Morphological Record of Oxygenic Photosynthesis in Conical Stromatolites

Morphological record of oxygenic photosynthesis in conical stromatolites

Tanja Bosak1,2, Biqing Liang1, Min Sub Sim, and Alexander P. Petroff

Department of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139

Edited by Paul F. Hoffman, Harvard University, Cambridge, MA, and approved May 15, 2009 (received for review January 27, 2009) Conical stromatolites are thought to be robust indicators of the meter-sized bubbles (13) [Fig. 1 and supporting information (SI) presence of photosynthetic and phototactic microbes in aquatic Fig. S1]. Using enrichment cultures of modern cone-forming environments as early as 3.5 billion years ago. However, photo- cyanobacteria from Yellowstone National Park, here, we test the taxis alone cannot explain the ubiquity of disrupted, curled, and influence of light on the centimeter- to submillimeter-scale contorted laminae in the crests of many Mesoproterozoic, Paleo- external and internal morphology of cyanobacterial cones and proterozoic, and some Archean conical stromatolites. Here, we link the formation of oxygen-rich bubbles in the tips of modern demonstrate that cyanobacterial production of oxygen in the tips cyanobacterial cones to the fossil gas bubbles present in the of modern conical aggregates creates contorted laminae and sub- central zone of modern, Proterozoic, and even some Archean millimeter-to-millimeter-scale enmeshed bubbles. Similarly sized conical stromatolites. fossil bubbles and contorted laminae may be present only in the crestal zones of some conical stromatolites 2.7 billion years old or Bubble Formation at the Tips of Modern Conical Structures younger. This implies not only that cyanobacteria built Proterozoic Light is critical both for the growth of photosynthetic cone- conical stromatolites but also that fossil bubbles may constrain the forming cyanobacteria (10) and as a determinant of the resulting timing of the evolution of oxygenic photosynthesis. morphology of biofilms (Fig. S2). Although ridged or flatter structures grow at higher light intensities, low-light conditions cyanobacteria ͉ microbialite enhance the growth of prominent cones with axes inclined in the direction of light (Fig. S2). Higher photosynthetic activity in the tips of these cones (Fig. 2B), in turn, often leads to the formation xygenic photosynthesis irreversibly changed the Earth’s of oxygen-rich bubbles in our enrichment cultures but not on the surface environment by using light energy to split water and O sides of cones (i.e., in the zones of highest photosynthetic activity evolve molecular oxygen (Eq. 1) under light-limiting conditions). These bubbles, colonized by a CO ϩ H O 3 O ͑g͒ ϩ CH O. mesh of filamentous cyanobacteria, are generally much smaller 2 2 2 2 than cones and do not confer a conical shape onto the mat. The timing of the evolution of this metabolism is controversial Bubbles are either clearly visible (Fig. 2A) or can be detected in (1–7), but it must have predated the geochemical record of initial cross-sections of modern lithifying cones as submillimeter- and oxygenation of the atmosphere at 2.4 billion years ago (Ga) (8). millimeter-diameter features with nearly-circular cross-sections The sedimentary record of photosynthetic microbial communi- (i.e., completely enclosed by laminae) (Fig. 2C and Figs. S3 and ties is at least 1 billion years older (9) and commonly written in S4). Bubbles surrounded by a thick, actively photosynthesizing the laminated and lithified sedimentary structures called stro- mesh can grow into irregularly shaped blisters, disrupt the matolites. Conical stromatolites are a distinct morphological laminae (Fig. 2C and Fig. S5) or initiate the growth of millime- group that, to date, lacks plausible abiotic analogs, but the ter- to centimeter-diameter tubes. metabolic provenance of their microbial builders remains diffi- If mechanically and gravitationally stable bubbles are to form, cult to establish even in structures much younger than 2.4 Ga. to persist, and to become preserved by fast lithification, they Ϸ Modern conical stromatolites are thought to owe their distinct should be smaller than 5 mm in diameter and heavily en- shape to biological processes because thin filamentous cyanobac- meshed. The recognition of fossil bubbles as features with teria are known to form small cones (10) even in the complete nearly-spherical cross-section will then be possible if the sur- absence of lithification. Light is essential for the growth of rounding microbial mesh is preserved by sufficiently small cyanobacterial biomass in modern cone-building biofilms (10). crystals (i.e., smaller than the average lamina thickness), and if The upward migration of phototactic filaments is thought to be significant recrystallization does not occur. In modern hot springs (14) and in our cultures that contain less than Ϸ2mM another mechanism contributing to the vertical growth of mod- Ϸ ern cones (10), although it remains unclear whether this vertical inorganic carbon, only bubbles smaller than 0.2 mm are MICROBIOLOGY enclosed by a thick mesh (Fig. S3). Larger nearly-spherical growth is due to phototaxis or simply to the enhanced growth at bubbles in these environments will be enclosed by a much more the tips of cones. Once a conical structure forms, models porous or discontinuous mesh of filaments and not necessarily suggests that the fast vertically accreting mat may propagate the preserved or identifiable. Bubbles that form in the centers of shape through successive laminae in the presence of fast lithi- very narrow central zones (Ͻ200 ␮m) would be similarly difficult fication (11). to preserve and recognize. In deeper waters, at lower photosyn- Models assuming an enhanced accumulation of biomass at topographic highs (11) or the vertical orientation of long fila- GEOLOGY ments at the tips of stromatolites (10) can account for the Author contributions: T.B., B.L., and M.S.S. designed research; T.B., B.L., M.S.S., and A.P.P. thickening of the laminae in the centers of conical stromatolites performed research; T.B., B.L., M.S.S., and A.P.P. analyzed data; and T.B. and B.L. wrote the (12). Yet, these models cannot account for other common paper. characteristics of the crestal zone, a prominent but poorly The authors declare no conﬂict of interest. understood internal feature defining an entire class of Paleo- and This article is a PNAS Direct Submission. Mesoproterozoic conical stromatolites that formed in quiet 1T.B. and B. L. contributed equally to this work. zones outside the influence of waves and storms (12) (Fig. 1A). 2To whom correspondence should be addressed. E-mail: [email protected]. The crestal zone often has contorted or discontinuous laminae, This article contains supporting information online at www.pnas.org/cgi/content/full/ some of which appear to have enclosed submillimeter- to milli- 0900885106/DCSupplemental.

