Intestinal microbiomes as complex ecosystems: Implications for intervention strategies

There are clear associations between colonization with intestinal microbiomes and the development of the mucosal immune system and of metabolic function. In laboratory rodents, single microbial species can expand whole sections of the immune system and colonization of gnotobiotic pigs with an oligobiota has similar effects. However, in the field, young animals rapidly become colonized with complex microbiomes acquired from their mothers and from the environment. These are a complex set of spatially-linked microbiomes in which oral, gastric, duodenal, jejunal, ileal, cecal and colonic compartments are sequential ecosystems: each compartment acquires microorganisms from the previous compartment and then contributes microorganisms to the next. Once intestinal microbiomes are considered as a set of sequentially-dependent, complex ecosystems, it is apparent that the strategies we use to manipulate them may need to be similarly complex to provide robust, predictable results over multiple units and management systems. Many trials document the administration of single organisms to weaning or growing pigs resulting in measurable change in some parameters and these effects are interpreted as direct effects of the administered organisms (“probiotics”) on host physiology. However, while this interpretation might be acceptable in a gnotobiotic system, it is less so where the probiotic competes with existing, complex ecosystems. In addition, the documented effects frequently vary between trials or disappear once applied in real-world husbandry systems. We propose that most administered ‘probiotics’ and prebiotics, and of many nutritional interventions act indirectly, by modifying the existing, complex spectrum of sequentially-dependent microbiomes. As a corollary, we propose that their effectiveness is dependent on the composition of the existing, complex set of microbiomes. Characterization and manipulation of the current, baseline microbiomes in a specific unit may be necessary before administration of nutritional interventions. In addition, microbial consortia may be more effective in modifying these microbiomes than single organisms.

Key Words: microbiome, ecosystem, probiotic, immunology.

Presented at the 9th Symposium on Gut Health in Production of Food Animals, St. Louis, USA, 2021. For information on the next edition, click here.