LETTER
No evidence for manganese-oxidizing photosynthesis In PNAS, Johnson et al. (1) argue that a hitherto unknown form of photosynthesis using Mn as electron donor was the precursor to the evolution of cyanobacteria. The authors conclude this from chemical tracers, particularly putative remnants of Mn oxides in the rock record some 2.4 billion y ago (1). Although we applaud the elegant analytical work in this report, we argue that the paper presents no evidence for Mn photosynthesis as precursor to cyanobacteria. To conclude that Mn oxide deposition in the Koegas requires Mn photosynthesis, Mn oxidation with O2 must be ruled out. O2 cannot be ruled out with the calculations made by Johnson et al. (1) because they use an inappropriate kinetic expression, do not fully consider the range of plausible depositional conditions, and place far too much faith in the ability of geochemical proxies to precisely and accurately define seawater O2 concentrations. To translate seawater O2 concentrations to Mnoxidation rates, Johnson et al. use a kinetic expression of microbial Mn oxidation derived from experiments in the Black Sea. Such expressions scale strongly with cell density, so their use in other environments without considering cell density is inappropriate and could lead to one to two orders-of-magnitude of uncertainty. Furthermore, sedimentation rates orders-of-magnitude lower than those used by Johnson et al. have been determined for the depositional basin (2). According to the kinetic expression used, O2 would be sufficient to sustain the observed Mn-oxide deposition at these sedimentation rates, even at Johnson et al.’s upper limit of 10−5.7 atm (2.6 nM).
This 10−5.7 atm O2 upper limit is based on the preservation of oxygen-sensitive detrital pyrites in the depositional basin and patterns of mass-independent fractionation of sulfur isotopes (the S-MIF proxy). Detrital pyrite preservation, however, is predicted to be possible at 10−3.1 atm O2 (1 μM). The S-MIF proxy yields an atmospheric O2 concentration (not seawater) only from reaction-transport modeling, which itself is based on putative and debated reactions for S-MIF formation with uncertain modes of S-MIF preservation (3). Moreover, by analogy to the modern ocean, productive seawater can be highly oversaturated in O2 with respect to the atmosphere, and surface ocean O2 concentrations of 20 μM have been predicted as possible, even under an Archean atmosphere of 10−7 atm O2 (4). Independent of the uncertainties in the sedimentation rates and kinetics of Mn oxidation, the O2 levels permissible within the constraints afforded by the proxies are sufficient to account for the observed Mn deposition. Finally, to assert that Mn photosynthesis predated cyanobacteria, the authors have generally dismissed geochemical evidence for much earlier O2 production as arising from other abiotic or biotic O2 sources. This argument is inconsistent with molecular clocks dating cyanobacterial evolution well before Koegas sediment deposition (5). If they existed, however, these alternative abiotic or biotic sources of O2 could lead to Mn-oxide deposition in the Koegas without requiring Mn oxidizing photosynthesis. Therefore, the
E4118 | PNAS | October 29, 2013 | vol. 110 | no. 44
conclusion that Mn-oxidizing photosynthesis produced the Koegas Mn deposits is highly tenuous. In our view, the Mn-oxide remnants in the Koegas rocks are more likely indicative of rising seawater oxygen concentrations leading up to the Great Oxidation Event, not Mn-oxidizing photosynthesis, for which we find no evidence. CarriAyne Jonesa and Sean Andrew Crowea,b,1 a
Department of Microbiology and Immunology and bDepartment of Earth, Ocean, and Atmospheric Sciences, University of British Columbia, Vancouver, BC, Canada V6T 1Z3 1 Johnson JE, et al. (2013) Manganese-oxidizing photosynthesis before the rise of cyanobacteria. Proc Natl Acad Sci USA 110(28): 11238–11243. 2 Altermann W, Nelson DR (1998) Sedimentation rates, basin analysis and regional correlations of three Neoarchaean and Palaeoproterozoic sub-basins of the Kaapvaal craton as inferred from precise U-Pb zircon ages from volcaniclastic sediments. Sediment Geol 120(1–4):225–256. 3 Whitehill AR, Ono S (2012) Excitation band dependence of sulfur isotope mass-independent fractionation during photochemistry of sulfur dioxide using broadband light sources. Geochim Cosmochim Acta 94:238–253. 4 Pavlov AA, Brown LL, Kasting JF (2001) UV shielding of NH3 and O2 by organic hazes in the Archean atmosphere. J Geophys Res Planets 106(E10):23267–23287. 5 Schirrmeister BE, de Vos JM, Antonelli A, Bagheri HC (2013) Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event. Proc Natl Acad Sci USA 110(5):1791–1796.
