Genome and catabolic subproteomes of the marine, nutritionally versatile, sulfate-reducing bacterium Desulfococcus multivorans DSM 2059.

Marvin Dörries,Michael Kube,Lars Wöhlbrand,Ralf Rabus,Richard Reinhardt

doi:10.1186/s12864-016-3236-7

Abstract

BackgroundSulfate-reducing bacteria (SRB) are key players of the carbon- and sulfur-cycles in the sediments of the world’s oceans. Habitat relevant SRBs are often members of the Desulfosarcina-Desulfococcus clade belonging to the deltaproteobacterial family of Desulfobacteraceae. Despite this environmental recognition, their molecular (genome-based) physiology and their potential to contribute to organic carbon mineralization as well as to adapt to changing environmental conditions have been scarcely investigated. A metabolically versatile representative of this family is Desulfococcus multivorans that is able to completely oxidize (to CO2) a variety of organic acids, including fatty acids up to C14, as well as aromatic compounds.ResultsIn this study the complete 4.46 Mbp and manually annotated genome of metabolically versatile Desulfococcus multivorans DSM 2059 is presented with particular emphasis on a proteomics-driven metabolic reconstruction. Proteomic profiling covered 17 substrate adaptation conditions (6 aromatic and 11 aliphatic compounds) and comprised 2D DIGE, shotgun proteomics and analysis of the membrane protein-enriched fractions. This comprehensive proteogenomic dataset allowed for reconstructing a metabolic network of degradation pathways and energy metabolism that consists of 170 proteins (154 detected; ~91 % coverage). Peripheral degradation routes feed via central benzoyl-CoA, (modified) β-oxidation or methylmalonyl-CoA pathways into the Wood-Ljungdahl pathway for complete oxidation of acetyl-CoA to CO2. Dissimilatory sulfate reduction is fueled by a complex electron transfer network composed of cytoplasmic components (e.g., electron transfer flavoproteins) and diverse membrane redox complexes (Dsr, Qmo, Hmc, Tmc, Qrc, Nuo and Rnf). Overall, a high degree of substrate-specific formation of catabolic enzymes was observed, while most complexes involved in electron transfer appeared to be constitutively formed.ConclusionsA highly dynamic genome structure in combination with substrate-specifically formed catabolic subproteomes and a constitutive subproteome for energy metabolism and electron transfer appears to be a common trait of Desulfobacteraceae members.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3236-7) contains supplementary material, which is available to authorized users.

Highlights

Sulfate-reducing bacteria (SRB) are key players of the carbon- and sulfur-cycles in the sediments of the world’s oceans
The present study extends our current knowledge on Desulfobacteraceae by reporting the first complete genome of a Desulfosarcina-Desulfococcus clade member, the nutritionally versatile Desulfococcus multivorans (Table 1)
Concept of metabolic reconstruction by proteogenomics The present study focused on the metabolic reconstruction of D. multivorans since it was originally described as a nutritionally versatile, completely oxidizing SRB [31]

Summary

Introduction

Sulfate-reducing bacteria (SRB) are key players of the carbon- and sulfur-cycles in the sediments of the world’s oceans. Members of the likewise deltaproteobacterial family Desulfobacteraceae are capable of complete oxidation and are nutritionally versatile [4] Their substrate spectra range from readily degradable simple fermentation endproducts via long-chain fatty acids to more challenging molecules such as aromatic compounds and hydrocarbons [4]. Members of the family Desulfobacteraceae have long been known to dominate bacterial populations in marine shelf sediments (e.g., [7,8,9,10]) and were recently detected in a sedimental sulfate methane transition zone [11] as well as an oxygen minimum zone off the coast of Namibia [12] To their ecophysiological relevance for the biogeochemistry of marine environments, interest in SRB arises from their long evolutionary history and their energy metabolism operating at the thermodynamic limit [13]. Studies on the differential proteomic level have been performed with D. autotrophicum HRM2 [17, 18] and D. toluolica Tol2 [15]

Methods

Results

Conclusion