Assessment of the stoichiometry and efficiency of CO2 fixation coupled to reduced sulfur oxidation

Abstract

Chemolithoautotrophic sulfur oxidizing bacteria (SOB) couple the oxidation of reduced sulfur compounds to the production of biomass. Their role in the cycling of carbon, sulfur, oxygen, and nitrogen is, however, difficult to quantify due to the complexity of sulfur oxidation pathways. We describe a generic theoretical framework for linking the stoichiometry and energy conservation efficiency of autotrophic sulfur oxidation while accounting for the partitioning of the reduced sulfur pool between the energy generating and energy conserving steps as well as between the main possible products (sulfate vs. zero-valent sulfur). Using this framework, we show that the energy conservation efficiency varies widely among SOB with no apparent relationship to their phylogeny. Aerobic SOB equipped with reverse dissimilatory sulfite reductase tend to have higher efficiency than those relying on the complete Sox pathway, whereas for anaerobic SOB the presence of membrane-bound, as opposed to periplasmic, nitrate reductase systems appears to be linked to higher efficiency. We employ the framework to also show how limited rate measurements can be used to estimate the primary productivity of SOB without the knowledge of the sulfate-to-zero-valent-sulfur production ratio. Finally, we discuss how the framework can help researchers gain new insights into the activity of SOB and their niches.

Productivity, metabolism and physiology of free-living chemoautotrophic Epsilonproteobacteria

“…Although CGE has not been measured for SUP05, related autotrophic Gammaproteobacteria do not differ considerably from our values (Klatt and Polerecky, 2015), indicating this will likely be a small bias. Similarly, while differing fluid chemistry may also affect microbial productivity, we only observed a 2-fold difference in CGE between diverse amendments (Fig 3-3).…”

“…For each model iteration, we simulated growth yields in silico using flux balance analysis (FBA) which accurately reproduces both overall efficiency as well as the ratio between growth yields on different energy sources. Overall efficiency is the proportion of electrons derived from substrate oxidation used to fix CO 2 , equivalent to (1-y) in Klatt and Polerecky (2015). It is possible to have a model where one, but not both of these parameters is consistent with experimental data.…”

“…However, proton translocation is not thought to be catalyzed by denitrification enzymes (Chen and Strous, 2013). Additionally, if denitrification enzymes were capable of energy conservation, the overall growth yield of S. denitrificans would be much higher in silico than in vivo (Timmer-Ten Hoor, 1981;Klatt and Polerecky, 2015). For these reasons, we rejected the possibility that denitrification enzymes could conserve energy.…”

“…For example, with nitrate or coupled nitrate/hydrogen amendments at 24 ∘ C, CGE was close to pure cultures of mesophilic sulfur-oxidizing Epsilonproteobacteria (Fig 3-3; Klatt and Polerecky (2015)). However, with oxygen additions at 24 ∘ C and nitrate/hydrogen additions at 50 ∘ C, CGE decreased by approximately 50%.…”

“…CGE is the estimated fraction of electron equivalents derived from electron donors that are used to reduce CO 2 into biomass, equivalent to the parameter 1-y from (Klatt and Polerecky, 2015). Total carbon fixed from bulk isotope measurements was determined as described above.…”