How sulphate-reducing microorganisms cope with stress: lessons from systems biology

Sulphate-reducing microorganisms (SRMs) are a physiologically and phylogenetically diverse group of anaerobic bacterial and archaeal species that are important both ecologically and industrially. The application of systems biology tools has provided insights into the stress responses in SRMs at the cell, population, community and ecosystem levels.Analyses using comparative and functional genomics support hydrogen cycling as a mode of energy metabolism that is characteristic of SRMs, and highlight the central role of this process in stress responses in Desulfovibrio vulgaris Hildenborough, the best known model SRM.D. vulgaris activates distinct pathways in response to specific stresses. This is consistent with comparative genomic analyses that reveal this species has an unusually large number of diverse response regulators for signal transduction.Despite the divergence in stress responses in D. vulgaris, the oxidative stress response seems to have a prevalent role in coping with many different stresses, as components of the defence pathways against reactive oxygen species are highly expressed even under non-oxidative stress conditions. This anticipatory expression may confer an adaptive advantage, as stress caused by reactive oxygen species is the most critical stress to anaerobes such as SRMs.The ability of D. vulgaris to grow syntrophically with methanogens allows its distribution and evolution in environments that are depleted of sulphate, a condition that is an insurmountable stress for other SRMs. Integrated 'omics' analyses further indicate that D. vulgaris has genes (such as those involved in hydrogen cycling) that are dedicated to survival by syntrophy, and that the bacteria can evolve enhanced stability and productivity as a part of a community.High-throughput sequencing and metagenomic technologies (such as GeoChip and PhyloChip) have been used to demonstrate that SRMs are widely distributed and well adapted to diverse environments. Metagenomic studies show that the distribution and activity of SRMs are constrained by the environmental boundaries defined by the cell's physiological limit to launch an effective stress response. Thus, a system-level understanding of stress responses provides critical knowledge for designing strategies for the application or elimination of SRMs in distinctive environments.Next-generation genomics and other new technologies hold great promise for us to gain a more comprehensive understanding of SRMs (for example, by linking genotypes to phenotypes through experimental evolution, by high-resolution population genomics studies of SRMs, and by modelling SRM activity in a variety of environments). Analysis of SRM populations in communities with different levels of complexity is essential for predicting the ecological and evolutionary responses of microbial communities to environmental change. Novel mathematical frameworks and computational tools will greatly help us address these challenges.