Growth‐independent cross‐feeding modifies boundaries for coexistence in a bacterial mutualism

Abstract

Nutrient cross‐feeding can stabilize microbial mutualisms, including those important for carbon cycling in nutrient‐limited anaerobic environments. It remains poorly understood how nutrient limitation within natural environments impacts mutualist growth, cross‐feeding levels and ultimately mutualism dynamics. We examined the effects of nutrient limitation within a mutualism using theoretical and experimental approaches with a synthetic anaerobic coculture pairing fermentative Escherichia coli and phototrophic Rhodopseudomonas palustris. In this coculture, E. coli and R. palustris resemble an anaerobic food web by cross‐feeding essential carbon (organic acids) and nitrogen (ammonium) respectively. Organic acid cross‐feeding stemming from E. coli fermentation can continue in a growth‐independent manner during nitrogen limitation, while ammonium cross‐feeding by R. palustris is growth‐dependent. When ammonium cross‐feeding was limited, coculture trends changed yet coexistence persisted under both homogenous and heterogenous conditions. Theoretical modelling indicated that growth‐independent fermentation was crucial to sustain cooperative growth under conditions of low nutrient exchange. In contrast to stabilization at most cell densities, growth‐independent fermentation inhibited mutualistic growth when the E. coli cell density was adequately high relative to that of R. palustris. Thus, growth‐independent fermentation can conditionally stabilize or destabilize a mutualism, indicating the potential importance of growth‐independent metabolism for nutrient‐limited mutualistic communities.