Eubacterium pyruvativorans sp. nov., a novel non-saccharolytic anaerobe from the rumen that ferments pyruvate and amino acids, forms caproate and utilizes acetate and propionate

Wallace, Robert John; McKain, Nest; McEwan, Neil R.; Miyagawa, Eiichi; Chaudhary, L. C.; King, T. P.; Walker, Nicola; Apajalahti, Juha H. A.; Newbold, C. J.

doi:10.1099/ijs.0.02110-0

Cited by 92 publications

(49 citation statements)

References 26 publications

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“…Eubacterium pyruvativorans is one of several non-saccharolytic bacteria isolated from the sheep rumen on the basis that it was able to grow on trypticase as the sole source of energy as well as a N source (Eschenlauer et al, 2002). This species is fairly closely related to other non-saccharolytic bacteria isolated in the same study (Eschenlauer et al, 2002;Wallace et al, 2003) and in other studies of non-saccharolytic ruminal bacteria (Attwood et al, 1998), and to bacteria isolated from the oral cavity (Cheeseman et al, 1996;Wade et al, 1999a, b). The main fermentation products of E. pyruvativorans are caproate and valerate, with butyrate and propionatenormally end products of anaerobic fermentation in the rumen and elsewhere -apparently being utilized (Eschenlauer et al, 2002;Wallace et al, 2003).…”

Section: Introductionmentioning

confidence: 78%

“…pyruvativorans was named as such because it grew most rapidly on pyruvate (Wallace et al, 2003). Since pyruvate is not abundant extracellularly in the rumen (Wallace, 1978), it appeared that the true substrate for its growth in vivo was probably amino acids, although the net utilization of C 3 and C 4 volatile fatty acids (VFAs) and a slight utilization of lactate suggested that E. pyruvativorans might have a wider metabolic role.…”

Section: Introductionmentioning

confidence: 99%

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Metabolic properties of Eubacterium pyruvativorans, a ruminal ‘hyper-ammonia-producing’ anaerobe with metabolic properties analogous to those of Clostridium kluyveri

Wallace¹,

Chaudhary²,

Miyagawa³

et al. 2004

Microbiology

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Eubacterium pyruvativorans I-6T is a non-saccharolytic, amino-acid-fermenting anaerobe from the rumen, isolated by its ability to grow on pancreatic casein hydrolysate (PCH) as sole C source. This study investigated its metabolic properties and its likely ecological niche. Additional growth was supported by pyruvate, vinyl acetate, and, to a lesser extent, lactate and crotonate, and also by a mixture of amino acids (alanine, glycine, serine and threonine) predicted to be catabolized to pyruvate. No single amino acid supported growth, and peptides were required for growth on amino acids. Alanine, followed by leucine, serine and proline, were used most extensively during growth, but only alanine and asparate were extensively modified before incorporation. Growth on PCH, but not on pyruvate, was increased by the addition of acetate, propionate and butyrate. L-Lactate was fermented incompletely, mainly to acetate, but no lactate-C was incorporated. Propionate and butyrate were utilized during growth, forming valerate and caproate, respectively. Labelling experiments suggested a metabolic pattern where two C atoms of butyrate, valerate and caproate were derived from amino acids, with the others being formed from acetate, propionate and butyrate. The metabolic strategy of E. pyruvativorans therefore resembles that of Clostridium kluyveri, which ferments ethanol only when the reaction is coupled to acetate, propionate or butyrate utilization. The fermentative niche of E. pyruvativorans appears to be to scavenge amino acids, lactate and possibly other metabolites in order to generate ATP via acetate formation, using volatile fatty acid elongation with C 2 units derived from other substrates to dispose of reducing equivalents.

