Spatial segregation as a necessity for beneficial gene loss in cross-feeding bacterial communities: a kinetic perspective on the Black Queen Hypothesis

Cross-feeding communities are common across diverse environments, such as soil, water, and host microbiomes. The Black Queen Hypothesis (BQH) [1] asserts that some metabolic functions are leaky and thus provide a public resource within a community. The public resource allows some community members to lose genes for the production of that resource as long as at least one member continues to produce the resource. Nitrogen fixation as a process that leaks ammonium is used as an example to explain why only certain prokaryotes encode nitrogenase. We explore the emergence of mutualistic cross-feeding in bacterial cocultures in the context of the BQH. We pair a slow-growing nitrogen-fixing cooperator with fast-growing fermentative partners that can either also fix nitrogen gas or require the product, ammonium. We demonstrate that spatial heterogeneity is necessary for the emergence of a partner strain that loses nitrogen-fixation.

[1] Morris, J.J., Lenski, R.E. and Zinser, E.R., 2012. The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. MBio, 3(2), pp.e00036-12.