Enzymes of Pyruvate and Phosphoenolpyruvate Carboxylation in Rumen Bacteria

Atwal, A. S.; Sauer, Frank

doi:10.4141/cjas74-072

Cited by 4 publications

(3 citation statements)

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“…Generation of ATP in propionate's randomizing pathway is also affected by other metabolic steps. Oxaloacetate (or malate) formation from phosphoenolpyruvate (PEP) entails the utilization of PEP high-energy phosphate bond, which is then not used to generate ATP, but when catalyzed by PEP carboxykinase, PEP carboxylation can still generate ATP or GTP without additional energy input (Atwal and Sauer, 1974 ). Also, when the entire randomizing pathway takes place in a single cell (i.e., without interspecies transfer of succinate), carboxylation of pyruvate to form oxaloacetate can occur coupled to methylmalonyl-CoA decarboxylation to propionyl-CoA, making oxaloacetate formation from pyruvate energetically neutral (Deborde and Boyaval, 2000 ).…”

Section: Discussionmentioning

confidence: 99%

Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: a meta-analysis

2015

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Maximizing the flow of metabolic hydrogen ([H]) in the rumen away from CH4 and toward volatile fatty acids (VFA) would increase the efficiency of ruminant production and decrease its environmental impact. The objectives of this meta-analysis were: (i) To quantify shifts in metabolic hydrogen sinks when inhibiting ruminal methanogenesis in vitro; and (ii) To understand the variation in shifts of metabolic hydrogen sinks among experiments and between batch and continuous cultures systems when methanogenesis is inhibited. Batch (28 experiments, N = 193) and continuous (16 experiments, N = 79) culture databases of experiments with at least 50% inhibition in CH4 production were compiled. Inhibiting methanogenesis generally resulted in less fermentation and digestion in most batch culture, but not in most continuous culture, experiments. Inhibiting CH4 production in batch cultures resulted in redirection of metabolic hydrogen toward propionate and H2 but not butyrate. In continuous cultures, there was no overall metabolic hydrogen redirection toward propionate or butyrate, and H2 as a proportion of metabolic hydrogen spared from CH4 production was numerically smaller compared to batch cultures. Dihydrogen accumulation was affected by type of substrate and methanogenesis inhibitor, with highly fermentable substrates resulting in greater redirection of metabolic hydrogen toward H2 when inhibiting methanogenesis, and some oils causing small or no H2 accumulation. In both batch and continuous culture, there was a decrease in metabolic hydrogen recovered as the sum of propionate, butyrate, CH4 and H2 when inhibiting methanogenesis, and it is speculated that as CH4 production decreases metabolic hydrogen could be increasingly incorporated into formate, microbial biomass, and perhaps, reductive acetogenesis in continuous cultures. Energetic benefits of inhibiting methanogenesis depended on the inhibitor and its concentration and on the in vitro system.

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Section: Discussionmentioning

confidence: 99%

Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: a meta-analysis

2015

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“…Enzyme studies on this bacterium by Joyner and Baldwin (25) and our own group (unpublished data) indicate that glucose is predominantly fermented via the Embden-Myerhof pathway as far as phosphoenolpyruvate. Succinate is thought to be formed via CO., fixation into phosphoenolpyruvate (33) by phosphoenolpyruvate carboxykinase, although the possibility that pyruvate carboxylase plays some role cannot be ruled out (1). Another portion of the phosphoenolpyruvate is metabolized to pyruvate.…”

