Gut Bacteria Shape Intestinal Microhabitats Occupied by the Fungus Candida albicans

Abstract

The human gut microbiota is composed of diverse microbes that not only compete but also rely on one another for resources and access to microhabitats in the intestine [1, 2]. Indeed, recent efforts to map the microbial biogeography of the gastrointestinal tract have revealed positive and negative co-associations between bacterial taxa [3, 4]. Here, we examine the spatial organization that the most prominent fungus of the human flora, Candida albicans, adopts in the gut of gnotobiotic mice either as the sole colonizer or in the presence of single bacterial species. We observe that, as a lone colonizer, C.albicans cells are distributed either adjacent to the inner mucus layer in the colon or throughout the intestinal lumen. In contrast to this pattern, in the presence of the saccharolytic Bacteroides thetaiotaomicron, the fungal cells localize to the interior of a Bacteroides-promoted outer mucus layer in which fungal and bacterial cells are in close association. We show that, invitro, although mucin provides minimal support to the proliferation of the fungus, barely altering its transcriptional landscape, Bacteroides- and glucanase-processed mucin can better fuel the growth of C.albicans. Our observations illustrate how a commensal fungus can settle in an intestinal microhabitat generated by the presence of a single gut bacterial taxon.