Longitudinal shifts in bacterial diversity and fermentation pattern in the rumen of steers grazing wheat pasture

doi:10.1016/j.anaerobe.2014.07.008

Anaerobe

Volume 30, December 2014, Pages 11-17

https://doi.org/10.1016/j.anaerobe.2014.07.008 Get rights and content

Highlights

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Rumen bacterial diversity in steers associated with grazing wheat pasture.
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Rumen bacterial communities dominated by Bacteroidetes and Firmicutes.
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Relevance of Bacteroidetes:Firmicutes ratio to animal health and production.
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Connection between microbiome and fermentation pattern in the rumen illustrated.

Abstract

Grazing steers on winter wheat forage is routinely practiced in the Southern Great Plains of the US. Here, we investigated the dynamics in bacterial populations of both solid and liquid ruminal fractions of steers grazing on maturing wheat forage of changing nutritive quality. The relationship between bacterial diversity and fermentation parameters in the liquid fraction was also investigated. During the first 28 days, the wheat was in a vegetative phase with a relatively high crude protein content (CP; 21%), which led to the incidence of mild cases of frothy bloat among steers. Rumen samples were collected on days 14, 28, 56 and 76, separated into solid and liquid fractions and analyzed for bacterial diversity using 16S pyrotag technology. The predominant phyla identified were Bacteroidetes (59–77%) and Firmicutes (20–33%) across both ruminal fractions. Very few differences were observed in the rumen bacterial communities within solid and liquid fractions on day 14. However, by day 28, the relatively high CP content complemented a distinct bacterial and chemical composition of the rumen fluid that was characterized by a higher ratio (4:1) of Bacteroidetes:Firmicutes and a corresponding lower acetate:propionate (3:1) ratio. Further, a greater accumulation of biofilm (mucopolysaccharide complex) on day 28 was strongly associated with the abundance of Firmicutes lineages such as Clostridium, Ruminococcus, Oscillospira and Moryella (P < 0.05) in the fiber fraction. Such changes were diminished as the CP concentration declined over the course of the study. The abundance of Firmicutes was noticeable by 76 d in both fractions which signifies the development of a core microbiome associated with digestion of a more recalcitrant fiber in the mature wheat. This study demonstrates dynamics in the rumen microbiome and their association with fermentation activity in the rumen of steers during the vegetative (bloat-prone) and reproductive stages of wheat forage.

Introduction

Hard-red winter wheat (Triticum aestivum) is an annual cool-season crop frequently managed for grain production as well as high-quality forage for beef cattle in the Southern Great Plains [1], [2], [3], [4], [5], [6]. Wheat forage production varies from season to season [2] and the quality and quantity of forage are dependent on a combination of factors such as precipitation, nitrogen (N) fertilization, and cultivar [7], [8]. Weight gains of 1.4 kg/day were reported in stocker cattle when maintained on wheat forage [9], and prolonged grazing led to greater profit potential [4].

Vegetative wheat is succulent, characterized by high crude protein (CP; 18–34%) and low neutral detergent fiber (NDF; 30–40%) values [4]. The CP content of vegetative wheat is comprised by a higher proportion of soluble fractions which undergo rapid fermentation in the rumen, resulting in the production of a mucopolysaccharide complex known as biofilm [3], [5]. Fermentation gases are entrapped in this biofilm result in the progressive distention of the rumen culminating in bloat. Frothy bloat in cattle is a metabolic disorder caused by the complex interactions between the structural and chemical composition of wheat forage, animal genetic factors, environmental conditions and rumen microbial activity [3], [5], [10], [11], [12]. Frothy bloat remains a challenge to most beef farmers as it reduces animal performance or results in mortality among stocker cattle [4].

Variation in the rumen microbiome can contribute substantially to the incidence of frothy bloat. Previously, we identified distinct microbial community composition between bloated and non-bloated steers utilizing denaturing gradient gel electrophoresis [3]. Monitoring shifts in community microbial populations has become less cumbersome with the employment of next generation sequencing technology. Utilizing this technology we demonstrated shifts in bacterial communities when steers transitioned from Bermudagrass hay to winter wheat. Further, we identified that both solid and liquid fractions of ruminal contents had distinct clustering patterns based on community composition associated with each diet [13], [14]. In the present study, we investigated the dynamics in bacterial populations of both solid and liquid ruminal fractions of steers grazing wheat forage of changing nutritive quality associated with advancing phenological development. Further, we attempted to determine the associative changes between the ruminal microbial community structure and the chemical composition of the rumen fluid when steers succumbed to wheat-induced frothy bloat.

