Effects of matric vs osmotic potential changes on Variovorax beijingensis transcription

ABSTRACT Soil water potential, which regulates microbe-available water, is controlled by osmotic and matric potential, which both become more negative as soils dry. While both parameters can independently alter water potential, the genetic mechanisms underlying microbial responses to both are unknown, with potentially different mechanisms available for microbes to respond to these hydrological parameters. To explore microbial responses to matric vs osmotic potential shifts independently, we evaluated the growth and transcription of Variovorax beijingensis in soils and liquid cultures of varying water potential. We found that this microbe respires in dilute minimal medium (−240 ± 104 kPa), in liquid medium containing sucrose (−1,323 ± 21 kPa), and in matrices that span a similar pressure range (−183 ± 55 and −1,393 ± 200 kPa). We show that the global gene expression patterns vary significantly across these four conditions, even when the matric potential and osmotic pressure are set to similar values. However, 68% of the differentially expressed genes (DEGs) observed when transitioning osmotic pressure in liquid medium from −240 to −1,323 kPa were also observed when transitioning matric potential from −183 to −1,393 kPa. As osmotic and matric potential approached the plant wilting point, both presented DEGs implicated in amino acid, betaine, and energy metabolism, as well as plant-growth promotion. 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. IMPORTANCE It 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 salinity (osmotic potential) and texture (matric potential), which both alter bioavailable water by contributing to total soil water potential. To investigate how the transcription 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. However, a large set of genes presented similar gene expression changes when osmotic and matric potential approached the plant wilting point, suggesting that these transcriptional changes are independent of the mechanism that alters soil water potential.