Dinner with friends: The role of DMSP in quorum sensing

Since Lawrence R. Pomeroy (1974) first noted the importance of microbes in marine food webs, much research has been dedicated to understanding the role that Bacteria serve in oceanic carbon flow. It has long been understood that Bacteria are integral in decomposing organic compounds from phytoplankton blooms. Of these compounds, one of the most abundant is a phytoplankton-derived organosulfur metabolite known as DMSP (dimethylsulfoniopropionate). While the metabolism of DMSP by heterotrophic bacterioplankton is well studied, the role of organic metabolites in inter-species interaction and communication is poorly understood. A new paper provides an exciting insight as to how DMSP may influence bacterial communication.

Johnson et al., 2016 set out to investigate the metabolic response to DMSP in a marine bacterium. The authors cultured Ruegeria pomeroyi (yes, named in honour of the eponymous marine microbiologist) in the presence of either DMSP or propionate (an organic control) and analysed how the differential treatments affected metabolomic fingerprints as determined by FT-ICR mass spectrometry. While no difference in growth rates was observed between the treatments, certain metabolites important in biogeochemical cycling differed significantly. For example, extracellular concentrations of the vitamin riboflavin (essential for the growth of certain microbial species) were much higher under the DMSP treatment. Most strikingly, the authors identified that the synthesis of an autoinducer involved in quorum sensing (N-(3-oxotetradecanoyl)-L-homoserine lactone) known as an AHL increased under the presence of DMSP by up to fifteen times. This provides exciting evidence that DMSP may play a role in interbacterial communication.

The genome of R. pomeroyi, a copiotrophic species in the Roseobacter clade, was sequenced in 2004 by Moran et al. and revealed a suite of differential metabolic pathways indicative of a ‘feast and famine’ lifestyle to exploit transient high-nutrient particles. DMSP is much more heavily concentrated within these particles than in dilute pelagic waters, and so the authors hypothesise that high cell densities associated with these particles exploit quorum sensing to control the cooperative release of digestive exoenzymes and may too benefit from differential metabolite synthesis from ‘cross-feeding’. The latter is supportive of a recent hypothesis in marine microbiology known as ‘The Black Queen Hypothesis’, as first proposed by Morris et al. in 2012. It states that genome reduction can be selected for in free-living bacterioplankton if incomplete metabolic pathways can be compensated for by concomitant cells. The release of high-value metabolites, such as riboflavin, at DMSP-rich, high nutrient particles by R. pomeroyi may allow an adaptive, cooperative exchange of such compounds among a diverse consortium.

While this study hints at an intriguing shift in how we understand microbial carbon flow, I would advise caution in placing too much confidence in the model suggested. The paper has only confirmed the presence of increased AHL synthesis in metabolomic profiles when this single species is grown in the presence of DMSP; the rest is conjecture. I would be interested to see how these ideas develop when tested against in vivo quorum sensing assays, perhaps using furanones or synthetic autoinducers to inhibit communication among multi-species consortia. While I believe mesocosm studies and comprehensive testing are needed to support these claims, this paper nevertheless provides an exciting insight into the complexities of microbial oceanic carbon flow. It will be fascinating to see how ‘The Black Queen Hypothesis’ in particular pans out as more data is gathered. 

Reviewed Paper: Johnson, W. M., Soule, M. C. K., & Kujawinski, E. B. (2016). Evidence for quorum sensing and differential metabolite production by a marine bacterium in response to DMSP. The ISME journal. http://www.nature.com/ismej/journal/v10/n9/full/ismej20166a.html 

R. pomeroyi Genome: Moran, M. A., Buchan, A., González, J. M., Heidelberg, J. F., Whitman, W. B., Kiene, R. P., ... & Brinkac, L. (2004). Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature, 432(7019), 910-913. http://www.nature.com/nature/journal/v432/n7019/abs/nature03170.html 

The Black Queen Hypothesis: Morris, J. J., Lenski, R. E., & Zinser, E. R. (2012). The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. MBio,3(2), e00036-12. http://mbio.asm.org/content/3/2/e00036-12.short