E-Letter responses to:

reports: Jessica Garvin, Roger Buick, Ariel D. Anbar, Gail L. Arnold, and Alan J. Kaufman Isotopic Evidence for an Aerobic Nitrogen Cycle in the Latest Archean Science 2009; 323: 1045-1048 [Abstract] [Full text] [PDF]

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Response to K. M. Towe's E-Letter

Jessica Garvin, Roger Buick, Ariel D. Anbar, Gail L. Arnold, Alan J. Kaufman   (30 July 2009)

Analysis of Archean Nitrogen Isotopic Data

Kenneth M. Towe   (30 July 2009)

Response to K. M. Towe's E-Letter 30 July 2009
Jessica Garvin Department of Earth and Space Sciences, University of Washington, Seattle, WA 98195, USA, Roger Buick, Ariel D. Anbar, Gail L. Arnold, Alan J. Kaufman Respond to this E-Letter: Re: Response to K. M. Towe's E-Letter	K. M. Towe has been a long-standing advocate of the idea of a generally oxidizing Archean environment (1, 2), a point of view for which there has recently been a resurgence of enthusiasm (3, 4). However, we stand by our arguments that the Mount McRae Shale nitrogen isotopic results and other geochemical data presented in companion papers (5, 6) point toward a generally anoxic environment with a brief interruption of somewhat more oxidizing conditions. We note that the scarcity of Mo and Re through most of the section, despite high (>1%) sulfide levels indicating the potential for thiol-organic scavenging (7), suggest low marine concentrations of these elements that are largely supplied by oxidative weathering (6). Moreover, the occurrence of large Δ33S mass-independently fractionated isotope anomalies, even in rocks with low organic carbon concentrations (5), implies that this signature was imparted by photolysis of sulfurous gases in an oxygen-deficient atmosphere and not by thermochemical sulfate reduction by organic compounds (4). The near-zero δ15N values through much of the section indicate low dissolved nitrate concentrations inhibiting heavy-isotope enrichment during denitrification (2). If Towe's oxic scenario were correct, we would expect persistent δ15N values above +5 per mil as in the modern oxygen- and nitrate-rich ocean, along with high Mo and Re abundances and negligible Δ33S. Instead, we find such features restricted to a narrow stratigraphic interval, most consistent with the temporary development of slightly oxygenic conditions in a persistently low-oxygen environment. Regarding Towe’s points: (i) Nitrogen fixation now allows the accumulation of substantial concentrations of dissolved nitrate in the ocean, despite the high energetic cost. This is because there is a leak of nitrogen from the bioavailable pool back to the atmosphere as N2 and N2O after denitrification, as well as to sediments as organic nitrogen. Thus, the system is close to a steady state, in which the leaks to the system encourage the continuation of nitrogen fixation in defiance of oxygenic inhibition and high energy cost. In an anoxic Archean world, ammonification would not inhibit nitrogen fixation as NH3 diffusion back to the atmosphere and organic nitrogen loss to sediments would serve as a similar stimulus to the maintenance of nitrogen fixation. (ii) Oxygen levels of 10-6 to 10-5 PAL should not, according to recent studies (8, 9), prohibit aerobic respiration given that the critical minimum level is approximately 10-7 atm (9). Thus, organic carbon would have been available for aerobic respiration and thus for oxygen consumption. Nitrogen-fixing microbes have many alternative strategies other than heterocysts to avoid oxygenic inhibition, such as temporal separation of N-fixation from O2 production, intracellular segregation of N-fixing from oxidative processes, and consortial living. So even if the TOC in Archean sedimentary rocks were all produced by oxygenic photosynthesis (a moot point for such ancient times when anoxygenic photosynthesis using Fe2+ and H2S may have been more significant), oxygen production need not have inhibited N-fixation. (iii) The 10-5 PAL figure refers to atmospheric levels of oxygen, not to those in the marine photic zone where dissolved O2 can be locally enhanced by oxygenic photosynthesis to levels supportive of nitrification, regardless of oxygen levels in the overlying atmosphere. (iv) Inhabitants of the photic zone are shielded from UV radiation even in the absence of an ozone shield by water attenuation of UV at all depths below the immediate surface layer. We see no compelling reason to adapt the data to fit an oxygenated atmosphere or to radically alter our perception of a generally anoxic Archean environment, albeit one in which temporary or localized oxygenic conditions could occur. Jessica Garvin, Roger Buick Department of Earth and Space Sciences and Astrobiology Program, University of Washington, Seattle, WA 98195-1310, USA. Ariel D. Anbar School of Earth and Space Exploration, and Department of Chemistry and Biochemistry, Arizona State University, Tempe, AZ 85287, USA. Gail L. Arnold School of Earth and Space Exploration, Arizona State University, Tempe, AZ 85287, USA. Alan J. Kaufman Department of Geology, University of Maryland, College Park, MD 20742, USA. References 1. K. M. Towe, Precambrian Res. 16, 1 (1981). 2. K. M. Towe, Palaeogeogr. Palaeoecol. 97, 113 (1991). 3. Y. Kato et al., Earth Planet. Sci. Lett. 278, 40 (2009). 4. Y. Watanabe, J. Farquhar, H. Ohmoto, Science 324, 370 (2009). 5. A. J. Kaufman et al., Science 317, 1900 (2007). 6. A. D. Anbar et al., Science 317, 1903 (2007). 7. N. Tribovillard, A. Riboulleau, T. Lyons, F. Baudin, Chem. Geol. 213, 385 (2004). 8. Q. Jin, C. M. Bethke, Geochim. Cosmochim. Acta. 69, 1133 (2005). 9. Q. Guo et al., Geology 37, 399 (2009).