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Section: Introductionmentioning

confidence: 78%

Section: Introductionmentioning

confidence: 99%

Metabolic properties of Eubacterium pyruvativorans, a ruminal ‘hyper-ammonia-producing’ anaerobe with metabolic properties analogous to those of Clostridium kluyveri

Wallace¹,

Chaudhary²,

Miyagawa³

et al. 2004

Microbiology

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“…The acetate production depends on PDH, which normally functions in aerobic metabolism (5,21,22). Eubacterium pyruvativorans is one of the few bacteria growing by fermentation of external pyruvate (35). The fermentation products are short-chain fatty acids, and the fermentation presumably requires PFOR.…”

Section: Resultsmentioning

confidence: 99%

Pyruvate Fermentation by Oenococcus oeni and Leuconostoc mesenteroides and Role of Pyruvate Dehydrogenase in Anaerobic Fermentation

Wagner

Tran²,

Richter

et al. 2005

Appl Environ Microbiol

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The heterofermentative lactic acid bacteria Oenococcus oeni and Leuconostoc mesenteroides are able to grow by fermentation of pyruvate as the carbon source (2 pyruvate 3 1 lactate ؉ 1 acetate ؉ 1 CO 2 ). The growth yields amount to 4.0 and 5.3 g (dry weight)/mol of pyruvate, respectively, suggesting formation of 0.5 mol ATP/mol pyruvate. Pyruvate is oxidatively decarboxylated by pyruvate dehydrogenase to acetyl coenzyme A, which is then converted to acetate, yielding 1 mol of ATP. For NADH reoxidation, one further pyruvate molecule is reduced to lactate. The enzymes of the pathway were present after growth on pyruvate, and genome analysis showed the presence of the corresponding structural genes. The bacteria contain, in addition, pyruvate oxidase activity which is induced under microoxic conditions. Other homo-or heterofermentative lactic acid bacteria showed only low pyruvate fermentation activity.Oenococcus oeni and Leuconostoc mesenteroides are heterofermentative lactic acid bacteria (LAB) that are closely related to each other and have previously been grouped within the same family due to many physiological and genetic similarities (6,8,9). O. oeni is used in wine fermentation for degradation of malic acid, whereas L. mesenteroides is used for fermentation of vegetables. Both bacteria convert hexoses by heterolactic fermentation to lactate, ethanol, and CO 2 . Ethanol formation from acetyl phosphate (or acetyl coenzyme A [acetyl-CoA]) is required for reoxidation of NAD(P)H, which is produced in the pentose phosphate pathway during hexose oxidation. In many heterolactic acid bacteria and in particular in O. oeni, NAD(P)H reoxidation by the ethanol pathway is slow because of low acetaldehyde dehydrogenase activity (16,26,27,34). When, in addition, coenzyme A (HSCoA), and consequently acetyl-CoA, is limiting due to a shortage of the precursor pantothenate, the low capacity of NAD(P)H reoxidation by the ethanol pathway limits the metabolism and growth rate of the bacteria (26). For this reason, O. oeni, and to some extent also L. mesenteroides, uses alternative pathways for NAD(P)H reoxidation, such as the reduction of erythrose-4-phosphate to erythritol, to overcome the limitation (26,34).In addition to the alternative endogenous pathways of erythritol and glycerol formation for NAD(P)H reoxidation, the bacteria are able to use external electron acceptors for reoxidation of NAD(P)H. Fructose, O 2 , and pyruvate can be used as electron sinks by O. oeni and L. mesenteroides, yielding mannitol, H 2 O 2 , and lactate as the reduced end products (16,23,27). O. oeni, which has very low capacities for NAD(P)H reoxidation in the ethanol pathway, gains significantly in metabolic and growth rates by the use of external electron acceptors.When pyruvate was supplied in excess as an electron acceptor, there were indications that pyruvate is not only used as an electron acceptor but also oxidized to acetate (27, 28). As shown here, pyruvate can be disproportionated to lactate and acetate at substantial rates and can be used...

