Ratios of rumen inoculum from Tibetan and Small-tailed Han sheep influenced in vitro fermentation and digestibility

https://doi.org/10.1016/j.anifeedsci.2020.114562Get rights and content

Highlights

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    Fermentation of Tibetan (TBI) and Small-tailed Han sheep rumen inocula (HSI) differed.

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    CH4 and H2 decreased with an increase in proportion of TBI.

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    Nutrient digestibilities increased with an increase in proportion of TBI.

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    Ratios of TBI: HSI inocula affected estimated Gibbs energy changes.

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    Metabolic hydrogen fluxes were shifted by ratios of TBI: HSI inocula.

Abstract

Tibetan sheep are well adapted to harsh environmental conditions and poor-quality forage and are known to produce less methane (CH4) gas than lowland sheep. In this study, rumen inocula from Tibetan sheep (TBI) and from Small-tailed Han sheep (HSI) were incubated in in vitro batch cultures in five ratios (TBI: HSI): 0:100, 25:75, 50:50, 75:25 or 100:0 for 72 h. With an increasing proportion of TBI, there was a linear decrease (P < 0.001) in gas and CH4 production on a degraded dry matter (DM) basis at 12, 24, 48 and 72 h. In addition, increasing the proportion of TBI increased the digestibility of DM (P < 0.05), neutral detergent fiber and acid detergent fiber and total and individual volatile fatty acids (VFA) concentrations at almost all time points. An increase in the TBI: HSI ratio resulted in less metabolic hydrogen ([2H]) incorporated into CH4 and more into propionate. The recovery of [2H] consistently decreased with an increase in the TBI: HSI ratio, indicating the existence of unaccounted [2H] in TBI. It would be important to study the rumen microbiome in Tibetan sheep with the use of classical microbiology and modern –omics techniques to identify [2H] sinks alternative to CH4, which could perhaps be stimulated in other domestic ruminants.

Introduction

The high-altitude Tibetan plateau is characterized by severe cold, low air and oxygen partial pressure, strong ultraviolet light and a short forage growing season (Long et al., 2008). Winters are particularly severe for grazing livestock as forage availability is often inadequate and of low quality. Yaks and Tibetan sheep are indigenous and well adapted to the region and their rumen microbiota have shown convergence of phenotypes related to energy metabolism (Zhang et al., 2016). They are able to utilize poor-quality forage of low protein content more efficiently than lowland ruminants (Wang, 2009; Zhou et al., 2019), with a resulting higher nutrient digestibility, volatile fatty acids (VFA) concentration and microbial protein (MCP) synthesis, and lower methane (CH4) production (Wang, 2009; Ding et al., 2010).

A number of rumen microbiology studies have been undertaken in an attempt to improve fiber digestion and ruminal fermentation efficiency, however, with little success (Weimer, 2015). Altering or enhancing rumen fermentation efficiency by transferring rumen inocula between ruminant breeds has shown some potential. For example, in vitro NDF digestibility and total VFA concentration (Oss et al., 2016), and in vivo protein digestibility (Ribeiro et al., 2017) increased in cattle (Bos taurus) receiving rumen inoculum or rumen contents from bison (Bison bison). In addition, a transfer of rumen inoculum from water buffalo to cattle increased both ruminal VFA and ammonia concentrations in cattle (Pamungkas et al., 2004). Young calves that received rumen contents from Holstein heifers exhibited a change in liver transcriptome and an increase in rumen microbiota abundance (Li et al., 2019), while lambs (Zhong et al., 2014) and bulls (Leo-Penu et al., 2016) that received rumen inocula from adults of their respective species increased feed intake. The rumen microbial transfer between breeds, the subject of this study, offers potential for manipulating the rumen function and reshaping rumen microbiota.

Previous studies have shown that Tibetan sheep and Small-tailed Han sheep differ in their rumen fermentation end products, which is associated with their different microbiomes and regulation of fermentation pathways (Zhang et al., 2016). In vitro fermentation techniques (IVFT) can be used to study and compare the effects of different sources of ruminal inocula on the digestion and fermentation of nutrients (Bueno et al., 2015; Zhang et al., 2016). Thus, we hypothesized that adding Tibetan sheep rumen inoculum to Small-tailed Han sheep inoculum would decrease CH4 production in vitro and would improve fermentation efficiency and nutrient digestibility. Our objective was to compare digestion and fermentation of oat hay in vitro using different ratios of inocula from Tibetan and Small-tailed Han sheep.

Section snippets

Study site, animals and feed

The study was conducted in November-December, 2016, at the Tibetan Ruminant Research Station (3154 m altitude; 37°12.4′N and 102°51.7′E), Nanniwan Village, Tianzhu Tibetan Autonomous County (northeastern Qinghai-Tibetan Plateau), Gansu Province, China. All procedures on the sheep followed the guidelines and protocols approved by the Animal Ethics Committee of Lanzhou University.

Six Tibetan sheep (body weight = 48.0 ± 1.41 kg) and six Small-tail Han sheep (body weight = 49.4 ± 1.55 kg), all

Results

Increasing the proportion of TBI in the inoculum decreased total GP from 48 h onwards and CH4 production and H2 accumulation from 24 h onwards (P < 0.05; Fig. 1). Asymptotic GP and CH4 and GP lag time decreased linearly (P < 0.05), whereas the GP fractional production rate (c) increased linearly (P < 0.001), with an increase in TBI (Table 2). There were treatment × time interactions for GP and CH4 production on a degraded DM basis (P < 0.001; Table 2). Methane production and GP on a degraded DM

Effect of rumen inoculum mix on gas production and digestibility

With an increase in fiber digestibility, there is generally an increase in GP in rumen fermentation (Sandoval-Castro et al., 2005; Alonso-Díaz et al., 2009). In this study, however, with an increase in the proportion of TBI, there was an increase in fiber digestibility but there was a decrease in GP. This result is difficult to explain, because in addition to greater fiber digestion, the TBI resulted in a VFA profile with greater acetate to propionate molar ratio. The production of acetate from

Conclusions

With the substrate and incubation conditions of this study, an increase in TBI inoculum reduced GP and decreased methanogenesis after 48 h of incubation, and increased DM and fiber digestibility. Microorganisms and microbial processes in TBI inoculum can be of interest to study [2H] sinks alternative to methanogenesis. Future research could study this microbial ecosystem with the use of metagenomics, metatranscriptomics and metaproteomics. It is possible that some sinks of [2H] alternative to CH

CRediT authorship contribution statement

Weiwei Wang: Conceptualization, Investigation, Formal analysis, Software, Writing - original draft. Emilio M. Ungerfeld: Conceptualization, Formal analysis, Writing - review & editing. A. Allan Degen: Formal analysis, Writing - review & editing. Xiaoping Jing: Investigation, Resources, Formal analysis. Wei Guo: Investigation, Formal analysis. Jianwei Zhou: Project administration, Formal analysis. Xiaodan Huang: Formal analysis. Shah Mudassar: Writing - review & editing. Fuyu Shi: Formal

Declaration of Competing Interest

The authors declare that no competing interests.

Acknowledgement

We thank the three reviewers for very helpful comments. This research was funded by the National Natural Science Foundation of China (31672453); The International Atomic Energy Agency IAEA (Research Contact No. 20769/R0); Transformation Program of Qinghai (2018-SF-145); International Science and Technology Cooperation Base of Mountain Eco-Agriculture of Gansu (054000037). The authors thank Jianjun Wang and Deli Liu for sample collections.

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