Successional colonization of perennial ryegrass by rumen bacteria

Huws, Sharon; Mayorga, Olga; Theodorou, Michael K.; Onime, Lucy A.; Kim, Eun Joong; Cookson, A. H.; Newbold, C. J.; Kingston‐Smith, Alison H.

doi:10.1111/lam.12033

Cited by 49 publications

(56 citation statements)

References 32 publications

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“…Prevotella is one of the most predominant bacterial genera found in the rumen, accounting for up to 20 % of the total bacteria found in sheep (Bekele et al 2010), between 14 and 60 % in dairy cows (Kong et al 2010; Stevenson and Weimer, 2007) and up to 90 % in steers (Huws et al 2010; 2013). The publication of the P. ruminicola 23 and Prevotella bryantii B(1)4 genomes (Purushe et al 2010) may explain why most of the fosmid sequences were similar to these entries as only limited information on other rumen bacteria is currently deposited.…”

Section: Discussionmentioning

confidence: 99%

Isolation and characterization of novel lipases/esterases from a bovine rumen metagenome

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Newbold

Kaderbhai

et al. 2015

Appl Microbiol Biotechnol

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Improving the health beneficial fatty acid content of meat and milk is a major challenge requiring an increased understanding of rumen lipid metabolism. In this study, we isolated and characterized rumen bacterial lipases/esterases using functional metagenomics. Metagenomic libraries were constructed from DNA extracted from strained rumen fluid (SRF), solid-attached bacteria (SAB) and liquid-associated rumen bacteria (LAB), ligated into a fosmid vector and subsequently transformed into an Escherichia coli host. Fosmid libraries consisted of 7,744; 8,448; and 7,680 clones with an average insert size of 30 to 35 kbp for SRF, SAB and LAB, respectively. Transformants were screened on spirit blue agar plates containing tributyrin for lipase/esterase activity. Five SAB and four LAB clones exhibited lipolytic activity, and no positive clones were found in the SRF library. Fosmids from positive clones were pyrosequenced and twelve putative lipase/esterase genes and two phospholipase genes retrieved. Although the derived proteins clustered into diverse esterase and lipase families, a degree of novelty was seen, with homology ranging from 40 to 78 % following BlastP searches. Isolated lipases/esterases exhibited activity against mostly short- to medium-chain substrates across a range of temperatures and pH. The function of these novel enzymes recovered in ruminal metabolism needs further investigation, alongside their potential industrial uses.Electronic supplementary materialThe online version of this article (doi:10.1007/s00253-014-6355-6) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Isolation and characterization of novel lipases/esterases from a bovine rumen metagenome

Privé

Newbold

Kaderbhai

et al. 2015

Appl Microbiol Biotechnol

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“…Primary colonisers attach to newly ingested forage particles, exude extracellular polymeric substances and then develop into biofilm colonies on perennial ryegrass leaf, for instance, in less than 1 h (Huws et al 2013). Bacteria have evolved signalling mechanisms that enable them to communicate and co-ordinate their activities so that they can respond quickly to environmental changes (such as establishment of nearby bacteria or the presence of nutrients or toxins); they exhibit a wide range of interactive, multicellular behaviors such as dispersal, nutrient acquisition, biofilm formation and quorum sensing (West et al 2006).…”

Section: The Importance Of Rumen Microbial Ecologymentioning

confidence: 99%

Interactions between microbial consortia in biofilms: a paradigm shift in rumen microbial ecology and enteric methane mitigation

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2014

Anim. Prod. Sci.

140

105

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Abstract. Minimising enteric CH 4 emissions from ruminants is a current research priority because CH 4 contributes to global warming. The most effective mitigation strategy is to adjust the animal's diet to complement locally available feed resources so that optimal production is gained from a minimum of animals. This essay concentrates on a second strategy -the use of feed additives that are toxic to methanogens or that redirect H 2 (and electrons) to inhibit enteric CH 4 emissions from individual animals. Much of the published research in this area is contradictory and may be explained when the microbial ecology of the rumen is considered.Rumen microbes mostly exist in organised consortia within biofilms composed of self-secreted extracellular polymeric substances attached to or within feed particles. In these biofilms, individual colonies are positioned to optimise their use of preferred intermediates from an overall process of organic matter fermentation that generates end-products the animal can utilise. Synthesis of CH 4 within biofilms prevents a rise in the partial pressure of H 2 (pH 2 ) to levels that inhibit bacterial dehydrogenases, and so reduce fermentation rate, feed intake and digestibility. In this context, hypotheses are advanced to explain changes in hydrogen disposal from the biofilms in the rumen resulting from use of anti-methanogenic feed additives as follows.Nitrate acts as an alternative electron sink when it is reduced via NO 2 -to NH 3 and CH 4 synthesis is reduced. However, efficiency of CH 4 mitigation is always lower than that predicted and decreases as NO 3 -ingestion increases. Suggested reasons include (1) variable levels of absorption of NO 3 -or NO 2 -from the rumen and (2) increases in H 2 production. One suggestion is that NO 3 -reduction may lower pH 2 at the surface of biofilms, thereby creating an ecological niche for growth of syntrophic bacteria that oxidise propionate and/or butyrate to acetate with release of H 2 .Chlorinated hydrocarbons also inhibit CH 4 synthesis and increase H 2 and formate production by some rumen methanogens. Formate diffuses from the biofilm and is converted to HCO 3 -and H 2 in rumen fluid and is then excreted via the breath. Short-chain nitro-compounds inhibit both CH 4 and formate synthesis when added to ruminal fluid but have little or no effect in redirecting H 2 to other sinks, so the pH 2 within biofilms may increase to levels that support reductive acetogenesis. Biochar or activated charcoal may also alter biofilm activity and reduce net CH 4 synthesis; direct electron transfer between microbes within biofilms may also be involved. A final suggestion is that, during their sessile life stage, protozoa interact with biofilm communities and help maintain pH 2 in the biofilm, supporting methanogenesis.

