Proteome remodeling in response to sulfur limitation in "Candidatus pelagibacter ubique"

The alphaproteobacterium "Candidatus Pelagibacter ubique" strain HTCC1062 and most other members of the SAR11 clade lack genes for assimilatory sulfate reduction, making them dependent on organosulfur compounds that occur naturally in seawater. To investigate how these cells adapt to sulfur limitation, batch cultures were grown in defined medium containing either limiting or nonlimiting amounts of dimethylsulfoniopropionate (DMSP) as the sole sulfur source. Protein and mRNA expression were measured before, during, and after the transition from exponential growth to stationary phase. Two distinct responses were observed, one as DMSP became exhausted and another as the cells acclimated to a sulfur-limited environment. The first response was characterized by increased transcription and translation of all "Ca. Pelagibacter ubique" genes downstream from the previously confirmed S-adenosyl methionine (SAM) riboswitches bhmT, mmuM, and metY. The proteins encoded by these genes were up to 33 times more abundant as DMSP became limiting. Their predicted function is to shunt all available sulfur to methionine. The secondary response, observed during sulfur-limited stationary phase, was a 6- to 10-fold increase in the transcription of the heme c shuttleencoding gene ccmC and two small genes of unknown function (SAR11-1163 and SAR11-1164). This bacterium's strategy for coping with sulfur stress appears to be intracellular redistribution to support methionine biosynthesis rather than increasing organosulfur import. Many of the genes and SAM riboswitches involved in this response are located in a hypervariable genome region (HVR). One of these HVR genes, ordL, is located downstream from a conserved motif that evidence suggests is a novel riboswitch.