Transmission of fungi and protozoa under grazing conditions from lactating yaks to sucking yak calves in early life

Abstract

Microbiota from mothers is an essential source of microbes in early-life rumen microbiota, but the contribution of microbiota from different maternal sites to the rumen microbiota establishment in neonates needs more data. To fill this gap, we collected samples from the mouth, teat skin, and rumen of lactating yaks and from the rumen of sucking calves concomitantly on seven occasions between days 7 and 180 after birth under grazing conditions. We observed that the eukaryotic communities clustered based on sample sites, except for the protozoal community in the teat skin, with negative correlations between fungal and protozoal diversities in the rumen of calves. Furthermore, fungi in the dam's mouth, which is the greatest source of the calf's rumen fungi, accounted for only 0.1%, and the contribution of the dam's rumen to the calf's rumen fungi decreased with age and even disappeared after day 60. In contrast, the average contribution of the dam's rumen protozoa to the calf's rumen protozoa was 3.7%, and the contributions from the dam's teat skin (from 0.7 to 2.7%) and mouth (from 0.4 to 3.3%) increased with age. Thus, the divergence in dam-to-calf transmissibility between fungi and protozoa indicates that the foundation of these eukaryotic communities is shaped by different rules. This study provides the first measurements of the maternal contribution to the fungal and protozoal establishment in the rumen of sucking and grazing yak calves in early life, which could be beneficial for future microbiota manipulation in neonatal ruminants. KEY POINTS: • Dam to calf transfer of rumen eukaryotes occurs from multiple body sites. • A minor proportion of rumen fungi in calves originated from maternal sites. • The inter-generation transmission between rumen fungi and protozoa differs.

Keywords: Dam-to-infant transmission; Eukaryotic microbes; Maternal contribution; Rumen microbial development.

Fig. 1

The experimental design depicting collection of samples and data analysis. Rumen, mouth, and teat skin samples of dams and rumen samples of calves were collected from 7 dam-calf pairs from day 7 to day 180 post-partum

Fig. 2

Fungal communities in the maternal and calf samples are diverse and affected by sampling site and time. A Alpha diversity measured by Shannon and Chao1 indices at different sample types across ages. B Non-metric multi-dimensional scaling plot based on Bray–Curtis distances. C UpSet plot showing the number of differential and shared fungal genera among different sample types

Fig. 3

Protozoal communities in the maternal and calf samples are diverse and affected by sampling site and time. A Alpha diversity measured by Shannon and Chao1 indices at different sample types across ages. B Non-metric multi-dimensional scaling plot based on Bray–Curtis distances. C UpSet plot showing the number of differential and shared protozoal genera among different sample types. *P < 0.05, **P < 0.01

Fig. 4

Different fungal communities in the maternal and calf samples. Relative abundances of fungal phyla (A) and genera (B) at different sites across ages. C Comparison of the relative abundances of the main fungi at different sites across ages at the genus level. *P < 0.05, **P < 0.01, ***P < 0.001

Fig. 5

Different protozoal communities in the maternal and calf samples. Relative abundances of protozoal phyla (A) and genera (B) at different sites across ages. C Comparison of the relative abundances of the main protozoa at different sites across ages at the genus level. *P < 0.05, **P < 0.01, ***P < 0.001

Fig. 6

Trans-domain relationships between fungi and protozoa in the rumen of yak calves. A Correlations between fungi and protozoa alpha diversities by Shannon and Chao1 indices in the rumen of yak calves across ages. B Correlations between fungi and protozoa main genera in the rumen of yak calves. *P < 0.05, **P < 0.01. x-axis denotes the main fungal genera while the y-axis denotes the main protozoal genera

Fig. 7

SourceTracker analysis of microbiota from different maternal sites in the rumen of calves. Proportion of rumen fungi (A) and protozoa (B) of yak calves from rumen, mouth, and teat skin (skin) of dams at different age groups. The number of outside circles means the proportion of contributions from different maternal sites to the rumen eukaryotes of calves, and different colors represent different maternal sites. The width of the end point of the band indicates the proportion of different maternal sites