Comparison of microbial populations in model and natural rumens using 16S ribosomal RNA‐targeted probes

Members of the domain Archaea contribute about 0.3 to 3.3% of the microbial small subunit (16S and 18S) rRNA in the rumen (22,39,60). Archaea have a range of different metabolisms and are found in many habitats (6), but those known to exist in the rumen are strictly anaerobic methanogens. Yanagita et al. (59) observed that 2.8 to 4.0% of ruminal microorganisms displayed autofluorescence characteristic of F 420 , a methanogen cofactor, able to be seen under UV illumination during microscopy. Taken together with the small subunit rRNA abundance data, this suggests that a large part of the archaeal population is made up of methanogens. Most species of methanogens can grow using H 2 and often formate as their energy sources and use the electrons derived from H 2 (or formate) to reduce CO 2 to CH 4 . Some species can grow with methyl groups, oxidizing some to CO 2 to produce electrons that are used to reduce further methyl groups to methane. A few species can grow with acetate, effectively dissimilating acetate to CH 4 and CO 2 . However, acetate is not metabolized to CH 4 to any significant extent in the rumen (13). This is probably because the rate of passage of rumen contents through the rumen is greater than the growth rate of acetateutilizing methanogens (53).In a normally functioning rumen, proteins and polymeric carbohydrates, which usually make up the largest part of the incoming feed, are fermented by a mixed microbial community to volatile fatty acids (VFAs), NH 4 ϩ , CO 2 , and H 2 . The hydrogen is metabolized by the methanogens. The VFAs are taken up by the animal across the rumen wall and serve as major carbon and energy sources for the ruminant. A part of the VFAs, undigested feed components, and microbial cells leave the rumen and enter the rest of the animal's digestive tract. The central role of H 2 in the rumen fermentation (12) means that, although methanogenic archaea make up only a small part of the rumen microbial biomass, they play an important role in rumen function and animal nutrition. Efficient H 2 removal leads to a nutritionally more favorable pattern of VFA formation and to an increased rate of fermentation by eliminating the inhibitory effect of H 2 on the microbial fermentation (26, 53).The rumen can be simplistically described as an open system with discontinuous solid (feed) and liquid (saliva and drinking water) inputs and multiple fractions that have different turnover rates (53). The methanogens in the rumen are found free in the rumen fluid, attached to particulate material and rumen protozoa, associated as endosymbionts within rumen protozoa, and attached to the rumen epithelium. The methanogens associated with these different fractions can be expected to have different growth rates since they will be removed from the rumen at different rates. In addition, the animal itself and the feed also influence the rate of passage of digesta through the rumen system (25). These different habitats may allow niche division among the methanogens and may explain some of the observed phyloge...

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Structure of the Archaeal Community of the Rumen

Janssen

Kirs

2008

Appl Environ Microbiol

534

472

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“…The collective activity of glycoside hydrolases is often greater than the sum of the individual enzyme activities, as a result of their synergistic interactions. Synergistic effects among endoglucanases, exoglucanases, and ␤-glucosidases have been reported, and the exoglucanases have a central role in cellulose degradation (25).Fibrobacter succinogenes has a major role in biodegradation of plant cell wall polymers in the rumen, based on its predominance in the rumens of animals ingesting a forage diet (30,37,41) and its capacity to digest plant cell walls during growth (8 …”

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Characterization and Synergistic Interactions of Fibrobacter succinogenes Glycoside Hydrolases

