Interactions of Phototropism and Gravitropism in Cyanobacteria

While gene expression in bacteria has been shown to be affected by near-zero or extremely high gravity, a mechanism has not been established to date. In larger organisms, gravity-sensing mechanisms usually rely on a dense body applying directional pressure which can be detected by the cell. Herein we demonstrate a means of observing the effect of gravity on cyanobacteria by differential expression of native pigments in response to both gravity and light. We observe that in the cyanobacterium Synechococcus sp. PCC 7002, the distribution of pigmentation within the cell, and across cell colonies, is regulated by combined directional sensing of incoming light, adhesion to a surface via extracellular matrix, and applied external force, including the normal force of gravity applied to the cell. Cells grown on a substrate orient their thylakoids on the cell faces proximal and distal to the substrate and locate both chlorophyll and phycobilins in both of these membrane regions; phycobilins are primarily targeted to the membrane region nearest to the light source, while chlorophyll is preferentially expressed in the region opposite the overall external force applied to the cell. The mechanism for distribution of pigments appears to be regulated by presence of polyphosphate bodies within the cell, and removal of polyphosphate negates the cells ability to sense external forces. Furthermore, colonial morphology is affected by application of force, with cells responding to the secretions of other cells along a gradient along the expected response to shading. These results represent a critical step toward understanding basal phototrophic regulatory mechanisms of light use and demonstrate the first known intracellular directional gravity response mechanism in a prokaryote. Statement of SignificanceTo date, no directionally sensitive gravity response mechanism has been observed in any prokaryote. We demonstrate the first evidence of a directional response to external force in a cyanobacterium. This pigment distribution force-directed response interacts with the conventional response to directional light. Furthermore, the cells appear to be able to respond to the presence of other cells above them via intercellular signaling which is not simply due to shading by light.