Physiological and Metabolic Effects of Carbon Monoxide Oxidation in the Model Marine Bacterioplankton Ruegeria pomeroyi DSS-3

Abstract

Ruegeria pomeroyi expresses carbon monoxide (CO) dehydrogenase and oxidizes CO; however, CO has no effect on growth. Nuclear magnetic resonance (NMR) spectra showed that CO has no effect on cellular metabolite profiles. These data support ecosystem models proposing that, even though bacterioplankton CO oxidation is biogeochemically significant, it has an insignificant effect on bacterioplankton productivity.A erobic chemolithoautotrophic utilization of carbon monoxide (CO) by carboxidotrophic bacteria has been studied for some time (1). Carboxidotrophs use CO oxidoreductase, commonly referred to as CO dehydrogenase (CODH), to convert CO to carbon dioxide (CO 2 ). With the energy conserved from CO oxidation, carboxidotrophs assimilate the CO 2 produced from CO, typically via the Calvin Benson Bassham cycle, with the key enzyme ribulose-1,5-bisphosphate carboxylase oxygenase (RuBisCO) (2).Primarily as a result of genome sequencing, a relatively new group of CO-utilizing bacteria have been identified and termed the "carboxydovores" (2). In contrast to carboxidotrophs, carboxydovores appear unable to use CO as a source of carbon for growth. Typical elevated CO concentrations used to grow carboxidotrophs appear to inhibit growth of some carboxydovores, and many lack the metabolic capacity to assimilate CO 2 (3). Carboxydovores are probably chemolithoheterotrophs, using CO as a supplementary energy source but requiring organic carbon for growth (2, 3).Ruegeria pomeroyi DSS-3 is one of the group of carboxydovores first identified by King (3). The R. pomeroyi genome contains two different CO oxidation (cox) gene operons and lacks RuBisCO (4). Even though R. pomeroyi has been shown to oxidize CO (3-5), the effects of CO oxidation on R. pomeroyi, or any other CO-oxidizing marine Roseobacter clade strain, remain uncharacterized. The aim of this study is to establish a baseline understanding of CO physiology and metabolism in the model marine bacterioplankton R. pomeroyi.R. pomeroyi was grown in marine ammonium mineral salt medium (MAMS) modified from that described in reference 6 by adding NaCl (20 g per liter) and was supplemented with glucose. CO was added to flask headspaces (0.1%), and flasks were incubated with shaking (150 rpm) at 30°C. CO uptake was monitored using an electrochemical CO meter (detection limit, ϳ17 ppm) (Anton, United Kingdom), and growth was measured using absorbance (optical density at 600 nm [OD 600 ]) (5). Glucose concentration was determined using a hexokinase/glucose-6-phosphate dehydrogenase assay (Sigma-Aldrich, United Kingdom).R. pomeroyi growth corresponded with glucose uptake (Fig. 1). Growth rates with glucose and with glucose plus CO were 0.116 Ϯ 0.010 h Ϫ1 and 0.114 Ϯ 0.012 h Ϫ1 , showing that CO had no significant effect during exponential growth. Throughout the experiment, R. pomeroyi depleted the headspace concentration of CO, indicating that CO oxidation occurs independently of growth phase. No effect of CO was detected when cells became glucose starved during stationary phase (Fig....

Trimethylamine and trimethylamine N-oxide are supplementary energy sources for a marine heterotrophic bacterium: implications for marine carbon and nitrogen cycling

“…Both TMA and thiosulphate are 'energy rich', in the sense that they can generate between seven and eight ATP molecules from the oxidation of one TMA or thiosulphate molecule. In contrast, carbon monoxide is a relatively 'energy poor' compound, only liberating two electrons, which does not appear to result in an enhancement of growth for R. pomeroyi (Cunliffe, 2012). The utilisation of MAs as a supplementary energy source is consistent with a growing body of data that points towards the success of certain heterotrophic bacterial groups that can generate energy from a wide range of sources, including reduced organic carbon compounds (Eiler, 2006;Moran and Miller, 2007;Boden et al, 2011b;Green et al, 2011;Steindler et al, 2011;Sun et al, 2011).…”

“…Ruegeria pomeroyi DSS-3 (basonym, Silicibacter pomeroyi DSS-3) is a member of the MRC, which was isolated off the coast of Georgia through enrichment with dimethylsulphoniopropionate (González et al, 2003). The genome of R. pomeroyi was sequenced in 2004 (Moran et al, 2004), and this bacterium is now a model organism enabling a better understanding of how and why marine bacteria metabolise a wide range of substrates (Moran et al, 2004;Cunliffe, 2012;Todd et al, 2012;Lidbury et al, 2014).…”

Trimethylamine N -oxide metabolism by abundant marine heterotrophic bacteria

“…Ecologically relevant representatives of the MRC are readily cultivated and amenable to genetic manipulation, thereby making them good model organisms to investigate bacterial ecophysiology in the marine environment. Ruegeria pomeroyi DSS-3, isolated off the coast of Oregon in the United States (35), is the best characterized model marine organism in this clade (32,(36)(37)(38)(39).…”

Interfacial photochemistry of biogenic surfactants: a major source of abiotic volatile organic compounds

“…These biogenic 25 surfactants form surface microlayers (SMLs) and influence biogeochemical and climate-related processes. 13,23 Furthermore, several studies demonstrated the incorporation of such biogenic surfactants into aerosol particles by primary processes, such as bubble bursting and sea spray formation, increasing the surfactant-covered surface area in the atmosphere by orders of magnitude. 24-31 30 Although previous studies demonstrated photo-induced VOC production from surfactants on aqueous solutions, these experiments were typically conducted far from ambient conditions or for a very limited number of samples.…”