Electron transport phosphorylation in rumen butyrivibrios: unprecedented ATP yield for glucose fermentation to butyrate

Hackmann, Timothy J.; Firkins, J.L.

doi:10.3389/fmicb.2015.00622

Cited by 64 publications

(63 citation statements)

References 63 publications

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“…S2A). However, as in a previous study (Hackmann and Firkins, ), we found that some Butyrivibrio and Pseudobutyrivibrio ( n = 3) encode an atypical pathway for forming butyrate (Supporting Information Fig. S2B).…”

Section: Resultssupporting

confidence: 86%

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Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short‐chain fatty acids

Hackmann

Ngugi

Firkins

et al. 2017

Environmental Microbiology

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Bacteria have been thought to follow only a few well-recognized biochemical pathways when fermenting glucose or other hexoses. These pathways have been chiseled in the stone of textbooks for decades, with most sources rendering them as they appear in the classic 1986 text by Gottschalk. Still, it is unclear how broadly these pathways apply, given that they were established and delineated biochemically with only a few model organisms. Here, we show that well-recognized pathways often cannot explain fermentation products formed by bacteria. In the most extensive analysis of its kind, we reconstructed pathways for glucose fermentation from genomes of 48 species and subspecies of bacteria from one environment (the rumen). In total, 44% of these bacteria had atypical pathways, including several that are completely unprecedented for bacteria or any organism. In detail, 8% of bacteria had an atypical pathway for acetate formation; 21% of bacteria had an atypical pathway for propionate or succinate formation; 6% of bacteria had an atypical pathway for butyrate formation and 33% of bacteria had an atypical or incomplete Embden-Meyerhof-Parnas pathway. This study shows that reconstruction of metabolic pathways - a common goal of omics studies - could be incorrect if well-recognized pathways are used for reference. Furthermore, it calls for renewed efforts to delineate fermentation pathways biochemically.

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Section: Resultssupporting

confidence: 86%

“…A previous study from our group found an atypical pathway for butyrate formation in most butyrivibrios ( Butyrivibrio and Pseudobutyrivibrio spp.) (Hackmann and Firkins, ). Specifically, the pathway involves the ion pump Ech hydrogenase, which together with Rnf generates an electrochemical potential and conserves energy.…”

Section: Discussionmentioning

confidence: 99%

Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short‐chain fatty acids

Hackmann

Ngugi

Firkins

et al. 2017

Environmental Microbiology

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“…Among bacteria genera or species that were studied in several experiments, Fibrobacter and Ruminococcus were negatively affected in most cases, but the effects on Butyrivibrio and Prevotella were highly variable. These latter genera comprise many species with somewhat different functions, different metabolic pathways (Hackmann and Firkins ) and different sensitivities to LA in cultures (Maia et al . ).…”

Section: Dietary Fat Shapes Rumen Microbiotamentioning

confidence: 99%

“…A specific effect of the cis double‐bonds could explain why most known biohydrogenating bacteria produce trans‐ C18:1, but do not further reduce it to stearic acid (see below). Hackmann and Firkins () reported that B. fibrisolvens could be less sensitive to LA than B. hungatei and Butyrivibrio proteoclasticus because its membrane has a lower fluidity due to more palmitic acid and less branched‐chain FA.…”

Section: Dietary Fat Shapes Rumen Microbiotamentioning

confidence: 99%

Rumen microbiota and dietary fat: a mutual shaping

et al. 2017

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Summary Although fat content in usual ruminant diets is very low, fat supplements can be given to farm ruminants to modulate rumen activity or the fatty acid (FA) profile of meat and milk. Unsaturated FAs, which are dominant in common fat sources for ruminants, have negative effects on microbial growth, especially protozoa and fibrolytic bacteria. In turn, the rumen microbiota detoxifies unsaturated FAs (UFAs) through a biohydrogenation (BH) process, transforming dietary UFAs with cis geometrical double‐bonds into mainly trans UFAs and, finally, into saturated FAs. Culture studies have provided a large amount of data regarding bacterial species and strains that are affected by UFAs or involved in lipolysis or BH, with a major focus on the Butyrivibrio genus. More recent data using molecular approaches to rumen microbiota extend and challenge these data, but further research will be necessary to improve our understanding of fat and rumen microbiota interactions.

