Growth of the marine luminous bacterium Vibrio fischeri on 3':5'-cyclic AMP: correlation with a periplasmic 3':5'-cyclic AMP phosphodiesterase

Abstract

Summary: The marine luminous bacterium Vibrio fischeri, the species-specific light-organ symbiont of monocentrid (pinecone) fish, grew on 3′:5′-cyclic adenosine monophosphate (cAMP) as a sole source of carbon and energy, a capability not previously described in bacteria. In a minimal, chemically defined medium containing cAMP as the sole source of carbon and energy, V. fischeri cells grew more slowly than on glucose or ribose, but as quickly as on 5′-AMP. Expression of luminescence, which is dependent on cAMP in V. fischeri, was stimulated in cells grown on cAMP compared to cells grown on glucose or ribose. All strains of V. fischeri tested (MJ-1, B-61, ATCC 7744, MJ-A1, CG-A1) grew on cAMP, as did strains of two other marine luminous bacteria, V. logei and Photobacterium phosphoreum, and strains of the terrestrial enteric bacterium Serratia marcescens. Other tested species of marine luminous bacteria (P. leiognathi, Shewanella [Alteromonas] hanedai, V. harveyi, V. orientalis, V. splendidus) and terrestrial enteric bacteria (Escherichia coli, Salmonella typhimurium), which grew on 5′-AMP or ribose, did not grow on cAMP. Assays on intact cells and periplasmic extracts revealed that V. fischeri MJ-1 produced a periplasmic 3′:5′-cAMP phosphodiesterase (cAMP phosphodiesterase) of very high specific activity [9·0 μmol phosphate released (mg protein)−1 min−1] and narrow substrate specificity (3′:5′-cAMP and 3′:5′-cGMP were attacked). The novel periplasmic location and unusually high activity of cAMP phosphodiesterase appear to account for the ability of this species to grow on cAMP. The periplasmic cAMP phosphodiesterase of V. fischeri night play a role in degrading free cAMP in seawater or in a cAMP-mediated aspect of the light organ symbiosis with monocentrid fish.