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. 2023 Dec 21:10:1272835.
doi: 10.3389/fvets.2023.1272835. eCollection 2023.

Enhancing rumen microbial diversity and its impact on energy and protein metabolism in forage-fed goats

Affiliations

Enhancing rumen microbial diversity and its impact on energy and protein metabolism in forage-fed goats

Alejandro Belanche et al. Front Vet Sci. .

Abstract

Introduction: This study explores if promoting a complex rumen microbiota represents an advantage or a handicap in the current dairy production systems in which ruminants are artificially reared in absence of contact with adult animals and fed preserved monophyte forage.

Methods: In order to promote a different rumen microbial diversity, a total of 36 newborn goat kids were artificially reared, divided in 4 groups and daily inoculated during 10 weeks with autoclaved rumen fluid (AUT), fresh rumen fluid from adult goats adapted to forage (RFF) or concentrate (RFC) diets, or absence of inoculation (CTL). At 6 months of age all animals were shifted to an oats hay diet to determine their ability to digest a low quality forage.

Results and discussion: Early life inoculation with fresh rumen fluid promoted an increase in the rumen overall microbial diversity which was detected later in life. As a result, at 6 months of age RFF and RFC animals had higher bacterial (+50 OTUs) and methanogens diversity (+4 OTUs) and the presence of a complex rumen protozoal community (+32 OTUs), whereas CTL animals remained protozoa-free. This superior rumen diversity and presence of rumen protozoa had beneficial effects on the energy metabolism allowing a faster adaptation to the forage diet, a higher forage digestion (+21% NDF digestibility) and an energetically favourable shift of the rumen fermentation pattern from acetate to butyrate (+92%) and propionate (+19%) production. These effects were associated with the presence of certain rumen bacterial taxa and a diverse protozoal community. On the contrary, the presence of rumen protozoa (mostly Entodinium) had a negative impact on the N metabolism leading to a higher bacterial protein breakdown in the rumen and lower microbial protein flow to the host based on purine derivatives urinary excretion (-17% to -54%). The inoculation with autoclaved rumen fluid, as source of fermentation products but not viable microbes, had smaller effects than using fresh inoculum. These findings suggest that enhancing rumen microbial diversity represents a desirable attribute when ruminants are fed forages in which the N supply does not represent a limiting factor for the rumen microbiota.

Keywords: energy metabolism; forage digestion; multi-kingdom; protein metabolism; protozoa; rumen microbiota; ruminants.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

Figures

Figure 1
Figure 1
Ilustration of the diferent stages of the experimental set up. Animals received an daily and oral inoculation with autoclaved rumen fluid (AUT), rumen fluids from adult animals fed forage (RFF), or fed concentrate diets (RFC) or without inoculation (CTL).
Figure 2
Figure 2
Box plot illustrating the rumen multi-kingdom diversity in terms of richness (A) and Shannon’s index (B) in 26-week-old goats measured at 21 days after a shift from a high-concentrate to a full forage diet (oats hay). During the first 10 weeks of age, goats (N = 36) received a daily and oral inoculation with autoclaved rumen fluid (AUT), rumen fluid from adult animals fed forage (RFF), or fed concentrate diets (RFC) or without inoculation (CTL). Principal coordinates analysis (C) illustrating relationships (ρ > 0.4) between the structure of the rumen microbiota and productive data. PERMANOVA values are provided based on the Bray–Curtis dissimilarity.
Figure 3
Figure 3
Principal Coordinate Analysis illustrating the structure of the rumen bacteria (A), methanogens (B), protozoa (C) and anaerobic fungi community (D) in 26-week-old goats measured at 21 days after a shift from a high-concentrate to a full forage diet (oats hay). During the first 10 weeks of age, goats (N = 36) received a daily and oral inoculation with autoclaved rumen fluid (AUT), rumen fluid from adult animals fed forage (RFF), or fed concentrate diets (RFC) or without inoculation (CTL). Relationships (ρ > 0.4) between the structure of the rumen microbiota and productive data are shown along with PERMANOVA values based on the Bray–Curtis dissimilarity.

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