Identification of Valerate as Carrying Capacity Modulator by Analyzing Lactiplantibacillus plantarum Colonization of Colonic Microbiota in vitro

Julia Isenring; Marc J A Stevens; Christoph Jans; Christophe Lacroix; Annelies Geirnaert

doi:10.3389/fmicb.2022.910609

Identification of Valerate as Carrying Capacity Modulator by Analyzing Lactiplantibacillus plantarum Colonization of Colonic Microbiota in vitro

Front Microbiol. 2022 May 30:13:910609. doi: 10.3389/fmicb.2022.910609. eCollection 2022.

Authors

Julia Isenring¹, Marc J A Stevens^{1

2}, Christoph Jans¹, Christophe Lacroix¹, Annelies Geirnaert¹

Affiliations

¹ Laboratory of Food Biotechnology, Department of Health Sciences and Technology, ETH Zürich, Zürich, Switzerland.
² Institute for Food Hygiene and Safety, University of Zürich, Zürich, Switzerland.

Abstract

Humans ingest many microorganisms, which may colonize and interact with the resident gut microbiota. However, extensive knowledge about host-independent microbe-microbe interactions is lacking. Here, we investigated such colonization process using a derivative of the model probiotic Lactiplantibacillus plantarum WCFS1 into continuously cultivated gut microbiota in the intestinal PolyFermS fermentation model inoculated with five independently immobilized human adult fecal microbiota. L. plantarum successfully colonized and organized itself spatially in the planktonic, that is, the reactor effluent, and sessile, that is, reactor biofilm, fractions of distinct human adult microbiota. The microbiota carrying capacity for L. plantarum was independent of L. plantarum introduction dose and second supplementation. Adult microbiota (n = 3) dominated by Prevotella and Ruminoccocus exhibited a higher carrying capacity than microbiota (n = 2) dominated by Bacteroides with 10⁵ and 10³ CFU/ml of L. plantarum, respectively. Cultivation of human adult microbiota over 3 months resulted in decreased carrying capacity and correlated positively with richness and evenness, suggesting enhanced resistance toward colonizers. Our analyses ultimately allowed us to identify the fermentation metabolite valerate as a modulator to increase the carrying capacity in a microbiota-independent manner. In conclusion, by uncoupling microbe-microbe interactions from host factors, we showed that L. plantarum colonizes the in vitro colonic community in a microbiota-dependent manner. We were further able to demonstrate that L. plantarum colonization levels were not susceptible to the introduction parameters dose and repeated administration but to microbiota features. Such knowledge is relevant in gaining a deeper ecological understanding of colonizer-microbiota interactions and developing robust probiotic strategies.

Keywords: PolyFermS; gut microbiome; intestinal ecology; microbiota invasion; probiotics.