Section snippets

Materials and methods

In the present study, fourteen ruminally cannulated (Angus and Hereford cross) steers were moved to graze a 20 ha wheat (T. aestivum; var Fannin) pasture at the Smith-Walker Research Unit (Vernon, Texas) for experimental grazing. During all phases of development and the experimental period, steers were provided ad libitum access to water and a complete mineral supplement. All animal surgical, management and research procedures were conducted under animal use protocols approved by the Texas A&M

Nutritive value of wheat

During the experimental period, the nutritive value of the wheat varied as a function of phenological development and precipitation patterns (Table 1). The wheat forage in February was in a vegetative phase characterized by 21% CP and 80% IVDMD. The nutritive quality of the wheat declined as it turned reproductive beginning in mid-March. Emerging seed heads were evident during the last 2 weeks of the experiment and the wheat had a nutritive value of 13% CP, 70% IVDMD, and 50% NDF. Overall,

Discussion

This study demonstrates the longitudinal shifts in the rumen bacterial populations of steers while grazing a progressively maturing pasture of wheat. Fiber and liquid ruminal fractions were analyzed individually as the bacterial community composition of each fraction is known to vary with time based on the physiological, anatomical and structural components of forage [13], [14], [22], [23], [24]. Further, the relationship between bacterial diversity and fermentation parameters in the liquid

Conclusions

This study is the first to report interrelationships of changing nutritive value with advancing plant phenologic development to shifts/adaptations in bacterial population dynamics and structure across rumen fractions in a relatively large number of cattle in a grazing environment. The composition of the rumen microbiome changed over time in a manner consistent with increased plant fiber and decreased protein content as wheat grew from the vegetative through reproductive phases of maturity.

Acknowledgment

The authors would like to thank Diamond V Mills, Inc. for the funding support granted to Texas AgriLife Research Center to undertake this study.

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Molecular biology, genetics and biotechnologyLongitudinal shifts in bacterial diversity and fermentation pattern in the rumen of steers grazing wheat pasture

Highlights

Abstract

Introduction

Section snippets

Materials and methods

Nutritive value of wheat

Discussion

Conclusions

Acknowledgment

Anim Feed Sci Technol

Vet Clin N Am Food Anim Pract

J Dairy Sci

Anaerobe

Anaerobe

Animal

Anaerobe

Anaerobe

FEMS Microbiol Rev

J Dairy Sci

Effect of monensin or ruminal fermentation, forage intake and weight gains of wheat pasture stocker cattle

J Anim Sci

Interrelationships of forage and steer growth dynamics on wheat pasture

J Range Manage

Effects of condensed tannins supplementation level on weight gain and in vitro and in vivo bloat precursors in steers grazing winter wheat

J Anim Sci

Yield and economic responses to phosphorus fertilizer placement in dual-use and grain-only wheat production systems

Agron J

Simulated growing-season precipitation and nitrogen effects on winter wheat yield

Agron J

Effect of nitrogen fertilisation on diurnal phenolic concentration and foam strength in forage of hard red wheat (Triticum aestivum L.) cv. Cutter

Crop Pasture Sci

Occurrence of condensed tannins in wheat and feasibility for reducing pasture bloat

Crop Sci

Bloat in cattle: XXIX. The foaming properties of clover proteins

N Z J Agric Res

Bloat in cattle

Rumen bacterial diversity dynamics associated with changing from bermudagrass hay to grazed winter wheat diets

Microb Ecol

Properties of a slime isolated from the rumen fluid of cattle bloating on clover pasture

J Anim Sci

Performance and forage utilization by beef cattle receiving increasing amounts of alfalfa hay as a supplement to low-quality, tallgrass-prairie forage

J Anim Sci

Official methods of analysis

Molecular biology, genetics and biotechnology
Longitudinal shifts in bacterial diversity and fermentation pattern in the rumen of steers grazing wheat pasture