The variations of native plasmids greatly affect the cell surface hydrophobicity of sphingomonads

Abstract

ABSTRACT The organic pollutant-degrading microorganisms with high cell surface hydrophobicity (CSH) are generally favorable due to the positive role of high CSH in pollutant capture and cell colonization. Sphingomonads, an important bacterial group with metabolic versatility, have significant potential for biodegradation and bioremediation of organic pollutants and generally harbor higher CSH than typical Gram-negative bacteria. However, the molecular mechanisms underlying their high CSH are still unclear. In this study, Sphingobium xenophagum C1, the most hydrophobic sphingomonad ever known, and its hydrophilic variant C2 were used to identify the genome variations responsible for the CSH difference by comparative genome and transcriptome analysis, as well as gene knockout verification. Our results indicated that the high CSH of strain C1 was largely attributed to the low copy number of the native plasmid p3, which mainly affected the transcriptional levels of outer membrane protein genes through direct and indirect means. In addition, loss of the genes on the native plasmid p5 involved in polysaccharide synthesis and secretion could increase CSH and cell surface friction. The bioinformatics analysis further revealed that some sphingomonad genomes also contained the long homologous fragments and/or key genes of p3 and p5. This study demonstrated the important role of native plasmids in regulating the CSH of sphingomonads, suggesting a novel CSH regulation strategy and evolution process. IMPORTANCE Microbial cell surface hydrophobicity (CSH) reflects nonspecific adhesion ability and affects various physiological processes, such as biofilm formation and pollutant biodegradation. Understanding the regulation mechanisms of CSH will contribute to illuminating microbial adaptation strategies and provide guidance for controlling CSH artificially to benefit humans. Sphingomonads, a common bacterial group with great xenobiotic-degrading ability, generally show higher CSH than typical Gram-negative bacteria, which plays a positive role in organic pollutant capture and cell colonization. This study verified that the variations of two native plasmids involved in synthesizing outer membrane proteins and polysaccharides greatly affected the CSH of sphingomonads. It is feasible to control their CSH by changing the plasmid copy number and sequences. Additionally, considering that plasmids are likely to evolve faster than chromosomes, the CSH of sphingomonads may evolve quickly to respond to environmental changes. Our results provide valuable insights into the CSH regulation and evolution of sphingomonads.