Metabolic division of labor (MDOL) represents one of
the most commonly
occurring interactions within natural microbial communities. Specifically,
in a variety of MDOL systems engaged in hydrocarbon degradation, a
sequential degradation is performed by several members with final
products that are necessary for the growth of each member. In these
MDOL systems, each strain catalyzes one or more specific reactions
of a multistep metabolic pathway, whose end products are then allocated
among the participants. While the benefit allocation is independent
of metabolic flux in well-mixed environments, it remains unclear how
the benefits are allocated when diffusion is limited. Here, we investigated
how MDOL communities assemble in a diffusion-limited environment,
by combining mathematical modeling with experimental inquiry using
a synthetic consortium engaged in MDOL. Our model analysis in a diffusion-limited
environment showed that, when the growth of all populations in the
community relies on the final product that can only be produced by
the last population, a diffusion gradient of the final products may
create a bias favoring the member producing the final products, resulting
in a higher relative abundance of the final product producer. Moreover,
such asymmetric allocation of the final products is enhanced by both
the lower diffusion rate and the higher metabolic flux (i.e., the
higher yields of the final products) in the MDOL. Our results show
that in a diffusively confined environment, metabolic flux constitutes
a determining factor in the assembly of the MDOL community. Together,
our findings are critical for a better understanding of how resource-sharing
microbial communities are established and should assist in designing
such communities for improved biomanufacturing and bioremediation.