Stability and volatility shape the gut bacteriome and Kazachstania slooffiae dynamics in preweaning, nursery and adult pigs

Abstract

The gut microbiome plays important roles in the maintenance of health and pathogenesis of diseases in the growing host. In order to fully comprehend the interplay of the gut microbiome and host, a foundational understanding of longitudinal microbiome, including bacteria and fungi, development is necessary. In this study, we evaluated enteric microbiome and host dynamics throughout the lifetime of commercial swine. We collected a total of 234 fecal samples from ten pigs across 31 time points in three developmental stages (5 preweaning, 15 nursery, and 11 growth adult). We then performed 16S rRNA gene amplicon sequencing for bacterial profiles and qPCR for the fungus Kazachstania slooffiae. We identified distinct bacteriome clustering according to the host developmental stage, with the preweaning stage exhibiting low bacterial diversity and high volatility amongst samples. We further identified clusters of bacteria that were considered core, increasing, decreasing or stage-associated throughout the host lifetime. Kazachstania slooffiae was absent in the preweaning stage but peaked during the nursery stage of the host. We determined that all host growth stages contained negative correlations between K. slooffiae and bacterial genera, with only the growth adult stage containing positive correlates. Our stage-associated bacteriome results suggested the neonate contained a volatile gut microbiome. Upon weaning, the microbiome became relatively established with comparatively fewer perturbations in microbiome composition. Differential analysis indicated bacteria might play distinct stage-associated roles in metabolism and pathogenesis. The lack of positive correlates and shared K. slooffiae-bacteria interactions between stages warranted future research into the interactions amongst these kingdoms for host health. This research is foundational for understanding how bacteria and fungi develop singularly, as well as within a complex ecosystem in the host’s gut environment.

Core-predominant gut fungus Kazachstania slooffiae promotes intestinal epithelial glycolysis via lysine desuccinylation in pigs

“…Thus, K. slooffiae might exhibit powerful metabolic activities in the intestinal tract and plays a critical regulatory role in host metabolism. Previous studies have also identified K. slooffiae as a member of the intestinal yeasts in pigs [ 7 , 30 , 38 , 86 , 112 – 117 ] and have shown that K. slooffiae can produce some bioactive substances, such as peptides, formic acid, and dehydroascorbic acid [ 118 ]. The total nitrogen and amino acid contents of K. slooffiae were higher than those of S. cerevisiae [ 118 ].…”

Weaning transition, but not the administration of probiotic candidate Kazachstania slooffiae, shaped the gastrointestinal bacterial and fungal communities in nursery piglets

“…We have previously reported increasing Shannon alpha diversity values with less variability over time in the fecal bacteriome of piglets through the weaning transition ( 15 , 16 ). The current study found that alpha diversity of the fecal bacteriome increased between day 14 to day 21 and remained constant between day 21 and day 49.…”

“…This taxon is the dominant species of Kazachstania in the piglet around the weaning transition ( 16 ). K. slooffiae has been detected as early as 3 days after birth ( 46 ), and abundance peaks shortly after weaning ( 14 ), but decreases as the piglet matures past the growing phase into adulthood ( 15 ). Previously, we collected samples at day 35 (weaned at day 21), and K. slooffiae was indeed a dominant fungal community in the mycobiome at this time ( 14 ).…”

“…Based on our past work, we have been able to detect K. slooffiae as early as 1 week after the transition to a grain-based diet after weaning ( 16 ). Others have been unable to detect K. slooffiae before the nursery period ( 15 ), thus indicating the possibility that K. slooffiae abundance increases in response to dietary changes after weaning.…”

“…Previously, characterization of the fecal microbiome as a representation of the gastrointestinal tract was important due to its noninvasive nature. However, bacterial and fungal colonization differs markedly between regions of the GI tract (13)(14)(15)(16). Therefore, a complete observation of discrete spatial microbiomes in conjunction with the fecal microbiome, which is representative of the transfer of content between these regions, can reveal more information about the potential for disease state in piglets during this critical transition.…”