Differential Colonization of Plant Parts by the Rumen Microbiota is likely to be due to Different Forage Chemistries

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

doi:10.4172/1948-5948.1000126

Cited by 17 publications

(21 citation statements)

References 42 publications

(51 reference statements)

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“…The process of colonizing ingested plant material by the rumen microbiome is rapid (Cheng et al, 1980; Miron et al, 2001; Russell and Rychlik, 2001; Koike et al, 2003a; Edwards et al, 2007, 2008b; Huws et al, 2013, 2014b, 2016), and eventually these populations form mature biofilms encompassed in self-produced polymeric substances (EPS) (Akin, 1976; Cheng et al, 1980, 1981; McAllister et al, 1994; Huws et al, 2013; Leng, 2014). We have previously shown that bacterial diversity attached to fresh perennial ryegrass (PRG) incubated within the rumen is different prior to 4 h and post 4 h of incubation, thus demonstrating that colonization undergoes primary (up to 4 h) and secondary (after 4 h) events, respectively (Huws et al, 2013, 2014b, 2016). Nonetheless, the functionality of the primary and secondary colonizers in terms of plant degradation and availability of nutrients to the host remains unclear.…”

Section: Introductionmentioning

confidence: 99%

Temporal Metagenomic and Metabolomic Characterization of Fresh Perennial Ryegrass Degradation by Rumen Bacteria

et al. 2016

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Understanding the relationship between ingested plant material and the attached microbiome is essential for developing methodologies to improve ruminant nutrient use efficiency. We have previously shown that perennial ryegrass (PRG) rumen bacterial colonization events follow a primary (up to 4 h) and secondary (after 4 h) pattern based on the differences in diversity of the attached bacteria. In this study, we investigated temporal niche specialization of primary and secondary populations of attached rumen microbiota using metagenomic shotgun sequencing as well as monitoring changes in the plant chemistry using mid-infrared spectroscopy (FT-IR). Metagenomic Rapid Annotation using Subsystem Technology (MG-RAST) taxonomical analysis of shotgun metagenomic sequences showed that the genera Butyrivibrio, Clostridium, Eubacterium, Prevotella, and Selenomonas dominated the attached microbiome irrespective of time. MG-RAST also showed that Acidaminococcus, Bacillus, Butyrivibrio, and Prevotella rDNA increased in read abundance during secondary colonization, whilst Blautia decreased in read abundance. MG-RAST Clusters of Orthologous Groups (COG) functional analysis also showed that the primary function of the attached microbiome was categorized broadly within “metabolism;” predominantly amino acid, carbohydrate, and lipid metabolism and transport. Most sequence read abundances (51.6, 43.8, and 50.0% of COG families pertaining to amino acid, carbohydrate and lipid metabolism, respectively) within these categories were higher in abundance during secondary colonization. Kyoto encyclopedia of genes and genomes (KEGG) pathways analysis confirmed that the PRG-attached microbiota present at 1 and 4 h of rumen incubation possess a similar functional capacity, with only a few pathways being uniquely found in only one incubation time point only. FT-IR data for the plant residues also showed that the main changes in plant chemistry between primary and secondary colonization was due to increased carbohydrate, amino acid, and lipid metabolism. This study confirmed primary and secondary colonization events and supported the hypothesis that functional changes occurred as a consequence of taxonomical changes. Sequences within the carbohydrate metabolism COG families contained only 3.2% of cellulose activities, on average across both incubation times (1 and 4 h), suggesting that degradation of the plant cell walls may be a key rate-limiting factor in ensuring the bioavailability of intra-plant nutrients in a timely manner to the microbes and ultimately the animal. This suggests that a future focus for improving ruminant nutrient use efficiency should be altering the recalcitrant plant cell wall components and/or improving the cellulolytic capacity of the rumen microbiota.

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Section: Introductionmentioning

confidence: 99%

Temporal Metagenomic and Metabolomic Characterization of Fresh Perennial Ryegrass Degradation by Rumen Bacteria

et al. 2016

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“…It is well established that forage-based diets promote increased bacterial diversity when compared to starch-based diets [60–63]. However, the role of particle size therein is unclear, as differences in the structural fiber composition and resulting bioavailability of nutrients that occur among plant species can select for distinct microbial communities [64]. In the present study, a smaller particle size feed increased bacterial diversity and sheep performance, likely by improving protein digestion of feed.…”

Section: Discussionmentioning

confidence: 55%

Pelleted-hay alfalfa feed increases sheep wether weight gain and rumen bacterial richness over loose-hay alfalfa feed