Author contributions: C.J. and S.A.C. designed research; C.J. performed research; C.J. analyzed data; and C.J. and S.A.C. wrote the paper. The authors declare no conflict of interest. 1
To whom correspondence should be addressed. E-mail: sean. [email protected].
www.pnas.org/cgi/doi/10.1073/pnas.1314380110
No evidence for manganese-oxidizing photosynthesis In PNAS, Johnson et al. (1) argue that a hitherto unknown form of photosynthesis using Mn as electron donor was the precursor to the evolution of cyanobacteria. The authors conclude this from chemical tracers, particularly putative remnants of Mn oxides in the rock record some 2.4 billion y ago (1). Although we applaud the elegant analytical work in this report, we argue that the paper presents no evidence for Mn photosynthesis as precursor to cyanobacteria. To conclude that Mn oxide deposition in the Koegas requires Mn photosynthesis, Mn oxidation with O2 must be ruled out. O2 cannot be ruled out with the calculations made by Johnson et al. (1) because they use an inappropriate kinetic expression, do not fully consider the range of plausible depositional conditions, and place far too much faith in the ability of geochemical proxies to precisely and accurately define seawater O2 concentrations. To translate seawater O2 concentrations to Mnoxidation rates, Johnson et al. use a kinetic expression of microbial Mn oxidation derived from experiments in the Black Sea. Such expressions scale strongly with cell density, so their use in other environments without considering cell density is inappropriate and could lead to one to two orders-of-magnitude of uncertainty. Furthermore, sedimentation rates orders-of-magnitude lower than those used by Johnson et al. have been determined for the depositional basin (2). According to the kinetic expression used, O2 would be sufficient to sustain the observed Mn-oxide deposition at these sedimentation rates, even at Johnson et al.’s upper limit of 10−5.7 atm (2.6 nM).
This 10−5.7 atm O2 upper limit is based on the preservation of oxygen-sensitive detrital pyrites in the depositional basin and patterns of mass-independent fractionation of sulfur isotopes (the S-MIF proxy). Detrital pyrite preservation, however, is predicted to be possible at 10−3.1 atm O2 (1 μM). The S-MIF proxy yields an atmospheric O2 concentration (not seawater) only from reaction-transport modeling, which itself is based on putative and debated reactions for S-MIF formation with uncertain modes of S-MIF preservation (3). Moreover, by analogy to the modern ocean, productive seawater can be highly oversaturated in O2 with respect to the atmosphere, and surface ocean O2 concentrations of 20 μM have been predicted as possible, even under an Archean atmosphere of 10−7 atm O2 (4). Independent of the uncertainties in the sedimentation rates and kinetics of Mn oxidation, the O2 levels permissible within the constraints afforded by the proxies are sufficient to account for the observed Mn deposition. Finally, to assert that Mn photosynthesis predated cyanobacteria, the authors have generally dismissed geochemical evidence for much earlier O2 production as arising from other abiotic or biotic O2 sources. This argument is inconsistent with molecular clocks dating cyanobacterial evolution well before Koegas sediment deposition (5). If they existed, however, these alternative abiotic or biotic sources of O2 could lead to Mn-oxide deposition in the Koegas without requiring Mn oxidizing photosynthesis. Therefore, the
E4118 | PNAS | October 29, 2013 | vol. 110 | no. 44
conclusion that Mn-oxidizing photosynthesis produced the Koegas Mn deposits is highly tenuous. In our view, the Mn-oxide remnants in the Koegas rocks are more likely indicative of rising seawater oxygen concentrations leading up to the Great Oxidation Event, not Mn-oxidizing photosynthesis, for which we find no evidence. CarriAyne Jonesa and Sean Andrew Crowea,b,1 a
Department of Microbiology and Immunology and bDepartment of Earth, Ocean, and Atmospheric Sciences, University of British Columbia, Vancouver, BC, Canada V6T 1Z3 1 Johnson JE, et al. (2013) Manganese-oxidizing photosynthesis before the rise of cyanobacteria. Proc Natl Acad Sci USA 110(28): 11238–11243. 2 Altermann W, Nelson DR (1998) Sedimentation rates, basin analysis and regional correlations of three Neoarchaean and Palaeoproterozoic sub-basins of the Kaapvaal craton as inferred from precise U-Pb zircon ages from volcaniclastic sediments. Sediment Geol 120(1–4):225–256. 3 Whitehill AR, Ono S (2012) Excitation band dependence of sulfur isotope mass-independent fractionation during photochemistry of sulfur dioxide using broadband light sources. Geochim Cosmochim Acta 94:238–253. 4 Pavlov AA, Brown LL, Kasting JF (2001) UV shielding of NH3 and O2 by organic hazes in the Archean atmosphere. J Geophys Res Planets 106(E10):23267–23287. 5 Schirrmeister BE, de Vos JM, Antonelli A, Bagheri HC (2013) Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event. Proc Natl Acad Sci USA 110(5):1791–1796.
Author contributions: C.J. and S.A.C. designed research; C.J. performed research; C.J. analyzed data; and C.J. and S.A.C. wrote the paper. The authors declare no conflict of interest. 1
To whom correspondence should be addressed. E-mail: sean. [email protected].
www.pnas.org/cgi/doi/10.1073/pnas.1314380110
