works
Oxygen limitation modulates pH regulation of catabolism and hydrogenases, multidrug transporters, and envelope composition in Escherichia coli K-12
Hayes, E. T., Wilks, J. C., Sanfilippo, P., Yohannes, E., Tate, D. P., Jones, B. D., Radmacher, M. D., BonDurant, S. S., & Slonczewski, J. L. (2006) · BMC Microbiology · doi:10.1186/1471-2180-6-89 · Cited by 140 · see citing works
Incubation at 25 °C prevents acid crash and enhances alcohol production in Clostridium carboxidivorans P7
Ramió‐Pujol, S., Ganigué, R., Bañeras, L., & Colprim, J. (2015) · Bioresource Technology · doi:10.1016/j.biortech.2015.05.077 · Cited by 136 · see citing works
Susceptibility of Clostridium perfringens to C2-C18 fatty acids
Skřivanová, E., Marounek, M., Dlouhá, G., & Kaňka, J. (2005) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2005.01709.x · Cited by 137 · see citing works
Inactivation of pathogens in anaerobic digestion systems for converting biowastes to bioenergy: A review
Jiang, Y., Xie, S., Dennehy, C., Lawlor, P. G., Hu, Z., Wu, G., Zhan, X., & Gardiner, G. E. (2019) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2019.109654 · Cited by 131 · see citing works
Performance, intestinal microflora, and wall morphology of weanling pigs fed sodium butyrate1
Biagi, G., Piva, A., Moschini, M., Vezzali, E., & Roth, F. X. (2007) · Journal of Animal Science · doi:10.2527/jas.2006-378 · Cited by 127 · see citing works
Structural and Functional Features of Formate Hydrogen Lyase, an Enzyme of Mixed-Acid Fermentation from Escherichia coli
Bagramyan, K. A., & Trchоunian, A. (2003) · Biochemistry (Moscow) · doi:10.1023/b:biry.0000009129.18714.a4 · Cited by 126 · see citing works
Microbial-growth inhibition during composting of food waste: Effects of organic acids
Cheung, H. N. B., Huang, G., & Yu, H. W. (2010) · Bioresource Technology · doi:10.1016/j.biortech.2010.02.062 · Cited by 117 · see citing works
Antimicrobial activity against Shigella sonnei and probiotic properties of wild lactobacilli from fermented food
Zhang, Y., Zhang, L., Du, M., Yi, H., Guo, C., Tuo, Y., Han, X., Li, J., Zhang, L., & Yang, L. (2011) · Microbiological Research · doi:10.1016/j.micres.2011.02.006 · Cited by 116 · see citing works
Bioactives from probiotics for dermal health: functions and benefits
Lew, L.-C., & Liong, M.-T. (2013) · Journal of Applied Microbiology · doi:10.1111/jam.12137 · Cited by 115 · see citing works
Short-Chain Fatty Acids as a Potential Treatment for Infections: a Closer Look at the Lungs
Machado, M. G., Sencio, V., & Trottein, F. (2021) · Infection and Immunity · doi:10.1128/iai.00188-21 · Cited by 114 · see citing works
Bacterial Stressors in Minimally Processed Food
Capozzi, V., Fiocco, D., Amodio, M. L., Gallone, A., & Spano, G. (2009) · International Journal of Molecular Sciences · doi:10.3390/ijms10073076 · Cited by 112 · see citing works
Novel Polyfermentor Intestinal Model (PolyFermS) for Controlled Ecological Studies: Validation and Effect of pH
Zihler, A., Fuentes, S., Dostal, A., Payne, A. N., Vazquez-Gutierrez, P., Chassard, C., Grattepanche, F., de Vos, W. M., & Lacroix, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077772 · Cited by 111 · see citing works
Effect of dietary concentrate to forage ratio on growth performance, rumen fermentation and bacterial diversity of Tibetan sheep under barn feeding on the Qinghai-Tibetan plateau
Liu, H., Xu, T., Xu, S., Ma, L., Han, X., Wang, X., Zhang, X., Hu, L., Zhao, N., Chen, Y., et al. (2019) · PeerJ · doi:10.7717/peerj.7462 · Cited by 110 · see citing works
Metabolic interactions between dynamic bacterial subpopulations
Rosenthal, A. Z., Qi, Y., Hormoz, S., Park, J., Li, H., & Elowitz, M. B. (2018) · eLife · doi:10.7554/elife.33099 · Cited by 105 · see citing works
Adaptation in Bacillus cereus: From Stress to Disease
Duport, C., Jobin, M.-P., & Schmitt, P. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01550 · Cited by 104 · see citing works
Bioprospecting for brewers: Exploiting natural diversity for naturally diverse beers
Cubillos, F. A., Gibson, B. R., Grijalva‐Vallejos, N., Krogerus, K., & Nikulin, J. (2019) · Yeast · doi:10.1002/yea.3380 · Cited by 104 · see citing works
Advances in research on solid-state fermented feed and its utilization: The pioneer of private customization for intestinal microorganisms
Yang, L., Zeng, X., & Qiao, S. (2021) · Animal nutrition · doi:10.1016/j.aninu.2021.06.002 · Cited by 104 · see citing works
Growth media in anaerobic fermentative processes: The underestimated potential of thermophilic fermentation and anaerobic digestion
Hendriks, A., van Lier, J. B., & de Kreuk, M. (2017) · Biotechnology Advances · doi:10.1016/j.biotechadv.2017.08.004 · Cited by 102 · see citing works
Characterization and Functional Analysis of the poxB Gene, Which Encodes Pyruvate Oxidase in Lactobacillus plantarum
Lorquet, F., Goffin, P., Muscariello, L., Baudry, J.-B., Ladero, V., Sacco, M., Kleerebezem, M., & Pascal Hols, A. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.12.3749-3759.2004 · Cited by 103 · see citing works
Acetic Acid Induces Expression of the Staphylococcus aureus cidABC and lrgAB Murein Hydrolase Regulator Operons
Rice, K. C., Nelson, J. B., Patton, T. G., Yang, S., & Bayles, K. W. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.3.813-821.2005 · Cited by 103 · see citing works
Potential of fructooligosaccharide prebiotics in alternative and nonconventional poultry production systems
Ricke, S. C. (2015) · Poultry Science · doi:10.3382/ps/pev049 · Cited by 104 · see citing works
Comparative Efficacy of an Organic Acid Blend and Bacitracin Methylene Disalicylate as Growth Promoters in Broiler Chickens: Effects on Performance, Gut Histology, and Small Intestinal Milieu
Samanta, S., Haldar, S., & Ghosh, T. K. (2009) · Veterinary Medicine International · doi:10.4061/2010/645150 · Cited by 99 · see citing works
The highly tolerant acetic acid bacterium Gluconacetobacter europaeus adapts to the presence of acetic acid by changes in lipid composition, morphological properties and PQQ-dependent ADH expression
Trček, J., Jernejc, K., & Matsushita, K. (2007) · Extremophiles · doi:10.1007/s00792-007-0077-y · Cited by 99 · see citing works
Strategies to control Salmonella in the broiler production chain
Immerseel, F. V., Zutter, L. D., Houf, K., Pasmans, F., Haesebrouck, F., & Ducatelle, R. (2009) · World s Poultry Science Journal · doi:10.1017/s0043933909000270 · Cited by 99 · see citing works
Survival of Escherichia coli O157:H7 during the fermentation of Spanish-style green table olives (conservolea variety) supplemented with different carbon sources
Spyropoulou, K. (2001) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(00)00510-9 · Cited by 98 · see citing works
pH-Dependent Catabolic Protein Expression during Anaerobic Growth of Escherichia coli K-12
Yohannes, E., Barnhart, D. M., & Slonczewski, J. L. (2003) · Journal of Bacteriology · doi:10.1128/jb.186.1.192-199.2004 · Cited by 98 · see citing works
Role of the Glutamate Decarboxylase Acid Resistance System in the Survival of Listeria monocytogenes LO28 in Low pH Foods
Cotter, P. D., O'reilly, K., & Hill, C. (2001) · Journal of Food Protection · doi:10.4315/0362-028x-64.9.1362 · Cited by 98 · see citing works
Kup is the major K+ uptake system in Escherichia coli upon hyper‐osmotic stress at a low pH
Trchоunian, A., & Kobayashi, H. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)00288-4 · Cited by 96 · see citing works
Effect of sodium, potassium, magnesium, and calcium salt cations on pH, proteolysis, organic acids, and microbial populations during storage of full-fat Cheddar cheese
McMahon, D. J., Oberg, C. J., Drake, M. A., Farkye, N. Y., Moyes, L. V., Arnold, M., Ganesan, B., Steele, J. L., & Broadbent, J. R. (2014) · Journal of Dairy Science · doi:10.3168/jds.2014-8071 · Cited by 95 · see citing works
Influence of Ni, Co, Fe, and Na additions on methane production in Sphagnum-dominated Northern American peatlands
Basiliko, N., & Yavitt, J. B. (2001) · Biogeochemistry · doi:10.1023/a:1006461803585 · Cited by 94 · see citing works
Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients
LaSarre, B., McCully, A. L., Lennon, J. T., & McKinlay, J. B. (2016) · The ISME Journal · doi:10.1038/ismej.2016.141 · Cited by 88 · see citing works