Ishaq

Lachman

Wenner

et al. 2019

Preprint

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24Diet composed of smaller particles can improve feed intake, digestibility, and animal growth or 25 health, but in ruminant species can reduce rumination and buffering -the loss of which may inhibit 26 fermentation and digestibility. However, the explicit effect of particle size on the rumen 27 microbiota remains untested, despite their crucial role in digestion. We evaluated the effects of 28 reduced particle size on rumen microbiota by feeding long-stem (loose) alfalfa hay compared to a 29 ground and pelleted version of the same alfalfa in yearling sheep wethers. In situ digestibility of 30 the pelleted diet was greater at 48 h compared with loose hay; however, distribution of residual 31 fecal particle sizes in sheep did not differ between the dietary treatments at any time point. Both 32 average daily gain and feed efficiency were greater for the wethers consuming the pelleted diet. 33 Observed bacterial richness was very low at the end of the adaptation period and increased over 34 the course of the study, suggesting the rumen bacterial community was still in flux after two weeks 35 of adaptation. The pelleted-hay diet group had a greater increase in bacterial richness, including 36 common fibrolytic rumen inhabitants. The pelleted diet was positively associated with several 37 Succiniclasticum, a Prevotella, and uncultured taxa in the Ruminococcaceae and Rickenellaceae 38 families and Bacteroidales order. Pelleting an alfalfa hay diet for sheep does shift the rumen 39 microbiome, though the interplay of diet particle size, retention and GI transit time, microbial 40 fermentative and hydrolytic activity, and host growth or health is still largely unexplored. 42It has been well established that the nutrient composition of a diet affects the 43 gastrointestinal tract (GIT) microbiota [1,2], yet the physical structure and complexity of the diet 44 may also alter its interactions with the GIT microbiota and host. In cattle, longer fiber particles 45 have been shown to improve rumination [3] and ultimately fiber digestibility [4]. However, shorter 46 or smaller diet particles can change the dynamics of digestion and produce a number of favorable 47 outcomes. Specifically, reductions in particle size associated with mastication or mechanized 48 processing correspond to increases in feed surface area and thus allow for greater microbial 49 attachment and relative fibrolytic and fermentative activities as has been shown in vitro [5]. 50Mechanical breakdown during diet preparation can also physically disrupt waxy plant cuticles and 51 cell walls that can otherwise impede microbial attachment and degradation, thus making plant 52 carbohydrates more available [6] and decreasing the potential confounding effect of forage 53 fragility within the rumen [7]. Hydrolytic activities are also likely further enhanced by the 54 reductions in buoyancy and increased functional specific gravity [8] associated with reduced 55 particle size, that would allow smaller particles to sink beneath the dorsally-located rumen mat ...

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“…According to Huws et al. (), heterogeneity of plant structures has a profound effect on attached bacterial diversity and on IVDMD.…”

Section: Discussionmentioning

confidence: 99%

“…After these tissues were degraded (48 hr), microbiota populations were also attached to lignified components of the leaf (vessels of the xylem and fibers), with a reduction in degradation evident (Figure 3g,h). According to Huws et al (2014), heterogeneity of plant structures has a profound effect on attached bacterial diversity and on IVDMD.…”

Section: Microbial Attachment and Cw Degradationmentioning

confidence: 99%

“…Festulolium , a cross hybrid, combines Lolium high yield, palatability, quality and rapid establishment with Festuca persistence and resistance to cold and dry climates in addition to showing regrowth capacity and resistance to biotic and abiotic factors (Ghesquière, Humphreys, & Zwierzkowski, ). The production and nutritional quality of cool‐season pasture during a year is highest between 4 and 6 weeks of regrowth (Hodgson, ), as occurs in Lolium perenne (Velasco‐Zebadúa, Hernández‐Garay, & González‐Hernández, ), and conversion of plant protein to microbial protein in the rumen is inefficient because only approximately 30% of ingested nitrogen is retained for meat and milk production (Huws et al., ).…”

Section: Introductionmentioning

confidence: 99%

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Histochemical changes in early and mature Festulolium and maturation's effects on rumen bacteria activity and in vitro degradation

et al. 2018

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The nutritional quality of grasses decreases with maturity due to increases in content of cell wall (CW) and lignified tissue, which affect the degradation and fermentation variables of the grasses. The effect of leaf age and tissue‐microbial attachment during the degradation of Festulolium at 28 and 35 days of regrowth was evaluated in vitro by gas production. Fragments from the middle part of the blade of Festulolium leaves were stained for lignin with phloroglucinol solution, and the lignified area was measured. Subepidermal fibers of the abaxial and adaxial central vein of leaves contributed most to the lignification of Festulolium at 35 days compared with that at 28 days. Variables of gas production and concentrations of volatile fatty acids and ammonia nitrogen were affected by regrowth age. Activity for cellulases (8.19 IU/g dry matter [DM]) was highest between 12 and 16 hr of incubation and for xylanases between 16 and 24 hr (51.09 IU/g DM) without differences between regrowth ages. Scanning electron microscopy showed the following sequence: primary CW degradation started at 12 hr, a large population of microbiota were attached to CWs with extracellular protein complexes at 24 hr, and microbiota were attached to lignified cells at 48 hr. Therefore, during in vitro CW degradation of Festulolium, enzymatic activities increased before microbiota attachment to CWs, which was maintained when xylanase activity declined. Thus, structural analysis conducted using histochemistry and scanning electron microscopy helped to characterize the degradation of plant tissues and the interactions with ruminal microorganisms.

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Differential Colonization of Plant Parts by the Rumen Microbiota is likely to be due to Different Forage Chemistries

Cited by 17 publications

References 42 publications

Temporal Metagenomic and Metabolomic Characterization of Fresh Perennial Ryegrass Degradation by Rumen Bacteria

Temporal Metagenomic and Metabolomic Characterization of Fresh Perennial Ryegrass Degradation by Rumen Bacteria

Pelleted-hay alfalfa feed increases sheep wether weight gain and rumen bacterial richness over loose-hay alfalfa feed

Histochemical changes in early and mature Festulolium and maturation's effects on rumen bacteria activity and in vitro degradation

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