Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community

Abstract

ABSTRACTInteractive microbial communities are ubiquitous, influencing biogeochemical cycles and host health. One widespread interaction is nutrient exchange, or cross-feeding, wherein metabolites are transferred between microbes. Some cross-fed metabolites, such as vitamins, amino acids, and ammonium (NH4+), are communally valuable and impose a cost on the producer. The mechanisms that enforce cross-feeding of communally valuable metabolites are not fully understood. Previously we engineered mutualistic cross-feeding between N2-fixingRhodopseudomonas palustrisand fermentativeEscherichia coli. EngineeredR. palustrisexcreted essential nitrogen as NH4+toE. coliwhileE. coliexcreted essential carbon as fermentation products toR. palustris. Here, we enriched for nascent cross-feeding in cocultures with wild-typeR. palustris, not known to excrete NH4+. Emergent NH4+cross-feeding was driven by adaptation ofE. colialone. A missense mutation inE. coliNtrC, a regulator of nitrogen scavenging, resulted in constitutive activation of an NH4+transporter. This activity likely allowedE. colito subsist on the small amount of leaked NH4+and better reciprocate through elevated excretion of organic acids from a largerE. colipopulation. Our results indicate that enhanced nutrient uptake by recipients, rather than increased excretion by producers, is an underappreciated yet possibly prevalent mechanism by which cross-feeding can emerge.