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

Abstract

Although Medicago sativa forms highly effective symbioses with the comparatively acid-sensitive genus Ensifer, its introduction into acid soils appears to have selected for symbiotic interactions with acid-tolerant R. favelukesii strains. Rhizobium favelukesii has the unusual ability of being able to nodulate and fix nitrogen, albeit sub-optimally, not only with M. sativa but also with the promiscuous host Phaseolus vulgaris. Here we describe the genome of R. favelukesii OR191 and genomic features important for the symbiotic interaction with both of these hosts. The OR191 draft genome contained acid adaptation loci, including the highly acid-inducible lpiA/acvB operon and olsC, required for production of lysine- and ornithine-containing membrane lipids, respectively. The olsC gene was also present in other acid-tolerant Rhizobium strains but absent from the more acid-sensitive Ensifer microsymbionts. The OR191 symbiotic genes were in general more closely related to those found in Medicago microsymbionts. OR191 contained the nodA, nodEF, nodHPQ, and nodL genes for synthesis of polyunsaturated, sulfated and acetylated Nod factors that are important for symbiosis with Medicago, but contained a truncated nodG, which may decrease nodulation efficiency with M. sativa. OR191 contained an E. meliloti type BacA, which has been shown to specifically protect Ensifer microsymbionts from Medicago nodule-specific cysteine-rich peptides. The nitrogen fixation genes nifQWZS were present in OR191 and P. vulgaris microsymbionts but absent from E. meliloti-Medicago microsymbionts. The ability of OR191 to nodulate and fix nitrogen symbiotically with P. vulgaris indicates that this host has less stringent requirements for nodulation than M. sativa but may need rhizobial strains that possess nifQWZS for N2-fixation to occur. OR191 possessed the exo genes required for the biosynthesis of succinoglycan, which is required for the Ensifer-Medicago symbiosis. However, 1H-NMR spectra revealed that, in the conditions tested, OR191 exopolysaccharide did not contain a succinyl substituent but instead contained a 3-hydroxybutyrate moiety, which may affect its symbiotic performance with Medicago hosts. These findings provide a foundation for the genetic basis of nodulation requirements and symbiotic effectiveness with different hosts.

Editorial: Maximizing nitrogen fixation in legumes as a tool for sustainable agriculture intensification, volume II

“…Failures in Medicago sativa (alfalfa) production have been attributed to low soil pH and the presence of inefficient parasitic rhizobia strains (Eardly et al, 1992;Del Papa et al, 1999;Eardly et al, 2022). This group of rhizobia generically, known as the Oregon-like strain, are competitive for nodulation of alfalfa in acid soils but exhibits low symbiotic efficiency.…”

Competitiveness and symbiotic efficiency in alfalfa of Rhizobium favelukesii ORY1 strain in which homologous genes of peptidases HrrP and SapA that negatively affect symbiosis were identified

“…Failures in alfalfa (Medicago sativa) production have been attributed to soil acid pH, aluminium toxicity (Bouton, 2012;Jaiswal et al, 2018;Shi et al, 2022) and the presence of parasite rhizobia strains that inefficiently nodulate alfalfa (Torres Tejerizo et al, 2011;Eardly et al, 2022). These parasite strains, known as Oregon-like, have tolerance to acidic conditions, a host broad range (Eardly et al, 1992;Del Papa et al, 1999), and its presence has also been confirmed in USA and Canada (Bromfield et al, 2010).…”

“…Likewise, Oregon strain LPU83 has been isolated from alfalfa root nodules in Argentina and was assigned to the novel species Rhizobium favelukesii (Torres Tejerizo et al, 2016). Oregon strains are competitive for the nodulation of alfalfa in acid soils and have low symbiotic efficiency in this legume (Del Papa et al, 2003;Torres Tejerizo et al, 2011;Eardly et al, 2022). For this reason, it is important to know the presence of this type of strain in places where alfalfa is grown, as well as their competitiveness respect to the inoculant used or native efficient strains present in the soil.…”