Abstract

Rhodobacter sphaeroides strain 2.4.1 is a widely studied bacterium that has recently been shown to cleave the abundant marine anti-stress molecule dimethylsulfoniopropionate (DMSP) into acrylate plus gaseous dimethyl sulfide. It does so by using a lyase encoded by dddL, the promoter-distal gene of a three-gene operon, acuR-acuI-dddL. Transcription of the operon was enhanced when cells were pre-grown with the substrate DMSP, but this induction is indirect, and requires the conversion of DMSP to the product acrylate, the bona fide co-inducer. This regulation is mediated by the product of the promoter-proximal gene acuR, a transcriptional regulator in the TetR family. AcuR represses the operon in the absence of acrylate, but this is relieved by the presence of the co-inducer. Another unusual regulatory feature is that the acuR-acuI-dddL mRNA transcript is leaderless, such that acuR lacks a Shine-Dalgarno ribosomal binding site and 5′-UTR, and is translated at a lower level compared to the downstream genes. This regulatory unit may be quite widespread in bacteria, since several other taxonomically diverse lineages have adjacent acuR-like and acuI-like genes; these operons also have no 5′ leader sequences or ribosomal binding sites and their predicted cis-acting regulatory sequences resemble those of R. sphaeroides acuR-acuI-dddL.

Highlights

  • Dimethylsulfoniopropionate (DMSP) is an abundant (,109 tons produced worldwide, each year) compatible solute that is made by many diverse marine phytoplankton, some macroalgal seaweeds and a few angiosperms [1]

  • Some DMSP-producing algae themselves can catabolise DMSP [3,4] and on senescence or viral lysis, the DMSP that is released from these algae can be catabolised by various marine bacteria and by some fungi [5,6]

  • 30 million tons (,10% of the total) of this dimethyl sulfide (DMS) escapes each year from the surface layers of the sea, representing the principal form by which biogenic sulfur is transferred to the atmosphere from the oceans [7]

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Summary

Introduction

Dimethylsulfoniopropionate (DMSP) is an abundant (,109 tons produced worldwide, each year) compatible solute that is made by many diverse marine phytoplankton, some macroalgal seaweeds and a few angiosperms [1]. Some DMSP-producing algae themselves can catabolise DMSP [3,4] and on senescence or viral lysis, the DMSP that is released from these algae can be catabolised by various marine bacteria and by some fungi [5,6]. Some of these catabolic pathways generate dimethyl sulfide (DMS), an important volatile in its own right. DMS oxidation products (e.g. sulfate) act as cloud condensation nuclei, with effects on albedo, reflecting radiation back to space [8]. DMS is a potent chemo-attractant for potential food supplies of marine animals, such as crustaceans (Copepods), seabirds (penguins, shearwaters, petrels) and mammals (harbour seals) [9,10,11,12]

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