Escherichia coli arbitrarily encompasses facultative anaerobic, rod-shaped bacteria with defined respiratory and fermentative types of metabolism. The species diversification has been further advanced by atypical strains whose features deviate from the essential species-specific morphological and metabolic cut-off. The morphological cut-off is exemplified by bacterial filamentation. E. coli filamentation has been studied from two different perspectives: the first considers filamentation as a result of adaptive strategies and response to stress, while the second is based on findings from the cell division of E. coli’s conditional mutants. Another cut-off is represented by E. coli’s inability to use citrate as a sole carbon and energy source, which can be overcome either by saltational or long-term evolution. In this study, we compared two atypical E. coli strains that belong to the same neuroinvasive ecovar but exhibit either of the two phenotypes that deviate from the species features. While E. coli RS218 exists in the form of filaments incapable of growth on citrate, strain IHE3034 is represented as normal-sized bacteria able to aerobically ferment citrate in the presence of glucose; in this paper we show that these two phenotypes result from a bona fide trade-off. With the help of comparative proteomics and metabolomics, we discovered the proteome required for the upkeep of these phenotypes. The metabolic profiles of both strains reveal that under aerobic conditions, RS218 undergoes oxidative metabolism, while IHE3034 undergoes – anaerobic respiration. Finally, we show that the use of citrate and the filament formation are both linked in a trade-off occurring via a c-di-GMP-dependent phase-variation event.