Conserved glycan-utilization strategies shape Akkermansiaceae success across aquatic and gut ecosystems.

Abstract

Elucidating interaction mechanisms and substrate specialization is central to understanding bacterial adaptation across ecological niches. Specialized mucin-degrading bacteria of the genus Akkermansia are widely recognized for their beneficial roles in the human gut, yet it remains unclear whether this specialization is unique to the gut or reflects a conserved ecological strategy across different hosts and environments. Here, we show that members of the family Akkermansiaceae share a deeply conserved genetic and mechanistic framework enabling colonization across gut and aquatic ecosystems. Comparative genomics of Akkermansiaceae representatives revealed niche-specific gene repertoires tightly adapted to substrate source and availability. Marine representatives encode distinct combinations of CAZymes and comparatively expanded sulfatase repertoires that enable the degradation of sulfated polysaccharides such as fucoidan, a recalcitrant substrate linked to carbon sequestration. Structural predictions and comparisons identified a conserved molecular system centered on a type IV-like pilus that mediates attachment to complex, fucose-rich glycans. The genes underlying this system are syntenic with the recently described mucin utilization locus in Akkermansia muciniphila, revealing an evolutionary continuity between aquatic and gut lineages. Seawater incubations with fluorescently labeled substrates confirmed fucoidan uptake and degradation by marine Akkermansiaceae. Together, these results reveal a unified glycan-utilization strategy spanning the environmental breadth of Akkermansiaceae and provide a mechanistic framework linking ecological success in marine environments to traits associated with probiotic functions in the human gut.