1. Lecture 8: Cyanobacteria and the Rise of Oxygen and Ozone Abiol 574

2. Different forms of cyanobacteria (formerly “blue-green algae”) a) Chroococcus b) Oscillatoria c) Nostoc (coccoid) (filamentous) (heterocystic) Nitrogen-fixing

3. Trichodesmium bloom Berman-Frank et al., Science (2001) Fix N in the morning Produce O 2 in the afternoon

4. Cyanobacteria are a key part of the modern marine ecosystem because of their ability to fix nitrogen We also know that oxygenic photosynthesis was first invented by the cyanobacteria, as clearly demonstated by molecular phylogeny 

5. cyanobacteria Chloroplasts in algae and higher plants contain their own DNA Cyanobacteria form part of the same branch on the rRNA tree Interpretation (due to Lynn Margulis * ): Chloroplasts resulted from endosymbiosis * and Konstantin Meresch- kowski long before this

6. Implications Oxygenic photosynthesis was only invented once! Cyanobacteria invented it, and then some eukaryote imported a cyanobacterium (endosymbiosis) and made a living from it. All higher plants and algae descended from this primitive eukaryote.

7. Cyanobacteria and the rise of O 2 Prokaryotic (no cell nucleus) –By contrast, eukaryotes have a cell nucleus Facultative aerobes (able to photosynthesize oxygenically or anoxygenically) Purported evidence for cyanobacteria at 2.7 Ga from 2-alpha methylhopanes preserved in sediments from the Pilbara Craton, Western Australia (R.E. Summons et al., Nature, 1999) These sediments were also thought to contain lipid biomarker evidence (steranes) for O 2 -requiring eukaryotes (J. Brocks et al., Science, 1999)

8. Early evidence for photosynthesis Presence of steranes in the 2.7 b.y-old Jeerinah formation in northwestern Australia (Summons et al., Nature, 1999; Eigenbrode & Freeman, PNAS, 2006)  free O 2 was present at this time, and thus cyanobacteria must have been present, as well --This is disputed by Jochen Brocks, who now thinks that the biomarkers are from later contamination Direct evidence for cyanobacteria (2-  methyl- hopanes) is also questioned by some because these compounds are found in other anaerobic bacteria http://www-eaps.mit.edu/geobiology/biomarkers/ steroids.html Steranes come from sterols, e.g., cholesterol

9. New Agouron drill core New drill holes (2 of them) done by the Agouron Institute, summer (2012) Second hole went through the 2.69-2.63 Ga Jeerinah Formation in western Australia Water (with fluorescent green dye) was used as the drilling fluid No biomarkers of any sort were found.. Interim Agouron Pilbara Drilling Project Report Roger Buick, Christian Hallmann, Katherine French and Roger Summons

10. That said, there is still pretty good evidence that O 2 was being produced before the GOE…

11. Science (2007) Mb is forms an insoluble sulfide in reduced environments A Mb enhancement in shales requires oxidative weathering of sulfides on land, followed by transport of soluble molybdate ion to sediments The best way to do this, in my view (and that of Reinhard and Planavsky, Nature, 2013) is for the entire atmosphere to become O 2 -rich for short time periods

12. Nature, Sept. 26, 2013 In a paper that is coming out today, Crowe et al. argue that atmospheric O 2 reached levels of ~3  10 -4 PAL at ~3.0 Ga The analysis is based on 53 Cr depletion in the Nsuze paleosol (above) and enrichment of 53 Cr and U in the contemporaneous Ijzermyn iron formation (next slide)

13. Cr isotopes and pO 2 Cr has two accessible oxidation states, Cr +3 and Cr +6. As with U, the oxidized state is soluble, while the reduced state is insoluble 53 Cr is enriched in the +6 state relative to 52 Cr when Cr is oxidized If O 2 is present during weathering, then 53 Cr is preferentially removed from soils and deposited in sediments, such as BIFs

14. Nature, Sept. 26, 2013 These data are from the Ijzermyn iron formation Both 53 Cr and U are enriched relative to the mantle and/or crust

