Among the first microorganisms to colonize the human gut of breastfed infants are bacteria capable of fermenting human milk oligosaccharides (HMOs). One of the most abundant HMOs, 2′-fucosyllactose (2′-FL), may specifically drive bacterial colonization of the intestine. Recently, differential growth has been observed across multiple species of
Akkermansia
on various HMOs including 2′-FL. In culture, we found growth of two species,
A. muciniphila
Muc
T
and
A. biwaensis
CSUN-19,on HMOs corresponded to a decrease in the levels of 2′-FL and an increase in lactose, indicating that the first step in 2′-FL catabolism is the cleavage of fucose. Using phylogenetic analysis and transcriptional profiling, we found that the number and expression of fucosidase genes from two glycoside hydrolase (GH) families, GH29 and GH95, vary between these two species. During the mid-log phase of growth, the expression of several GH29 genes was increased by 2′-FL in both species, whereas the GH95 genes were induced only in
A. muciniphila
. We further show that one putative fucosidase and a β-galactosidase from
A. biwaensis
are involved in the breakdown of 2′-FL. Our findings indicate that the plasticity of GHs of human-associated
Akkermansia
sp. enables access to additional growth substrates present in HMOs, including 2′-FL. Our work highlights the potential for
Akkermansia
to influence the development of the gut microbiota early in life and expands the known metabolic capabilities of this important human symbiont.
IMPORTANCE
Akkermansia
are mucin-degrading specialists widely distributed in the human population.
Akkermansia biwaensis
has recently been observed to have enhanced growth relative to other human-associated
Akkermansia
on multiple human milk oligosaccharides (HMOs). However, the mechanisms for enhanced growth are not understood. Here, we characterized the phylogenetic diversity and function of select genes involved in the growth of
A. biwaensis
on 2′-fucosyllactose (2′-FL), a dominant HMO. Specifically, we demonstrate that two genes in a genomic locus, a putative β-galactosidase and α-fucosidase, are likely responsible for the enhanced growth on 2′-FL. The functional characterization of
A. biwaensis
growth on 2′-FL delineates the significance of a single genomic locus that may facilitate enhanced colonization and functional activity of select
Akkermansia
early in life.