Abstract

Photosynthetic bacteria can switch from planktonic lifestyle to phototrophic biofilm in mats in response to environmental changes. The mechanisms of phototrophic biofilm formation are, however, not characterized. Herein, we report a two-component system EmbRS that controls the biofilm formation in a photosynthetic member of the Burkholderiales order, the purple bacterium Rubrivivax gelatinosus. EmbRS inactivation results in cells that form conspicuous bacterial veils and fast-sinking aggregates in liquid. Biofilm analyses indicated that EmbRS represses the production of an extracellular matrix and biofilm formation. Mapping of transposon mutants that partially or completely restore the wild-type (WT) phenotype allowed the identification of two gene clusters involved in polysaccharide synthesis, one fully conserved only in Thauera sp., a floc-forming wastewater bacterium. A second two-component system BmfRS and a putative diguanylate cyclase BdcA were also identified in this screen suggesting their involvement in biofilm formation in this bacterium. The role of polysaccharides in sinking of microorganisms and organic matter, as well as the importance and the evolution of such regulatory system in phototrophic microorganisms are discussed.

Highlights

  • Photosynthetic bacteria are versatile microorganisms that can grow either as plankton or aggregates in phototrophic biofilms and colonize diverse aquatic environments

  • We found that mutation in RGS1_10407 led to a partial planktonic mode of growth and different colony morphology of the mutant compared to DEmbRS null mutant

  • Among the genes identified in the genetic screen that might be negatively regulated by EmbRS, we focused our study on the expression profile of three genes cpsG (RGS1_80151), wcbM (RGS1_10417), gltA (RGS1_10433) involved in polysaccharide and probably the extracellular matrix biosynthesis and on the twocomponent system regulator encoding gene bmfR (RGS1_30022) that seems to positively control the biofilm formation

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Summary

Introduction

Photosynthetic bacteria are versatile microorganisms that can grow either as plankton or aggregates in phototrophic biofilms and colonize diverse aquatic environments. Phototrophic biofilms, referred to as microbial phototrophic mats, usually grow on surfaces when exposed to light These mats can contain diatoms, algae, cyanobacteria, purple and green bacteria and even nonphototrophic microorganisms (De Philippis et al 2005; Roeselers et al 2008). Two genes encoding a putative two-component system were identified in the vicinity of the PGC cluster Their localization 276 nucleotides downstream bchP in the PGC suggested that this system may be involved in regulation of photosynthesis in Rubrivivax. The results provide new insight into the molecular and regulatory mechanisms by which Rubrivivax switches between planktonic and biofilm lifestyles and perhaps unravel an evolutionary step toward photosynthetic lifestyle of this bacterium

Experimental Procedures
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Conflict of Interest

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