The ability of Escherichia coli O157:H7 to decrease its intracellular pH and resist the toxicity of acetic acid
Diez‐Gonzalez, F., & Russell, J. B. (1997) · Microbiology · doi:10.1099/00221287-143-4-1175 · Cited by 168 · see citing works
Self-citation
Another explanation for the toxicity of fermentation acids at low pH: anion accumulation versus uncoupling
Russell, J. B. (1992) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1992.tb04990.x · Cited by 573 · see citing works
Self-citation
Bioenergetics of lactic acid bacteria: cytoplasmic pH and osmotolerance
Kashket, E. R. (1987) · FEMS Microbiology Letters · doi:10.1016/0378-1097(87)90110-8 · Cited by 49 · see citing works
Internal pH and Acid Anion Accumulation in Listeria monocytogenes and Escherichia coli Exposed to Lactic or Acetic Acids at Mildly Acidic pH
Branson, S. R., Broadbent, J. R., & Carpenter, C. E. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.803271 · Cited by 17 · see citing works
Resistance of Streptococcus bovis to acetic acid at low pH: relationship between intracellular pH and anion accumulation
Russell, J. B. (1991) · Applied and Environmental Microbiology · doi:10.1128/aem.57.1.255-259.1991 · Cited by 75 · see citing works
Self-citation