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0900885106 PNAS ͉ July 7, 2009 ͉ vol. 106 ͉ no. 27 ͉ 10939–10943 Downloaded by guest on October 4, 2021 Fig. 1. Center of a conical stromatolite [Atar Formation, Atar Group, Mauritania, Late Mesoproterozoic (53, 54), sample provided by A. Maloof]. (A) Mosaic photomicrograph of the central zone (thin section). The white rectangle surrounds the area shown in B, and the arrows point to fossil bubbles. (Scale bar, 1 cm.) (B) A typical nearly-circular submillimeter feature surrounded by dark laminae in the middle of the stromatolite (white arrow). This fossil bubble is found on top of a larger, irregularly shaped feature surrounded by contorted laminae (outlined by a dashed line) that may be a former mat-trapped bubble. (Scale bar, 1 mm.) (C) Fossil bubbles are absent from laminae on the sides of the same conical stromatolite. (Scale bar, 1 mm.) (D) Histogram showing the diameters (in millimeters) of fossil bubbles in 18 well-preserved Proterozoic conical stromatolites. Bubbles were identiﬁed as submillimeter- and millimeter-diameter features with nearly-circular cross-sections enclosed by laminae.

thetic rates, or in solutions rich in dissolved inorganic carbon, Discussion however, even millimeter-scale photosynthetic bubbles will be The presence of cone-forming cyanobacteria can easily explain extensively covered by a microbial mesh and more likely to be the growth of bubbles enclosed by primary laminae in the crests preserved by syngenetic mineralization (Figs. S4, S5, and S6). of conical stromatolites and the accumulation of sufficient gas to overcome considerable hydrostatic pressure at depth (more than Bubbles in Proterozoic Conical Stromatolites twice the atmospheric pressure at 10 m). On the other hand, Nearly-circular features enclosed by contorted laminae are light-independent microbial production of gases such as H2, primarily observed at the tips of some well-preserved Protero- CH4,CO2, CO, and H2S, N2O, and N2 require abundant organic zoic conical stromatolites but not on the sides (Fig. 1 and Fig. matter or high concentrations of nitrate in the solution, the latter S1). The analogy with modern laminated cones suggests that requiring the presence of atmospheric oxygen. Unlike oxygen these circular features originated as submillimeter- to millime- bubbles that give a circular shape to the laminae formed by ter-sized gas bubbles. The localization of millimeter-scale con- primary producers at the top of the structure (Fig. 2 and Fig. S4), torted laminae in conical stromatolites to the topographic highs fenestrae originating from the decay of unmineralized organic implies that those were the spots of active in situ production of matter in rapidly accreting tips tend to destroy the primary gas, whereas the absence of fossil bubbles on the sides of conical lamination and tend to have irregular shape distributions (e.g., stromatolites suggests that the local gas concentration was not ref. 15). In contrast, the inferred bubbles in conical stromatolites sufficient to create bubbles. Areas enclosed by contorted and are restricted only to the crests even in the very narrow (milli- sometimes disrupted laminae (12) in the crests of conical meter-wide) central zones (Fig. S1), where they do not disrupt stromatolites are thus a likely consequence of gas release the surrounding laminae. The degradation of organic matter by resulting from higher microbial metabolic activity on the topo- methanogenic microbes can produce bubbles at large depths (16) graphic highs (Fig. 1 and Fig. S1). These inferred gas bubbles in that, coupled with methanotrophy, can lead to the precipitation coniform stromatolites can occupy anywhere from 0% to Ϸ20% of large-scale carbonate structures with central vents. These of the central zone (13). carbonate structures differ from conical stromatolites because