Meng

Jun

Forsberg

2007

Appl Environ Microbiol

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The objectives of this study were to characterize Fibrobacter succinogenes glycoside hydrolases from different glycoside hydrolase families and to study their synergistic interactions. The gene encoding a major endoglucanase (endoglucanase 1) of F. succinogenes S85 was identified as cel9B from the genome sequence by reference to internal amino acid sequences of the purified native enzyme. Cel9B and two other glucanases from different families, Cel5H and Cel8B, were cloned and overexpressed, and the proteins were purified and characterized. These proteins in conjunction with two predominant cellulases, Cel10A, a chloride-stimulated cellobiosidase, and Cel51A, formerly known as endoglucanase 2 (or CelF), were assayed in various combinations to assess their synergistic interactions using ball-milled cellulose. The degree of synergism ranged from 0.6 to 3.7. The two predominant endoglucanases produced by F. succinogenes, Cel9B and Cel51A, were shown to have a synergistic effect of up to 1.67. Cel10A showed little synergy in combination with Cel9B and Cel51A. Mixtures containing all the enzymes gave a higher degree of synergism than those containing two or three enzymes, which reflected the complementarity in their modes of action as well as substrate specificities.The degradation of complex plant cell wall polysaccharides, such as cellulose and hemicellulose, by cellulolytic microorganisms is one of the major steps of the global carbon cycle. Cellulolytic organisms typically produce multiple glycoside hydrolases that act in concert, releasing mono-and oligosaccharides from the polysaccharides. The collective activity of glycoside hydrolases is often greater than the sum of the individual enzyme activities, as a result of their synergistic interactions. Synergistic effects among endoglucanases, exoglucanases, and ␤-glucosidases have been reported, and the exoglucanases have a central role in cellulose degradation (25).Fibrobacter succinogenes has a major role in biodegradation of plant cell wall polymers in the rumen, based on its predominance in the rumens of animals ingesting a forage diet (30,37,41) and its capacity to digest plant cell walls during growth (8

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“…Two species, Fibrobacter intestinalis and Fibrobacter succinogenes have been characterized based on 16S rRNA sequences and phenotypic properties. Both F. intestinalis and F. succinogenes are present in the rumen and ceca of cattle, pigs, and rats (3,19,30,42). Of these two species F. succinogenes has received the most attention because of its substantially higher fibrolytic activity (28,42).…”

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“…Both F. intestinalis and F. succinogenes are present in the rumen and ceca of cattle, pigs, and rats (3,19,30,42). Of these two species F. succinogenes has received the most attention because of its substantially higher fibrolytic activity (28,42). Genetic studies have identified seven cellulases and four xylanases, and have also shown that cellulose-binding proteins are important for the cellulolytic activity of this strain (9).…”

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Novel Molecular Features of the Fibrolytic Intestinal Bacterium Fibrobacter intestinalis Not Shared with Fibrobacter succinogenes as Determined by Suppressive Subtractive Hybridization

Meng

Nelson²,

Daugherty³

et al. 2005

J Bacteriol

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Suppressive subtractive hybridization was conducted to identify unique genes coding for plant cell wall hydrolytic enzymes and other properties of the gastrointestinal bacterium Fibrobacter intestinalis DR7 not shared by Fibrobacter succinogenes S85. Subtractive clones from F. intestinalis were sequenced and assembled to form 712 nonredundant contigs with an average length of 525 bp. Of these, 55 sequences were unique to F. intestinalis. The remaining contigs contained 764 genes with BLASTX similarities to other proteins; of these, 80% had the highest similarities to proteins in F. succinogenes, including 30 that coded for carbohydrate active enzymes. The expression of 17 of these genes was verified by Northern dot blot analysis. Of genes not exhibiting BLASTX similarity to F. succinogenes, 30 encoded putative transposases, 6 encoded restriction modification genes, and 45% had highest similarities to proteins in other species of gastrointestinal bacteria, a finding suggestive of either horizontal gene transfer to F. intestinalis or gene loss from F. succinogenes. Analysis of contigs containing segments of two or more adjacent genes revealed that only 35% exhibited BLASTX similarity and were in the same orientation as those of F. succinogenes, indicating extensive chromosomal rearrangement.

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Comparison of microbial populations in model and natural rumens using 16S ribosomal RNA‐targeted probes

Cited by 73 publications

References 36 publications

Structure of the Archaeal Community of the Rumen

Structure of the Archaeal Community of the Rumen

Characterization and Synergistic Interactions of Fibrobacter succinogenes Glycoside Hydrolases

Novel Molecular Features of the Fibrolytic Intestinal Bacterium Fibrobacter intestinalis Not Shared with Fibrobacter succinogenes as Determined by Suppressive Subtractive Hybridization

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