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Section: Introductionmentioning

confidence: 99%

“…Previous studies have shown temporal changes in bacterial (Edwards et al, 2007; Huws et al, 2013) and fungal (Edwards et al, 2008) populations during ruminal incubation of fresh perennial rye grass ( Lolium perenne ). Specifically, these studies revealed a rapid colonization of the plant material within 5 min of rumen-incubation by both bacterial (Edwards et al, 2007) and fungal populations, followed by a compositional shift in bacterial populations between 2 and 4 h following incubation (Huws et al, 2013). Compositional dynamics may vary among forage types based on observed differences in fiber disappearance and fibrolytic enzyme activities (Bowman and Firkins, 1993) and the observed temporal changes in microbiota may be affected by residual plant metabolism of fresh forages (Huws et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…Specifically, these studies revealed a rapid colonization of the plant material within 5 min of rumen-incubation by both bacterial (Edwards et al, 2007) and fungal populations, followed by a compositional shift in bacterial populations between 2 and 4 h following incubation (Huws et al, 2013). Compositional dynamics may vary among forage types based on observed differences in fiber disappearance and fibrolytic enzyme activities (Bowman and Firkins, 1993) and the observed temporal changes in microbiota may be affected by residual plant metabolism of fresh forages (Huws et al, 2013). Here we provide evidence that similar temporal changes occur during the in situ incubation of dried switchgrass and correspond to changes in methanogen abundance.…”

Section: Introductionmentioning

confidence: 99%

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Temporal dynamics of fibrolytic and methanogenic rumen microorganisms during in situ incubation of switchgrass determined by 16S rRNA gene profiling

et al. 2014

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The rumen microbial ecosystem is known for its biomass-degrading and methane-producing phenotype. Fermentation of recalcitrant plant material, comprised of a multitude of interwoven fibers, necessitates the synergistic activity of diverse microbial taxonomic groups that inhabit the anaerobic rumen ecosystem. Although interspecies hydrogen (H2) transfer, a process during which bacterially generated H2 is transferred to methanogenic Archaea, has obtained significant attention over the last decades, the temporal variation of the different taxa involved in in situ biomass-degradation, H2 transfer and the methanogenesis process remains to be established. Here we investigated the temporal succession of microbial taxa and its effect on fiber composition during rumen incubation using 16S rRNA amplicon sequencing. Switchgrass filled nylon bags were placed in the rumen of a cannulated cow and collected at nine time points for DNA extraction and 16S pyrotag profiling. The microbial community colonizing the air-dried and non-incubated (0 h) switchgrass was dominated by members of the Bacilli (recruiting 63% of the pyrotag reads). During in situ incubation of the switchgrass, two major shifts in the community composition were observed: Bacilli were replaced within 30 min by members belonging to the Bacteroidia and Clostridia, which recruited 34 and 25% of the 16S rRNA reads generated, respectively. A second significant shift was observed after 16 h of rumen incubation, when members of the Spirochaetes and Fibrobacteria classes became more abundant in the fiber-adherent community. During the first 30 min of rumen incubation ~13% of the switchgrass dry matter was degraded, whereas little biomass degradation appeared to have occurred between 30 min and 4 h after the switchgrass was placed in the rumen. Interestingly, methanogenic members of the Euryarchaeota (i.e., Methanobacteria) increased up to 3-fold during this period of reduced biomass-degradation, with peak abundance just before rates of dry matter degradation increased again. We hypothesize that during this period microbial-mediated fibrolysis was temporarily inhibited until H2 was metabolized into CH4 by methanogens. Collectively, our results demonstrate the importance of inter-species interactions for the biomass-degrading and methane-producing phenotype of the rumen microbiome—both microbially facilitated processes with global significance.

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Successional colonization of perennial ryegrass by rumen bacteria

Cited by 49 publications

References 32 publications

Isolation and characterization of novel lipases/esterases from a bovine rumen metagenome

Isolation and characterization of novel lipases/esterases from a bovine rumen metagenome

Interactions between microbial consortia in biofilms: a paradigm shift in rumen microbial ecology and enteric methane mitigation

Temporal dynamics of fibrolytic and methanogenic rumen microorganisms during in situ incubation of switchgrass determined by 16S rRNA gene profiling

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