Trade-off between oxygen and iron acquisition in bacterial cells at the air-liquid interface

The air-liquid interface is a selectively advantageous niche for aerobes due to the accessibility to oxygen. Various species of aerobes form a biofilm-like structure at air-liquid interfaces, known as a pellicle. Although the pellicle is one of the major growth modes of microorganisms, the metabolic features of pellicle cells and the determinative factors for pellicle formation are largely unknown. In this study, we investigated the factors affecting pellicle growth by the facultative aerobe Pseudomonas aeruginosa, and also examined the gene expression profiles of pellicle cells in order to characterize features of the pellicle lifestyle. A mutant strain deficient in the production of exopolysaccharides displayed poor pellicle-forming ability and a growth disadvantage under static conditions compared with the wild-type strain. Notably, supplementation of culture medium with an alternative electron acceptor, nitrate, led to diminished pellicle formation. Nitrate facilitated the growth of an anaerobic planktonic cell subpopulation that acted as a competitor for iron with the aerobic subpopulation, resulting in the observed pellicle reduction. Transcriptome analysis revealed that pellicle cells were under aerobic and iron-depleted states. Thus, although pellicle formation certainly confers a growth advantage under static conditions, pellicle cells face a nutritional trade-off between oxygen and iron acquisition.