Journal Article

Starvation responses impact interaction dynamics of human gut bacteria Bacteroides thetaiotaomicron and Roseburia intestinalis

Université libre de Bruxelles (ULB), Simoens, Kenneth, Liu, Bin, Gonze, Didier, Krzynowek, Anna, Rega Institute for Medical Research [Leuven] ; Catholic University of Leuven = Katholieke Universiteit Leuven (KU Leuven), Garza, Daniel Rios, Faust, Karoline, Procédés biotechnologiques au service de l'environnement (UR PROSE) ; Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Bernaerts, Kristel, Geirnaert, Annelies

2023

Overview

Abstract Bacterial growth often alters the environment, which in turn can impact interspecies interactions among bacteria. Here, we used an in vitro batch system containing mucin beads to emulate the dynamic host environment and to study its impact on the interactions between two abundant and prevalent human gut bacteria, the primary fermenter Bacteroides thetaiotaomicron and the butyrate producer Roseburia intestinalis. By combining machine learning and flow cytometry, we found that the number of viable B. thetaiotaomicron cells decreases with glucose consumption due to acid production, while R. intestinalis survives post-glucose depletion by entering a slow growth mode. Both species attach to mucin beads, but only viable cell counts of B. thetaiotaomicron increase significantly. The number of viable co-culture cells varies significantly over time compared to those of monocultures. A combination of targeted metabolomics and RNA-seq showed that the slow growth mode of R. intestinalis represents a diauxic shift towards acetate and lactate consumption, whereas B. thetaiotaomicron survives glucose depletion and low pH by foraging on mucin sugars. In addition, most of the mucin monosaccharides we tested inhibited the growth of R. intestinalis but not B. thetaiotaomicron. We encoded these causal relationships in a kinetic model, which reproduced the observed dynamics. In summary, we explored how R. intestinalis and B. thetaiotaomicron respond to nutrient scarcity and how this affects their dynamics. We highlight the importance of understanding bacterial metabolic strategies to effectively modulate microbial dynamics in changing conditions.

• Publisher: Nature Publishing Group,CCSD,Nature Publishing Group UK,Oxford University Press
• Subject: 101/58 / 14/34 / 14/35 / 38/39 / 45/22 / 45/23 / 45/91 / 631/326/2565/2134 / 631/326/2565/855 / Acetic acid / Acid production / Bacteria / Bacteroides - physiology / Bacteroides thetaiotaomicron / Bacteroides thetaiotaomicron - genetics / Beads / Biomedical and Life Sciences / Cell culture / Depletion / Dynamics / Ecology / Evolutionary Biology / Flow cytometry / Glucose / Glucose - metabolism / Humans / Life Sciences / Machine learning / Metabolomics / Microbial Ecology / Microbial Genetics and Genomics / Microbiology / Microorganisms / Monoculture / Monosaccharides / Mucin / Mucins - metabolism / Nutrient dynamics / Roseburia intestinalis