Global transcriptome analysis of Rhizobium favelukesii LPU83 in response to acid stress

Abstract

Acidic environments naturally occur worldwide and inappropriate agricultural management may also cause acidification of soils. Low soil pH values are an important barrier in the plant-rhizobia interaction. Acidic conditions disturb the establishment of the efficient rhizobia usually used as biofertilizer. This negative effect on the rhizobia-legume symbiosis is mainly due to the low acid-tolerance of the bacteria. Here, we describe the identification of relevant factors in the acid tolerance of Rhizobium favelukesii using transcriptome sequencing. A total of 1,924 genes were differentially expressed under acidic conditions, with ca. 60% underexpressed. R. favelukesii acid response mainly includes changes in the energy metabolism and protein turnover, as well as a combination of mechanisms that may contribute to this phenotype, including GABA and histidine metabolism, cell envelope modifications and reverse proton efflux. We confirmed the acid-sensitive phenotype of a mutant in the braD gene, which showed higher expression under acid stress. Remarkably, 60% of the CDS encoded in the symbiotic plasmid were underexpressed and we evidenced that a strain cured for this plasmid featured an improved performance under acidic conditions. Hence, this work provides relevant information in the characterization of genes associated with tolerance or adaptation to acidic stress of R. favelukesii.

The Genome of the Acid Soil-Adapted Strain Rhizobium favelukesii OR191 Encodes Determinants for Effective Symbiotic Interaction With Both an Inverted Repeat Lacking Clade and a Phaseoloid Legume Host

“…OR191 produced 0.1 mg ml –1 and 0.5 mg ml –1 EPS at pH 7.0 and 5.8, respectively, representing a fivefold increase in EPS production in acidic conditions. This differs from previous reports of EPS production in R. favelukesii LPU83 T , which found no significant difference in the amount of EPS obtained from cells grown under neutral and acidic conditions ( Nilsson et al, 2020 ). In contrast, the E. medicae strain WSM419 produced 0.05 mg ml –1 and 4.65 mg ml –1 EPS at pH 7.0 and 5.8, respectively, representing a 93-fold increase in EPS production in acidic conditions.…”

“…The olsC gene, which has been identified as being important for the production of hydroxylated ornithine lipid species that increase stress tolerance in CIAT899 T ( Rojas-Jiménez et al, 2005 ; Vences-Guzmán et al, 2011 ), was present in both the highly acid tolerant strain R. tropici CIAT899 T and in R. favelukesii strains but was absent from E. medicae WSM419 and E. meliloti 1021. This accords with proteomic and transcriptomic studies of R. favelukesii LPU83 T that revealed changes in proteins and genes associated with lipid metabolism involving the cell envelope in response to acid stress, however, these studies also suggested that some acid-responsive regulatory systems differ in LPU83 T compared with Ensifer strains ( Nilsson et al, 2019 , 2020 ).…”

“…Additionally, R. favelukesii contains the highly acid-induced lpiA and acvB genes, but lacks the associated regulatory system described for this operon in Ensifer ( Reeve et al, 2006 ), indicating that an unidentified pH responsive regulatory system is present in R. favelukesii . Several mechanisms for acid tolerance in R. favelukesii LPU83 T have been suggested by Nilsson et al (2019 , 2020) .…”

Rhizobial Exopolysaccharides and Type VI Secretion Systems: A Promising Way to Improve Nitrogen Acquisition by Legumes

“…Secreted EPS are increased under abiotic stress (Hirsch, 1996;Sorroche et al, 2018;Primo et al, 2020). However, at acid pH R. tropici CIAT899 showed a lower production of biopolymers (Avelar Ferreira et al, 2012), whereas EPS production was not affected in R. favelukesii LPU83 (Nilsson et al, 2021).…”

Algalization of Acid Soils with Desmodesmus sp. MAS1 and Heterochlorella sp. MAS3 Enriches Bacteria of Ecological Importance

“…In fact, only a few studies have indicated the potential of microalgae as biofertilizers in soil microcosm experiments. ,− Only a few studies have discussed the microbial community structure and function in soils associated with various acidification units . Very recently, Nilsson et al reported that acid conditions are an important barrier in plant–rhizobia interaction, and it disturbs the establishment of efficient rhizobia used as biofertilizers. We used two acid-tolerant microalgal strains, Desmodesmus sp.…”