Bradyrhizobium diazoefficiens USDA 110 displays plasticity in the attachment phenotype when grown in different soybean root exudate compounds

Armaan Kaur Sandhu; McKenzie Rae Brown; Senthil Subramanian; Volker S Brözel

doi:10.3389/fmicb.2023.1190396

Bradyrhizobium diazoefficiens USDA 110 displays plasticity in the attachment phenotype when grown in different soybean root exudate compounds

Front Microbiol. 2023 May 18:14:1190396. doi: 10.3389/fmicb.2023.1190396. eCollection 2023.

Authors

Armaan Kaur Sandhu¹, McKenzie Rae Brown¹, Senthil Subramanian^{1

2}, Volker S Brözel^{1

3}

Affiliations

¹ Departments of Biology and Microbiology, South Dakota State University, Brookings, SD, United States.
² Department of Agronomy, Horticulture and Plant Science, South Dakota State University, Brookings, SD, United States.
³ Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria, South Africa.

Abstract

Introduction: Bradyrhizobium diazoefficiens, a symbiotic nitrogen fixer for soybean, forms nodules after developing a symbiotic association with the root. For this association, bacteria need to move toward and attach to the root. These steps are mediated by the surface and phenotypic cell properties of bacteria and secreted root exudate compounds. Immense work has been carried out on nodule formation and nitrogen fixation, but little is known about the phenotype of these microorganisms under the influence of different root exudate chemical compounds (RECCs) or how this phenotype impacts the root attachment ability.

Methods: To address this knowledge gap, we studied the impact of 12 different RECCs, one commonly used carbon source, and soil-extracted solubilized organic matter (SESOM) on attachment and attachment-related properties of B. diazoefficiens USDA110. We measured motility-related properties (swimming, swarming, chemotaxis, and flagellar expression), attachment-related properties (surface hydrophobicity, biofilm formation, and attachment to cellulose and soybean roots), and surface polysaccharide properties (colony morphology, exopolysaccharide quantification, lectin binding profile, and lipopolysaccharide profiling).

Results and discussion: We found that USDA 110 displays a high degree of surface phenotypic plasticity when grown on the various individual RECCs. Some of the RECCs played specific roles in modulating the motility and root attachment processes. Serine increased cell surface hydrophobicity and root and cellulose attachment, with no EPS formed. Gluconate and lactate increased EPS production and biofilm formation, while decreasing hydrophobicity and root attachment, and raffinose and gentisate promoted motility and chemotaxis. The results also indicated that the biofilm formation trait on hydrophilic surfaces (polystyrene) cannot be related to the attachment ability of Bradyrhizobium to the soybean root. Among the tested phenotypic properties, bacterial cell surface hydrophobicity was the one with a significant impact on root attachment ability. We conclude that USDA 110 displays surface plasticity properties and attachment phenotype determined by individual RECCs from the soybean. Conclusions made based on its behavior in standard carbon sources, such as arabinose or mannitol, do not hold for its behavior in soil.

Keywords: Bradyrhizobium diazoefficiens; attachment; biofilm; phenotype; phenotypic plasticity; root; root exudate; soybean.

Grants and funding

AS was supported by a National Science Foundation Assistantship. This material is based upon work supported by the National Science Foundation/EPSCoR RII Track-1: Building on The 2020 Vision: Expanding Research, Education, and Innovation in South Dakota, Award OIA-1849206 and by the South Dakota Board of Regents. We acknowledge the use of the SDSU-FGCF supported in part by NSF/EPSCoR Grant No. 0091948 and by the State of South Dakota.