Investigation of roles of divalent cations in Shewanella oneidensis pellicle formation reveals unique impacts of insoluble iron

Background

Bacteria adopt a variety of lifestyles in their natural habitats and can alternate among different lifestyles in response to environmental changes. At high cell densities, bacteria can form extracellular matrix encased cell population on submerged tangible surfaces (biofilms), or at the air–liquid interface (pellicles). Compared to biofilm, pellicle lifestyle allows for better oxygen access, but is metabolically more costly to maintain. Further understanding of pellicle formation and environmental cues that influence cellular choices between these lifestyles will definitely improve our appreciation of bacterial interaction with their environments.

Methods

Shewanella oneidensis cells were cultured in 24-well plates with supplementation of varied divalent cations, and pellicles formed under such conditions were evaluated. Mutants defective in respiration of divalent cations were used to further characterize and confirm unique impacts of iron.

Results and conclusions

Small amount of Fe^2 + was essential for pellicle formation, but presence of over-abundant iron (0.3 mM Fe^2 + or Fe^3 +) led to pellicle disassociation without impairing growth. Such impacts were found due to S. oneidensis-mediated formation of insoluble alternative electron acceptors (i.e., Fe₃O₄) under physiologically relevant conditions. Furthermore, we demonstrated that cells preferred a lifestyle of forming biofilm and respiring on such insoluble electron acceptors under tested conditions, even to living in pellicles.

General significance

Our finding suggests that bacterial lifestyle choice involves balanced evaluation of multiple aspects of environmental conditions, and yet-to-be-characterized signaling mechanism is very likely underlying such processes.