Section: Discussionmentioning

confidence: 99%

Metabolism and growth yields in Bacteroides ruminicola strain b14

Howlett¹,

Mountfort²,

Turner³

et al. 1976

Appl Environ Microbiol

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Metabolism of D-glucose by Bacteroides ruminicola subsp. brevis, strain B,4, has been examined. Growth yield studies gave molar growth yields, corrected for storage polysaccharide, of approximately 66 g (dry weight)/mol of glucose fermented. The storage polysaccharide amounted to about 14% of the total dry weight, or 55% of the total cellular carbohydrate, at full growth. After correcting glucose utilization for incorporation into cellular carbohydrate, measurement of product formation showed that 1.1 succinate, 0.8 acetate, and 0.35 formate are produced and 0.5 CO2 net is taken up during the fermentation of 1 glucose under the conditions used. The implication of these results with respect to adenosine 5'-triphosphate (ATP) molar growth yield calculations is discussed. If substratelevel phosphorylation reactions alone are responsible for ATP generation, then the ATP molar growth yield must be about 23 g (dry weight)/mol of ATP. Alternatively, if anaerobic electron transfer-linked phosphorylation also occurs, the ATP molar growth yield will be lower. Bacteroides ruminicola is one of the more numerically important bacteria found in the rumen, representing 6 to 19% of the total culturable carbohydrate fermenters present (8). It is not immediately obvious why B. ruminicola can compete so successfully in this anaerobic environment, which contains so many other carbohydrate-utilizing, organic acid-producing bacteria. Part of the reason for its quantitative predominance may be the result of its great versatility towards possible carbohydrate and nitrogen sources utilized (7, 8). However, it is also likely that the species has a highly efficient energy metabolism and can multiply rapidly. This study set out to examine growth yields of B. ruminicola, as an index of its energy metabolism, to discover whether the yields are "normal" or "anomalous" (19) and can be predicted from the products of fermentation. Careful attention has been paid to correction for storage polysaccharide and carbon recovery in products, which can both lead to erroneous results if ignored. B. ruminicola has a b-type cytochrome, which may be involved in fumarate reduction by reduced nicotinamide adenine dinucleotide (40); such electron transport systems in other bacteria have sometimes been postulated to be coupled to anaerobic electron transport phosphorylation reactions (3, 16, 28). If such a system is operative in B. ruminicola, then adenosine 5'-triphosphate (ATP) yields will be higher than can be accounted for by substrate-level phosphorylation reactions. Caldwell (D. R. Caldwell, Diss. Abstr. Int. B. 31:1419) has previously suggested that ATP yields in B. ruminicola strain GA33 are between 4.5 and 7.8 ATP/ mol of glucose, based on measurements of cellular protein. MATERIALS AND METHODS Bacteria. B. ruminicola subsp. brevis, strain B,4 (7, 8), was used in the present work and was kindly supplied by M. P. Bryant of the University of Illinois. This strain was used in preference to the type strain, strain GA33, because strain B,4 clumps rather less ...

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“…The labelling pattern oflysine (Table 3) synthesized from [1-14C]acetate is clearly consistent with the sequence of reactions shown in Scheme 1, in which lysine is synthesized with the 14C label in C-2, C-3 and C-6. The carboxylation of pyruvate to oxaloacetate (Scheme 1) by enzymes of rumen microorganisms was described previously (Atwal & Sauer, 1974).…”

Section: Lysinementioning

confidence: 99%

Amino acid biosynthesis in mixed rumen cultures

Sauer¹,

Erfle²,

Mahadevan³

1975

Biochemical Journal

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Mixed rumen micro-organisms, maintained in continuous culture readily incorporated labelled HCO3- and acetate into amino acids. Labelled propionate, in contrast, was utilized only for isoleucine biosynthesis, but failed to label other amino acids to any significant extent. Evidence was obtained showing that in these mixed, i.e. symbiotic, cultures foward tricarboxylic acid-cycle reactions only proceed to 2-oxoglutarate. 14C distribution in amino acids clearly shows that 2-oxoglutarate is not oxidized further by tricarboxylic acid-cycle enzymes. Instead, acetate is carboxylated to pyruvate which is then carboxylated to oxaloacetate. Oxaloacetate equilibrates with fumarate and thereby carbon atoms 1 and 4 as well as carbon atoms 2 and 3 are randomized. Evidence was also obtained for the carboxylation of propionate to 2-oxobutyrate, isovalerate to 4-methyl-2-oxopentanoate, phenylacetate and hydroxyphentlacetate to the corresponding phenyl- and hydroxyphenyl-pyruvic acids and succinate to 2-oxoglutarate. Of the amino acid precursors investigated, only 3-hydroxypyruvate, the precursor of serine, appeared to be synthesized via an oxidative step, i.e. 3-phosphoglyceric acid to 3-phosphohydroxypyruvic acid. Most 2-oxo precursors of amino acids in these organisms appear to be formed via reductive carboxylation of the precursor acid.

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Enzymes of Pyruvate and Phosphoenolpyruvate Carboxylation in Rumen Bacteria

Cited by 4 publications

References 5 publications

Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: a meta-analysis

Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: a meta-analysis

Metabolism and growth yields in Bacteroides ruminicola strain b14

Amino acid biosynthesis in mixed rumen cultures

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