Analysis of Archean Nitrogen Isotopic Data 30 July 2009
Kenneth M. Towe Department of Paleobiology, Smithsonian Institution, Eatonton, GA 31024, USA Respond to this E-Letter: Re: Analysis of Archean Nitrogen Isotopic Data	J. Garvin et al. ("Isotopic evidence for an aerobic nitrogen cycle in the latest Archean," Reports, 20 February 2009, p. 1045) accept the prevailing mainstream view that Archean oxygen levels were at or below 10-6 present atmospheric level (PAL) as they attempt to explain new nitrogen isotopic data from the organic carbon-rich 2.5-billion-year-old Mount McRae Shale. They recognize that lightning combustion is not an adequate source of fixed nitrogen in such a low-oxygen atmosphere. They therefore suggest that "microbial N2 fixation introduced NH4+ to the ocean, and increased O2 [at 10-5 PAL] promoted the oxidation of NH4+ to NO3- or NO2-" (p. 1046). They further suggest that nitrifying bacteria then used this increased surface-ocean oxygenation to convert the ammonium to nitrate as part of an aerobic nitrogen cycle. This explanation faces several problems. The very low oxygen levels assumed by Garvin et al. make their scenario for the nitrogen cycle unlikely. (i) For free-living nitrogen-fixing microbes to introduce meaningful ammonium to the Archean ocean for oxidation to nitrates, they would have to fix an amount of nitrogen substantially above their biological needs and excrete the excess. Nitrogen fixation is an energetically expensive process that requires substantial ATP per mol of N2 reduced (1). For that reason, if there is exogenous ammonia available, even at micromolar levels, nitrogenase enzymes, their nif-gene expression, and the production of oxygen-sensitive heterocysts are repressed. This ammonia repression should make the hypothesized introduction of meaningful microbial NH4+ to the surrounding Archean ocean waters an anomalous energy-intensive and potentially self-limiting, if not self-repressive, process. (ii) Surface ocean oxygen postulated to have increased from 10-6 to 10-5 PAL O2 would still be at much too low a level to support aerobic respiration. This oxygen-requiring process is necessary for the organic carbon recycling that today strongly limits carbon burial. Therefore, with this biological "sink" unavailable to rapidly sequester the net oxygen from the high productivity indicated by the high total organic carbon content of this Archean shale (noted in the Report), large quantities of net photosynthetic oxygen would have been released to the surface waters (2). Even without free ammonia, this oxygen alone would have placed pressure on nitrogen-fixing microbes, especially those without heterocysts. Elsewhere, in several attempts to circumvent this dilemma, such high-productivity blooms have been computer modeled as local "oxygen oases" (3, 4). These hypothetical cyanobacterial blooms are awkwardly model-restricted to living under an atmosphere with methane levels fixed at 1000 ppm (4) by a methanogenic H2-based stagnant surface ocean productivity (5). (iii) Nitrifying bacteria are repressed if dissolved oxygen drops to levels below about 1 to 2 mg/liter (ppm) at which point nitrification is inhibited. As with aerobic recycling of organic carbon, a surface-ocean oxygen level increased to 10-5 PAL cannot have sustained substantial nitrification. (iv) A global atmosphere, even at 10-5 PAL oxygen, cannot support a stratospheric ozone screen and virtually no UV protection would exist for surface-dwelling microbiotas, especially those using visible light for primary production of organic carbon (plankton; stromatolites). Given these difficulties, should the isotopic data be adapted to fit the computer-modeled atmospheres, or should these continually changing models be adjusted to fit the new data? An atmosphere closer to 10-2 PAL [as in Garvin et al.’s Report and (6)] may help explain the various inconsistencies. Lightning-induced fixation of nitrogen could take place, a moderate ozone screen would allow photosynthesis, and no hypothetical oxygen oases would be required. Kenneth M. Towe Department of Paleobiology, Smithsonian Institution, 157 Broadlands Drive, Eatonton, GA 31024, USA. References 1. J. R. Postgate, Phil. Trans. R. Soc. London B296, 375 (1982). 2. K. M. Towe, Nature 348, 54 (1990). 3. J. F. Kasting, Global Planet. Change 97, 125 (1991). 4. A. A. Pavlov, J. F. Kasting, Astrobiology 2, 27 (2002). 5. P. Kharecha et al., Geobiology 3, 53 (2005). 6. K. M. Towe, Adv. Space Res. 18, 7 (1996).