Environmental potassium regulates bacterial flotation, antibiotic production and turgor pressure in Serratia through the TrkH transporter

Abstract

Summary Serratia sp. strain ATCC 39006 (S39006) can float in aqueous environments due to natural production of gas vesicles (GVs). Expression of genes for GV morphogenesis is stimulated in low oxygen conditions, thereby enabling migration to the air–liquid interface. Quorum sensing (via SmaI and SmaR) and transcriptional and post‐transcriptional regulators, including RbsR and RsmA, respectively, connect the control of cell buoyancy, motility and secondary metabolism. Here, we define a new pleiotropic regulator found in screens of GV mutants. A mutation in the gene trkH , encoding a potassium transporter, caused upregulation of GV formation, flotation, and the prodigiosin antibiotic, and downregulation of flagellar motility. Pressure nephelometry revealed that the mutation in trkH affected cell turgor pressure. Our results show that osmotic change is an important physiological parameter modulating cell buoyancy and antimicrobial production in S39006, in response to environmental potassium levels.

Experimental Evolution of Anticipatory Regulation in Escherichia coli

“…A mutation in trkH is often associated with aminoglycoside resistance in bacteria ( Lazar et al, 2013 ; Apjok et al, 2019 ). It also plays important roles in osmotic response, modulation of membrane potential, pH maintenance, and overall fitness in a variety of bacterial species ( Castaneda-Garcia et al, 2011 ; Ochrombel et al, 2011 ; Quintero-Yanes et al, 2019 ).…”

The FloR master regulator controls flotation, virulence and antibiotic production in Serratia sp. ATCC 39006

“…In addition, due to light scattering, colonies of some bacteria containing gas vesicles can appear white opaque (Walsby, 1994). Because S39006 colonies are red, due to the production of prodigiosin, we used the prodigiosin mutant NWA19 (pigC) that exhibited the white opaque phenotype to facilitate facile mutant screening (Ramsay et al, 2011;Lee et al, 2017;Quintero-Yanes et al, 2019). Random transposon mutagenesis was performed on NWA19 and over 18,000 transposon-containing colonies were screened for a translucent phenotype (those likely to be defective in gas vesicle formation).…”

“…Images were taken with a QICAM monochrome camera adapted to QCapture Pro-6 software. Transmission electron microscopy (TEM) images were obtained from cells in static liquid cultures prepared as reported previously (Quintero-Yanes et al, 2019). Cell images were obtained using a FEI Tecnai G2 TEM in the Cambridge Advance Imaging Centre, University of Cambridge.…”

“…Gas vesicle synthesis in some bacteria is responsive to different signals, enabling migration to, and persistence at, physiologically suitable depths of the water column (Walsby, 1994). Consequently, the production of these structures in some bacteria may be sensitive to light, nitrogen, oxygen, phosphorus and potassium availability (Walsby, 1976;Allison and Walsby, 1981;Brookes and Ganf, 2001;Ramsay et al, 2011;Quintero-Yanes et al, 2019).…”

“…Oxygen limitation stimulates expression of the gvpA1-gvpY operon, facilitating gas vesicle assembly and bacterial migration to, and persistence at, the air-liquid interface, thereby enabling access to oxygen (Ramsay et al, 2011). In contrast, potassium uptake via the low-affinity transporter, TrkH, downregulates the gvpA1-gvpY operon (Quintero-Yanes et al, 2019). TrkH controls cell buoyancy, turgor pressure, motility and prodigiosin production in S39006.…”