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“…Caproic acid is a side product in the acidogenic fermentation of a complex biomass or sugars (37,38). It is generally produced by anaerobic bacteria such as Clostridium kluyveri (39) and Eubacterium pyruvativorans (40) or by cocultures of C. kluyveri with ruminal cellulolytic bacteria using cellulose as a substrate (41). In this study, we observed significant correlations between caproic acid content and the relative abundances of four core prokaryotic populations (Lactobacillus, Clostridium IV [OTU2212], unclassified Clostridiaceae 1 [OTU3893], and unclassified Anaerobrancaceae [OTU3251]) (P Ͻ 0.01).…”

Section: Discussionmentioning

confidence: 99%

Prokaryotic Communities in Pit Mud from Different-Aged Cellars Used for the Production of Chinese Strong-Flavored Liquor

Tao

Rui

et al. 2014

Appl Environ Microbiol

166

228

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cChinese strong-flavored liquor (CSFL) accounts for more than 70% of all Chinese liquor production. Microbes in pit mud play key roles in the fermentation cellar for the CSFL production. However, microbial diversity, community structure, and cellar-agerelated changes in pit mud are poorly understood. Here, we investigated the prokaryotic community structure and diversity in pit-mud samples with different cellar ages (1, 10, 25, and 50 years) using the pyrosequencing technique. Results indicated that prokaryotic diversity increased with cellar age until the age reached 25 years and that prokaryotic community structure changed significantly between three cellar ages (1, 10, and 25 years). Significant correlations between prokaryotic communities and environmental variables (pH, NH 4 ؉ , lactic acid, butyric acid, and caproic acid) were observed. Overall, our study results suggested that the long-term brewing operation shapes unique prokaryotic community structure and diversity as well as pit-mud chemistry. We have proposed a three-phase model to characterize the changes of pit-mud prokaryotic communities. C hinese strong-flavored liquor (CSFL), also called "Luzhou flavor liquor," accounts for more than 70% of Chinese liquor production (1). It is produced by the unique and traditional Chinese solid-state fermentation technique, which has a history of several thousand years. In brief, a cellar is constructed by digging a rectangular soil pit in which the entire inner wall is covered with precultured pit mud. The precultured pit mud is usually prepared by mixing aged pit mud (as an inoculum), fresh common soil, and water and incubating the mixture for about a year in an anaerobic cellar before use. The raw materials for the fermentation, including wheat, sorghum, and corn, are mixed, crushed, and distilled by steaming. The steamed raw material is supplied with 2% to 3% (wt/wt) Daqu-starter, which mainly includes mold and yeast, and placed into the cellar. The cellar is sealed with common mud, and fermentation is allowed to proceed for 60 days. Fermented material is then taken out of the cellar and distilled to make Chinese liquor. The process described above is periodically repeated after new fermentation materials are supplied.Microbes in the pit mud produce various flavor components such as butyric acid, caproic acid, and ethyl caproate. In particular, ethyl caproate is recognized as a key component affecting the CSFL flavor and quality. In general, CSFL quality improves with increasing cellar age. High-quality liquor is produced only in old cellars, which are maintained at least for 20 years by continuous use (2, 3). In particular, some long-aged cellars have been used for several hundred years without interruption, and well-known CSFLs such as Wuliangye, Jiannanchun, and Luzhoulaojiao are brewed in such long-aged cellars (1, 4). High CSFL quality is attributed to the maturing process of pit mud, which results in a well-balanced microbial community structure and diversity in the pit mud to produce distinctive flavo...

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Eubacterium pyruvativorans sp. nov., a novel non-saccharolytic anaerobe from the rumen that ferments pyruvate and amino acids, forms caproate and utilizes acetate and propionate

Cited by 92 publications

References 26 publications

Metabolic properties of Eubacterium pyruvativorans, a ruminal ‘hyper-ammonia-producing’ anaerobe with metabolic properties analogous to those of Clostridium kluyveri

Metabolic properties of Eubacterium pyruvativorans, a ruminal ‘hyper-ammonia-producing’ anaerobe with metabolic properties analogous to those of Clostridium kluyveri

Pyruvate Fermentation by Oenococcus oeni and Leuconostoc mesenteroides and Role of Pyruvate Dehydrogenase in Anaerobic Fermentation

Prokaryotic Communities in Pit Mud from Different-Aged Cellars Used for the Production of Chinese Strong-Flavored Liquor

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