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Fibrobacter communities in the gastrointestinal tracts of diverse hindgut-fermenting herbivores are distinct from those of the rumen.

ABSTRACT: The genus Fibrobacter contains cellulolytic bacteria originally isolated from the rumen. Culture-independent investigations have since identified Fibrobacter populations in the gastrointestinal tracts of numerous hindgut-fermenting herbivores, but their physiology is poorly characterized due to few representative axenic cultures. To test the hypothesis that novel Fibrobacter diversity exists in hindgut fermenters, we performed culturing and 16S rRNA gene amplicon sequencing on samples collected from phylogenetically diverse herbivorous hosts. Using a unique approach for recovering axenic Fibrobacter cultures, we isolated 45 novel strains from 11 different hosts. Full-length 16S rRNA gene sequencing of these isolates identified nine discrete phylotypes (cutoff = 0.03%) among them, including several that were only isolated from hindgut-fermenting hosts, and four previously unrepresented by axenic cultures. Our phylogenetic analysis indicated that six of the phylotypes are more closely related to previously described subspecies of Fibrobacter succinogenes, while the remaining three were more closely related to F. intestinalis. Culture-independent bacterial community profiling confirmed that most isolates were representative of numerically dominant phylotypes in their respective samples and strengthened the association of certain phylotypes with either ruminants or hindgut-fermenters. Despite considerable phylogenetic diversity observed among the Fibrobacter strains isolated here, phenotypic characterization suggests a conserved specialization for growth on cellulose.

SUBMITTER: Neumann AP

PROVIDER: S-EPMC5599356 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Effects of subacute ruminal acidosis (SARA) challenges on the bacteria in rumen fluid, cecal digesta, and feces of dairy cows were determined using 16S rRNA gene pyrosequencing and real-time quantitative PCR. Six non-lactating Holstein cows with cannulas in the rumen and cecum were used in a 3 × 3 Latin square arrangement of treatments. During the first 3 wk of each experimental period, cows received a control diet containing 70% forages on a dry matter (DM) basis. In wk 4 of each period, cows received one of three diets: (1) the control diet; (2) a diet in which 34% of the dietary DM was replaced with pellets of ground wheat and barley (GBSC); or (3) a diet in which 37% of dietary DM was replaced with pellets of ground alfalfa (APSC). Rumen fluid, cecal digesta and feces were collected on d 5 of wk 4 of each period and the composition of the bacterial community was studied. Rumen fermentation responses were reported in a companion study. Both SARA-inducing challenges resulted in similar digesta pH depressions (as shown by the companion study), and reduced bacterial richness and diversity in rumen fluid, but GBSC had the larger effect. None of the challenges affected these measures in cecal digesta, and only GBSC reduced bacterial richness and diversity in feces. Only GBSC reduced the abundance of Bacteroidetes in rumen fluid. Abundances of limited number of bacterial genera identified by 16S rRNA gene sequencing in the rumen, cecum and feces were affected by the GBSC. The APSC did not affect any of these abundances. Both challenges increased the abundances of several starch, pectin, xylan, dextrin, lactate, succinate, and sugar fermenting bacterial species in the rumen, cecum, and feces as determined by qPCR. Only GBSC increased that of Megasphaera elsdenii in the rumen. Both challenges decreased the abundance of Streptococcus bovis, and increased that of Escherichia coli, in cecal digesta and feces, with GBSC having the larger effect. These results showed that the SARA challenges caused moderate and reversible changes of the composition of the bacteria in the foregut and hindgut, with the greater changes observed during GBSC.

Project description:Fibrobacter succinogenes is a cellulolytic bacterium that plays an essential role in the degradation of plant fibers in the rumen ecosystem. It converts cellulose polymers into intracellular glycogen and the fermentation metabolites succinate, acetate, and formate. We developed dynamic models of F. succinogenes S85 metabolism on glucose, cellobiose, and cellulose on the basis of a network reconstruction done with the automatic reconstruction of metabolic model workspace. The reconstruction was based on genome annotation, five template-based orthology methods, gap filling, and manual curation. The metabolic network of F. succinogenes S85 comprises 1,565 reactions with 77% linked to 1,317 genes, 1,586 unique metabolites, and 931 pathways. The network was reduced using the NetRed algorithm and analyzed for the computation of elementary flux modes. A yield analysis was further performed to select a minimal set of macroscopic reactions for each substrate. The accuracy of the models was acceptable in simulating F. succinogenes carbohydrate metabolism with an average coefficient of variation of the root mean squared error of 19%. The resulting models are useful resources for investigating the metabolic capabilities of F. succinogenes S85, including the dynamics of metabolite production. Such an approach is a key step toward the integration of omics microbial information into predictive models of rumen metabolism. IMPORTANCE F. succinogenes S85 is a cellulose-degrading and succinate-producing bacterium. Such functions are central for the rumen ecosystem and are of special interest for several industrial applications. This work illustrates how information of the genome of F. succinogenes can be translated to develop predictive dynamic models of rumen fermentation processes. We expect this approach can be applied to other rumen microbes for producing a model of rumen microbiome that can be used for studying microbial manipulation strategies aimed at enhancing feed utilization and mitigating enteric emissions.

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Fibrobacter communities in the gastrointestinal tracts of diverse hindgut-fermenting herbivores are distinct from those of the rumen.

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