Effects of matric versus osmotic potential changes on Variovorax beijingensis transcription

Abstract

Soil microbes must continuously adapt to changes in water availability, which dynamically fluctuates with weather and irrigation, and these adaptations are closely linked to soil CO2 emissions. Soil water potential, which regulates microbe-available water, is controlled by both osmotic and matric potential, which both increase as soils dry. While both parameters can independently increase water potential, the genetic mechanisms underlying microbial responses to both are unknown, with potentially different mechanisms available for soil microbes to respond to these hydrologic parameters. To explore microbial responses to matric versus osmotic potential shifts, we evaluated the growth and transcription of Variovorax beijingensis in soils and liquid cultures of varying water potential. We find this microbe respires in dilute minimal medium (-240 {+/-}104 kPa), in liquid medium supplemented with sucrose (-1323 {+/-}20.8 kPa), and in a pair of matrices that span a similar range of pressures (-183 {+/-}55 and -1393 kPa {+/-}200 kPa). We show that the global gene expression patterns vary significantly across all four conditions, even when the matric potential and osmotic pressure are set to similar values. However, the direction of gene expression changes correlated for 68% of the transcripts arising from an increase in osmotic pressure within liquid medium and an increase in matric potential within the different soils. While a large overlap was observed in the Variovorax transcriptional response to shifts in both osmotic and matric potential, the responses were not identical, with matric potential shifts leading to 2.55-fold more genes exhibiting differential expression. IMPORTANCEIt remains hard to establish how changes in soil water properties affect microbial behaviors that regulate soil health, and the energy with which soil water is held is likely a holistic control on at least some of those microbial behaviors. This energy is controlled by parameters associated with soil saltiness (osmotic potential) and texture (matric potential), which both alter bioavailable water by contributing to total soil water potential. To investigate how the global transcriptional profile of a soil microbe changes when the microbe-available water is altered either by changing soil texture or by changing osmolyte concentrations, we varied osmotic and matric potential individually and performed RNA sequencing. We observe differences in the transcriptome across all conditions analyzed. A larger number of genes are differentially expressed as matric potential increases; however, many of the transcripts differentially expressed as osmotic pressure increases covary with those observed as the matrix potential increases.