15. Let’s now look at the geologic evidence for the (main) rise of O 2 …

16. Geologic O 2 Indicators H. D. Holland (1994) (Detrital) Blue boxes indicate low O 2 Red boxes indicate high O 2 Dates have been revised; the initial rise of O 2 is now placed at 2.45 Ga

17. Permian and Triassic Redbeds A redbed from the Palo Duro Canyon in West Texas http://www.utpb.edu/ceed/GeologicalResources/West_Texas_Geology/ links/permo_triassiac.htm

18. Caprock Canyon (Permian and Triassic) redbeds Redbeds contain oxidized, or ferric iron (Fe +3 ) –Fe 2 O 3 (Hematite) Their formation requires the presence of atmospheric O 2 Reduced, or ferrous iron, (Fe +2 ) is found in sandstones older than ~2.2 b.y. of age http://www.utpb.edu/ceed/GeologicalResources/West_Texas_Geology/links/permo_triassiac.htm

19. Banded iron- formation or BIF (>1.8 b.y ago) Fe +2 is soluble, while Fe +3 is not BIFs require long- range transport of iron  The deep ocean was anoxic when BIFs formed

20. What BIFs tell us about O 2 Need to have an anoxic deep ocean filled with ferrous iron, Fe +2, in order to supply the iron (Holland, 1973) –Rare Earth element patterns  Much of the iron comes from the midocean ridges Banding is probably caused by seasonal upwelling

21. Witwatersrand gold ore with detrital pyrite (~3.0 Ga) Pyrite = FeS 2 oxidized during weathering today  Atmospheric O 2 was low when this deposit formed P. Cloud, Oasis in Space (1988)

22. What detrital pyrite and uraninite tell us about O 2 Uraninite: UO 2 (U +4 ) –U +4 insoluble, U +6 soluble (opposite behavior from iron) Oxidative weathering of the land surface was not occurring prior to ~2.3 Ga Atmospheric O 2 was therefore fairly low (< about 10 -2 PAL (times the Present Atmospheric Level)

23. The best evidence for the rise of O 2 now comes from sulfur isotopes…

24. S isotopes and the rise of O 2 Sulfur has 4 stable isotopes: 32 S, 33 S, 34 S, and 36 S Normally, these separate along a standard mass fractionation line In very old (Archean) sediments, the isotopes fall off this line Requires photochemical reactions (e.g., SO 2 photolysis) in a low-O 2 atmosphere SO 2 + h  SO + O –This produces “MIF” (mass-independent fractionation)

25. “Normal” isotope mass fractionation Vibrational energy levels depend inversely on the reduced mass  = (k/m R ) 1/2 E n = (n+½) h  Increasing the mass of one or both atoms decreases the vibrational frequency and energy, thereby strengthening chemical bonds A simple harmonic oscillator

26. S isotopes in Archean sediments Sulfides (pyrite) fall above the mass fractionation line Sulfates (barite) fall below it Farquhar et al. (2001) (FeS 2 ) (BaSO 4 )  33 S

27.  33 S versus time Farquhar et al., Science, 2000 73 Phanerozoic samples High O 2 Low O 2

28. Updated sulfur MIF data (circa 2008) (courtesy of James Farquhar) glaciations (Note the increase in vertical scale)

29. MIF data summer 2013 The pattern in  33 S continues to hold as new data are added Note the significant disparity between positive and negative  33 S values –Need a larger sulfur reservoir for the negative values so that the isotopic signal is diluted

30. MIF data summer 2013 Note also the apparently smaller values of  33 S near 3.0 Ga, the same time that the new Cr isotope data point to finite levels of atmospheric O 2 –The MIF signal wouldn’t disappear entirely even if pO 2 was high, because of reworking of older MIF-rich sediments

31. Question: What does the sulfur MIF tell us? 1.Must have had low enough O 2 (and O 3 ) to allow SO 2 to be photolyzed 2.Must have had low enough O 2 to prevent all volcanic SO 2 from being oxidized to sulfate, as it is today Start with point 2 

32. Archean sulfur cycle Kasting, Science (2001)[Redrawn from Kasting et al., OLEB (1989)] In a low-O 2 atmosphere, volcanic SO 2 can be either oxidized or reduced (or it can exit the atmosphere as SO 2 ) By contrast, today, virtually all SO 2 is oxidized to sulfate; thus, any MIF signal is eliminated by homogenization