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“…Through aerobic oxidation, this stored energy can be made readily available to the host for cellular growth and maintenance. During anaerobic fermentation, the coenzyme NAD + is reduced to NADH/H + through a process of substrate linked phosphorylation (Hackmann and Firkins, 2015). For fermentation to continue, NAD + needs to be regenerated (oxidised) by NAD-linked hydrogenases, which are only thermodynamically favourable at low partial pressures of hydrogen.…”

Section: Rumen Fermentationmentioning

confidence: 99%

Microbial Community Structure and Functionality in Ruminants Fed the Probiotic Bacillus amyloliquefaciens H57

Schofield¹

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In the agricultural industry, farmers are continually searching for ways to improve animal production. Developing a more efficient digestive system is one such way that this can be achieved.In domesticated ruminants such as sheep and cattle, the feed material is initially digested in the largest and most prominent compartment of the alimentary canal: the rumen. The rumen is populated by a complex community of microorganisms that are capable of degrading the tough fibrous components of the plant cell wall, releasing fermentable and digestible carbohydrates, proteins, lipids and nucleic acids. Probiotics, defined as "live microorganisms that, when administered in adequate amounts, confer a health benefit on the host", have been used as a means to influence the rumen microbial community to improve the efficiency of feed digestion.In this study we cultivate the probiotic Bacillus amyloliquefaciens strain H57 as an inoculum, to be added to pelleted animal feed in concentrations of 10 9 cfu kg -1 (Chapter 2). To determine the genetic makeup of H57, its genome was sequenced (Chapter 3). The sequence analysis revealed a number of antimicrobial lipopeptides and polyketides, which if expressed in the rumen could significantly alter the rumen microbial community. Other genes of interest within the H57 genome include a number of carbohydrate degrading enzymes as well as those involved with nitrate reduction, which has been recognised as a potential alternative electron acceptor under anaerobic conditions such as the rumen.The H57 inoculum was administered in two animal feeding trials, one using pregnant Dorper ewes and the other using newborn dairy calves. In both instances a significant increase in weight gain was observed in the H57 fed animals compared to the control group. As a means to understand how H57 benefits these animals, the rumen microbial community was profiled by sequencing PCR amplicons of the 16S rRNA gene (Chapter 4). Analysis of the calf rumen microbiome did not reveal any significant differences between the control calves and those that were fed H57 for eight weeks. The only differences in the rumen community occurred between the initial sampling at four weeks and after weaning at eight weeks. In the sheep, however, there was a clear shift in microbial community structure between the control and H57 fed sheep. In both the control and H57 fed sheep the most abundant bacterial populations were Prevotella, although different species were dominant in each treatment group. The H57 fed sheep also had an abundance of Roseburia.Further analysis into the genetic potential and functionality of differentially abundant rumen microorganisms was performed on the sheep samples using metagenomic and metatranscriptomic sequencing. It was found that in the H57 fed sheep the rumen microbial community had an increased expression of hemicellulolytic enzymes, including β-glucosidase/β-galactosidase, α-galactosidase and L-arabinose isomerase. As hemicellulose contributes a significant portion of plant iii cell wall bio...

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Electron transport phosphorylation in rumen butyrivibrios: unprecedented ATP yield for glucose fermentation to butyrate

Cited by 64 publications

References 63 publications

Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short‐chain fatty acids

Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short‐chain fatty acids

Rumen microbiota and dietary fat: a mutual shaping

Microbial Community Structure and Functionality in Ruminants Fed the Probiotic Bacillus amyloliquefaciens H57

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