Abstract
The FUT2 gene encodes an α-1,2-fucosyltransferase responsible for the expression of ABO histo-blood-group antigens on mucosal surfaces and bodily secretions. Individuals who carry at least one functional allele are known as “secretors,” whereas those homozygous for loss-of-function mutations are known as “non-secretors.” Non-secretor individuals are more susceptible to chronic inflammatory disorders such as Crohn’s Disease, which may be mediated by alterations in the microbiota. Here, we investigated the dynamics of microbial community assembly with respect to genotype using a Fut2-deficient mouse model, taking the genotype of the maternal lineage over two generations into account. We found strong differences in community assembly of microbial communities over time, depending on the Fut2 genotype of the host and that of their progenitors. By applying network analyses, we further identified patterns of specialization and stabilization over time, which are influenced by the host and parental genotype during the process of community development. We also show genotype- and breeding-dependent patterns of community susceptibility to disturbance in a novel in silico approach integrating ecological- and network analysis. Our results indicate that it may be important to investigate the influence of Fut2 genotype in a familial context in order to fully understand its role in the etiology of chronic inflammatory disorders.
Highlights
The host-associated microbiota represent a complex phenotype composed of diverse microbial taxa and functions with important contributions to host fitness
To explore the microbial communities at a basic level, we first investigated the dynamics of the major microbial taxonomic groups over time and among locations of the gastrointestinal tract (GIT; intestinal tissue sampled in mature mice, approx. 15 weeks of age/11 weeks after weaning)
When we consider the interaction of Fut2 genotype and breeding direction we find mainly differences according to differential abundance in the fecal bacterial communities 1, 3, and 5-weeks after weaning (Figure 3 and Supplementary Tables S7, S8)
Summary
The host-associated microbiota represent a complex phenotype composed of diverse microbial taxa and functions with important contributions to host fitness. The well-known α-1,2fucosyltransferase encoded by the FUT2 gene is responsible for the presence of ABH blood-group antigens in bodily secretions and displays widespread variation among human populations (Liu et al, 1998; Koda et al, 2000; Pang et al, 2001), characterized by loss-of-function mutations that disrupt glycan fucosylation (i.e., the “non-secretor” phenotype) (Koda et al, 2000) These sugar chains represent an important source of nutrients and attachment sites for resident bacteria (Hooper and Gordon, 2001), and represent a target for pathogens (Thom et al, 1989; Ilver et al, 1998; Lindesmith et al, 2003; Ruiz-Palacios et al, 2003). Non-secretor status is associated with increased susceptibility to chronic inflammatory disorders such as Crohn disease (McGovern et al, 2010), possibly due to changes in the intestinal microbiota (Rausch et al, 2011; Wacklin et al, 2011, 2014; Tong et al, 2014)
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