Unusual Morphological Changes of a Novel Wrinkled Bacterium Isolated from the Rice Rhizosphere Under Nutrient Stress

Abstract

Bacterial cell morphology might result from natural selection to gain a competitive advantage under environmentally stressful conditions such as nutrient limitation. In nutrient-limited conditions, a higher surface-to-volume ratio is crucial for cell survival because it allows for a more efficient exchange of nutrients and waste products. A bacterial strain YC6860T isolated from the rhizosphere of rice (Oryza sativa L.) showed pleomorphic behavior with smooth cell morphology and wrinkled surface rods depending upon nutritional conditions. Based on scanning and transmission electron microscopy studies, we hypothesized that the surface-to-volume ratio of cells would increase with decreasing nutrient concentrations and tested this quantitatively. The transition from smooth to wrinkled cell surface morphology could be one of the adaptation strategies by which YC6860T maximizes its ability to access available nutrients. To characterize the properties of the wrinkled strain, we performed taxonomic and phylogenetic analyses. 16S rRNA gene sequencing results showed that the strain represented a novel, deep-rooting lineage within the order Rhizobiales with the highest similarity of 94.2% to Pseudorhodoplanes sinuspersici RIPI 110T. Whole-genome sequencing was also performed to characterize its genetic features. The low phylogenetic and genetic similarity is probably related to the wrinkled morphology of the strain. Therefore, we propose that the strain YC6860T might belong to a new genus and species, named Rugositalea oryzae. In addition, taxonomic analysis showed that YC6860T is Gram-negative, aerobic, and rod-shaped with regular surface wrinkles under nutrient-limiting conditions, resembling a delicate twist of fusilli, with groove depths of 48.8 +/- 3.7 nm and spacing of 122.5 +/- 16.9 nm. This unique cell structure with regular rugosity could be the first finding that has not been reported in the existing bacterial morphology.