Ecology of the multi-kingdom human gut microbiota assembly: insights from preterm infants
The new-born human gut is like a desert island for the microbiota: in fact, it evolves predictably with pioneer species colonizing the gut after birth, followed by an ordered succession of microorganisms. This colonizing process can be studied in a privileged manner in preterm infants, as well as the potentially shaping influences of the environment, the host and interactions between microorganisms in such a complex ecosystem.
To identify the specific role of any individual factor, Chitong Rao et al. used multi-kingdom absolute abundance quantification, ecological modelling and experimental validation. By quantifying the absolute dynamics of bacteria, fungi and archaea in a longitudinal cohort of 178 preterm infants, they uncovered microbial blooms and extinctions, and showed an inverse correlation between bacterial and fungal loads in the infant gut. They also infer computationally and demonstrate experimentally in vitro and in vivo – in mouse models – that predictable assembly dynamics may be driven by directed, context-dependent interactions between specific microorganisms: for example, a late-arriving bacterium, Klebsiella, exploits the pioneer one, Staphylococcus, to gain ground within the gut. Notably, interactions between different kingdoms were found to influence assembly: a single fungal species — Candida albicans – was able to inhibit multiple dominant genera of gut bacteria.
Therefore, they demonstrated that the predictable patterns of assembly of the preterm infant gut microbiota can be driven by direct, context-dependent interactions between specific microorganism strains. In fact, there seems to be a common mechanism of assembly between the infant microbiota and macroscopic ecological succession. Just as in macroscopic ecosystems, microorganisms may exploit one another to establish within the infant gut, and direct interactions between kingdoms appear to have a central role in community dynamics. In other words, we – as humans – are some sort of a microcosmic version of a rainforest or the Blue River.
The very reducibility of gut microbiota assembly to simple, pair-wise interactions has important implications for understanding and ultimately manipulating microbial ecosystems in health and disease.
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