33. “Archean” sulfur removal rates Pavlov and Kasting (2002) Typically, SO 2, H 2 S, and S 8 are the main exit routes for sulfur from a low-O 2 atmosphere

34. Production of sulfur “MIF” by SO 2 photolysis J.R. Lyons, GRL (2007) UV absorption coefficientsBlowup of different forms of SO 2 The different isotopologues of SO 2 (e.g. 32 SO 2 and 33 SO 2 ) absorb UV radiation at slightly different wavelengths MIF signal forms here

35. PNAS, 2009 Shielding by OCS (or O 3 ) produces the right sign for  33 S because of the slope of their absorption x-sections in the 190-220 nm region Mark Claire and I don’t think this actually works, though. One reason is that OCS is very short-lived in a low-O 2 environment. We’re still arguing about how exactly the MIF signal is generated. 190 200210220 Wavelength (nm)

36. There still are some who don’t believe that sulfur MIF requires low O 2 Hiroshi’s group has suggested that sulfur MIF was caused by reactions between sulfate and organic matter in sediments, not by atmospheric processes They have produced one datapoint with  33 S  2‰ (diagram on right). This was done by reacting solid glycine with sulfate in the lab. The proposed mechanism for producing MIF is surface reactions --To my knowledge, this has not been supported by theory or, more precisely, the supporting theory has been shown to be incorrect (Balan et al., EPSL, 2009) Science, 2009 Laboratory data Sedimentary sulfides

37. Possible alternative mechanisms for causing sulfur MIF Spin-orbit (hyperfine) interactions between the nucleus and the electron cloud (referred to by geochemists as a magnetic isotope effect, or MIE) –Ruled out for Farquhar’s data because the effect is seen in both 33 S (nuclear spin 1) and 36 S (nuclear spin 0) –Significant  36 S measured in 2 of 9 of Yumiko’s experiments  inconclusive? Nuclear field shift effect –Electrostatic interaction between a non-spherical nucleus and the electron cloud

38. http://www.ornl.gov/info/ornlreview/v36_1_03/article_34.shtml Caption: The likely shape of a deformed uranium-234 nucleus was determined in 1971 by ORNL physicists. This and other unstable nucleides have measureable electric quadru- pole moments 234 U nucleus Halflife: ~250,000 yrs

39. http://ie.lbl.gov/systematics/chart_thb2.pdf

40. Quadrupole deformation chart http://ie.lbl.gov/systematics/chart_thb2.pdf Sulfur Bottom line: It’s very unlikely that sulfur MIF was caused by nuclear field shift effects So, the only fractionation mechanism that appears plausible is still SO 2 photolysis  Farquhar’s story still stands Sulfur

41. Finally, let’s think about what this implies for stratospheric ozone…

42. The rise of ozone Ozone (O 3 ) is important as a shield against solar UV radiation Very little ozone would have been present prior to the rise of atmospheric O 2 We can calculate how the ozone layer develops as atmospheric O 2 levels increase 

43. Ozone and temperature at different O 2 Levels 1-D climate modelPhotochemical model A. Segura et al. Astrobiology (2003) The ozone layer The ozone layer does not really disappear until O 2 levels fall below ~1% of the Present Atmospheric Level (PAL)

44. Ozone column depth vs. pO 2 Kasting et al. (1985) Why the nonlinearity? O 2 + h  O + O O + O 2 + M  O 3 + M As O 2 decreases, O 2 photolysis occurs lower down in the atmosphere where number density (M) is higher -- So, O 3 column depth is virtually unaffected Eventually, the photolysis peak moves into the tropo- sphere, where H 2 O also photolyzes, producing O 3 - destroying HO x radicals

45. Conclusions Atmospheric O 2 levels were low prior to ~2.4 b.y. ago –Cyanobacteria were responsible for producing this O 2 –The best evidence for this comes from sulfur MIF An effective ozone screen against solar UV radiation was established by the time pO 2 reached ~0.01 PAL, probably around 2.4 Ga (Not discussed) O 2 probably went up for a second time near the end of the Proterozoic, 600-800 m.y. ago, possibly triggering the Cambrian explosion