Authors: Russell, J. B., & Diez-Gonzalez, F.
Affiliations: Agricultural Research Service (US)
ORCID: Russell, James B.
Venue: Advances in Microbial Physiology
Publisher: Elsevier
Published: 1997
Volume: 39
Pages: 205-234
ISSN: 0065-2911 (ISSN-L)
DOI: 10.1016/s0065-2911(08)60017-x
OpenAlex: W1570063046
Cited by: 498
References: 130
Citations by year: 2026: 16 · 2025: 16 · 2024: 26 · 2023: 21 · 2022: 27 · 2021: 28 · 2020: 17 · 2019: 18 · 2018: 18 · 2017: 18 · 2016: 21 · 2015: 19 · 2014: 22 · 2013: 20 · 2012: 24
FWCI: 5.92
Type: book chapter
Language: en
Open access: closed
Locations: Advances in microbial physiology/Advances in Microbial Physiology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Keywords: fermentation acids, bacterial growth inhibition, low pH, proton motive force, intracellular pH, membrane potential, potassium accumulation, Escherichia coli O157:H7, Escherichia coli K-12, Gram-positive bacteria, microbial ecology
MeSH terms: Acids, Animals, Bacteria, Biological Transport, Fermentation, Food Microbiology, Hydrogen-Ion Concentration, Intestinal Diseases, Rumen, Silage, Soil Microbiology, Solvents, Acetic Acid

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

The effects of fermentation acids on bacterial growth

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks