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Another Chemolithotrophic Metabolism Missing in Nature: Sulfur Comproportionation

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Another Chemolithotrophic Metabolism Missing in Nature: Sulfur Comproportionation Environmental Microbiology (2020) 00(00), 00–00 doi:10.1111/1462-2920.14982 Correspondence Another chemolithotrophic metabolism missing in nature: sulfur comproportionation Jan P. Amend ,1,2* Heidi S. Aronson ,1 Introduction Jennifer Macalady 3 and Douglas E. LaRowe 2 Reaction energetics have been used, at least in part, 1Department of Biological Sciences, University of to posit the existence of several previously undetected Southern California, Los Angeles, CA, 90089. microbial metabolisms. The core argument reads that 2Department of Earth Sciences, University of Southern sufficiently exergonic redox reactions can drive cellu- California, Los Angeles, CA, 90089. lar functions of hypothetical microorganisms. In a clas- 3 Department of Geosciences, Pennsylvania State sic example, Broda calculated standard Gibbs University, University Park, PA, 16802. energies to propose that anaerobic ammonia oxidation with nitrate or nitrite (later termed anammox) could Summary fuel certain chemolithotrophs ‘missinginnature’ (Broda, 1977). It took nearly 20 years until microbial Chemotrophic microorganisms gain energy for cellular catalysis of this process was confirmed in a laboratory – functions by catalyzing oxidation reduction (redox) wastewater sludge reactor (Vandegraaf et al., 1995), reactions that are out of equilibrium. Calculations of the and several more years until it was documented in ΔG Gibbs energy ( r) can identify whether a reaction is natural environments with nitrite as the oxidant thermodynamically favourable and quantify the accom- (Kuypers et al., 2003). It is now recognized that the panying energy yield at the temperature, pressure and activity of anammox bacteria may account for as much chemical composition in the system of interest. Based as half of the nitrogen turnover in marine sediments ΔG on carefully calculated values of r, we predict a novel (Kuenen, 2008). – microbial metabolism sulfur comproportionation In another example, anaerobic oxidation of methane 2− + Ð 0 (3H2S+SO4 +2H 4S +4H2O). We show that at (AOM) by marine sediment microorganisms was hypothe- elevated concentrations of sulfide and sulfate in sized by Barnes and Goldberg on the strengths of meth- acidic environments over a broad temperature range, ane and sulfate concentration profiles from the anoxic this putative metabolism can be exergonic (ΔGr<0), sediments in the Santa Barbara Basin (California, USA), – −1 yielding ~30 50 kJ mol . We suggest that this may be and on a modest negative free energy change calculated fi suf cient energy to support a chemolithotrophic for the in situ conditions (Barnes and Goldberg, 1976). metabolism currently missing from the literature. Other Other geochemical evidence for AOM in methane–sulfate versions of this metabolism, comproportionation to transition zones of marine sediments followed (Martens 2− Ð 2− fi thiosulfate (H2S+SO4 S2O3 +H2O) and to sul te and Berner, 1977; Iversen and Jorgensen, 1985; Hoehler 2− Ð 2− + et al., 1994). Lipid biomarkers, gene surveys, fluores- (H2S+3SO4 4SO3 +2H ), are only moderately exergonic or endergonic even at ideal geochemical cence microscopy and carbon isotopes then confirmed a conditions. Natural and impacted environments, structured symbiotic relationship between a methane- including sulfidic karst systems, shallow-sea hydro- oxidizing archaeon and a sulfate-reducing bacterium thermal vents, sites of acid mine drainage, and acid– (Hinrichs et al., 1999; Boetius et al., 2000; Orphan sulfate crater lakes, may be ideal hunting grounds for et al., 2001). finding microbial sulfur comproportionators. A third example, which puzzled microbiologists for over a century, was the apparent lack in nature of com- plete ammonia oxidation (comammox). Based again in part on a thermodynamic argument, an organism with Received 3 December, 2019; revised 28 February, 2020; accepted 7 March, 2020. *For correspondence. E-mail [email protected]; Tel. this putative metabolism should have growth advan- (+1) 213 740 0652. tages – but perhaps not kinetic advantages – over © 2020 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. 2 J. P. Amend, H. S. Aronson, J. Macalady and D. E. LaRowe incomplete ammonia oxidizers (Costa et al., 2006). environment under consideration; temperature and pres- Analogous to the first two scenarios noted above, com- sure play a far more limited role. ammox bacteria were subsequently identified, culti- The direction in which a reaction can proceed and the vated and characterized from an elevated temperature associated energy yield are readily determined with the biofilm in an oil exploration well (Daims et al., 2015) relation: and from a recirculating aquaculture system (van Δ Δ 0 ð Þ Kessel et al., 2015). Their environmental distribution Gr = Gr + RTlnQr, 4 and ecological significance, however, are still largely Δ Δ 0 speculative (Koch et al., 2019). where Gr and Gr stand for the overall and standard Here, we use a thermodynamic approach to predict the Gibbs energy of reaction r, respectively, R and existence of another novel microbial metabolism – sulfur T represent the gas constant and temperature (K), comproportionation. Based on geochemical parameters, respectively, and Qr denotes the activity product. Values we then identify a number of natural and impacted target of Qr can be calculated with the expression environments where sulfur comproportionation is ener- Y ν fi i,r ð Þ getically favourable and where nding microorganisms Qr = ai , 5 capable of this metabolism may be possible. where ai represents the activity (unitless) of the ith spe- cies and ν stands for the corresponding stoichiometric Results and discussion i, r reaction coefficient. The activities of liquid water and pure Sulfur comproportionation can be interpreted either as solids, including S0 in Reaction 1, are typically set to the anaerobic oxidation of sulfide with sulfate as the elec- unity (1.0), but those of aqueous solutes are computed tron acceptor, or conversely, as the lithotrophic reduction with the equation of sulfate with sulfide as the electron donor. This process can be written to various intermediate oxidation state sul- γ Ci ð Þ ai = i 0 , 6 fur compounds, including to elemental sulfur as Ci − 3H S+SO2 +2H+ Ð 4S0 +4H O ð1Þ γ 0 2 4 2 where i, Ci and Ci stand for, respectively, the activity coefficient (unitless), concentration (usually in molality, to thiosulfate as m) and standard state concentration (usually 1 m). Values of γi can be calculated with an expression of the Debye– 2− Ð 2− ð Þ H2S+SO4 S2O3 +H2O 2 Hückel equation that takes into account the ionic strength of the solution, and the charge and other properties of and to sulfite as the solute species. For recent discussions on this topic, the reader can consult Dick (2019), LaRowe and Amend 2− Ð 2− + : ð Þ H2S + 3SO4 4SO3 +2H 3 (2019) and references therein. Energy yields for Reaction 1 were calculated at ele- Note that the reverse of Reactions 1–3 describes sulfur vated, but geochemically reasonable activities (and by disproportionation, a confirmed metabolism carried out extension, concentrations) of aqueous sulfide and sulfate by, among others, members of the Deltaproteobacteria and plotted in Fig. 1 as a function of temperature and and Thermodesulfobacteria in several natural environ- pH. It can be seen in this figure that Reaction 1 is exer- ments, including marine sediments, shallow- and deep- gonic (ΔG1<0) at acidic conditions over the entire temper- sea hydrothermal systems and alkaline hot springs (Bak ature range (0–100C) considered here. It is and Pfennig, 1987; Finster et al., 1998; Slobodkin et al., thermodynamically most favourable, with energy yields − 2012; Kojima et al., 2016; Slobodkina et al., 2016; exceeding 30 kJ mol 1,atpH≤ 3 and temperature − Slobodkin and Slobodkina, 2019). Amenabar and Boyd ≤50C; energy yields are greater than ~50 kJ mol 1 at (2018) recently reported on the first archaeal S0 pH ≤ 1 and temperature ≤ 20C. The same data are plot- disproportionator, the thermoacidophile Acidianus (strain ted in Fig. 2 as a function of sulfate and sulfide activities DS80) that is widely distributed in hot springs of Yellow- at four combinations of temperature and pH: 15C and stone National Park (Wyoming, USA). Whether the for- pH 2, 50C and pH 2, 15C and pH 5 and 50C and ward (comproportionation) or reverse (disproportionation) pH 5. This figure demonstrates that Reaction 1 can be reaction is thermodynamically favourable, depends exergonic over wide ranges of elevated but reasonable predominantly on the chemical composition of the sulfate and sulfide levels, but only at very low pH; to be © 2020 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd., Environmental Microbiology Sulfur comproportionation 3 exergonic at pH 5 (or above), the required sulfate and so. Regardless of temperature, it requires high concen- sulfide activities would have to be extremely, perhaps trations of sulfate and sulfide and very low concentrations unrealistically, high. of thiosulfate, but it is not limited to acidic pHs. As an Note that at the conditions considered here, H2S is the example, values of ΔG2 calculated with the same high − − − − dominant sulfide species, and HS (or S2 )
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