Fig. 2. Oxygen and bubble production in modern conical aggregates dominated by cyanobacteria. (A) Bubbles often form at the tips of cones and are partly or completely covered by biofilm. Note that these bubbles did not lift the mat up into a conical structure. (Scale bar, 5 mm.) (B) Profiles of oxygen (filled circles) and gross photosynthetic rate (white bars) and oxygen uptake rate (gray bars) within a cone. Depth 0 mm denotes the tip of the cone and Ϫ6 mm is the bottom of the cone. (C) Transmitted-light micrograph of a 30-␮m-thick thin section of a cone showing disrupted fabrics, large voids (former blisters), and bubbles in the center. Multiple pores surrounded by cyanobacterial filaments were present in the series of successive thick sections, confirming that the porosity was not an artifact. The sample had an elliptical cross-section, and it was sectioned along the minor axis. (Scale bar, 1 mm.)

10940 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0900885106 Bosak et al. Downloaded by guest on October 4, 2021 Table 1. Presence of contorted laminae, a distinct axial zone, and bubble-like structures in Archean conical stromatolites Contorted laminae and/or Cement-ﬁlled contorted laminae Age, Ga* distinct axial zone (possible fossil bubbles) Reference† Continent

3.4 Absent Absent Allwood et al., 2007 (37); Hofmann Australia et al., 1999 (38); Lowe, 1980 (39) 3.1–2.9 Absent Absent Beukes and Lowe, 1989 (40) Africa 3.0–2.8 Unclear‡ Unclear‡ Hofmann et al., 1985 (41) North America 2.9–2.7 Unclear§¶ Unclear§¶ Wilks and Nisbet, 1985 (42) North America 2.8 Ϯ? Probably absentʈ Probably absentʈ Donaldson and deKemp, 1998 (43) North America 2.7 Present Present Hofmann and Masson, 1994 (23) North America 2.7 Present Present** Sakurai et al., 2005 (44); Van Australia Kranendonk et al., 2006 (25) 2.7–2.6 Poorly deﬁned and Unclear¶ Grey, 1981 (45) Australia narrow 2.7 Present Present Hofmann et al., 1991 (24) North America 2.6–2.9 Present Unclear¶ Srinivasan et al., 1990 (46) Asia 2.7–2.6 Present Present Walter, 1983 (47); Abell et al., 1985 Africa (48) 2.7–2.6 Unclear¶ Unclear¶ Lambert, 1998 (49) North America Ͻ2.63 Unclear¶ Unclear¶ Murphy and Sumner, 2008 (50) Australia 2.63–2.52 Present Present Beukes, 1987 (26); Buck, 1980 (51); Africa Altermann, 2008 (27)

*Ages based on the references listed in table 1 in Schopf (52) and Hofmann (28). †References only given for the sources that contain detailed descriptions and/or images of conical stromatolites. ‡Biogenicity and stromatolitic nature questionable (41). ¶Insufﬁcient detail given in the published pictures or preserved. §Stromatolites are poorly preserved. ʈInsufﬁcient detail given in the published picture. **Contorted laminae consistent with the former presence of a bubble can be seen in the middle of a well-developed central zone can be seen in Van Kranendonk et al. (25), although we are not aware of any published photographs showing a thin section.

the former lack continuous laminae, their porosity is not spatially conical stromatolites as early as 2.7 Ga (23–25) and in more restricted to topographic highs, and they contain carbonate widespread cones on Late Archean carbonate platforms (26, 27) minerals exhibiting characteristically depleted carbon isotopes (Table 1 and Fig. 3). The apparent absence of fossil bubbles in (17) that are not observed in well-preserved stromatolites (18). the few Archean cones older than 2.7 Ga (Table 1 and Fig. S7) The presence of methanogens in communities with anoxygenic may be attributed both to poor preservation and to a very small photosynthetic microbes could potentially account for the large- number of described conical stromatolites (28), but further scale conical shape of stromatolites, and, possibly, the localiza- experiments are needed to determine whether these cones could tion of bubbles at the tips. This model is unlikely because have grown in the presence of anoxygenic photosynthetic mi- anoxygenic phototrophs and methanogens actually compete for crobes. The origin of gas-related features in Archean conical substrates in some modern environments (19), suggesting that stromatolites thus deserves focused investigation because these intense production of methane should not be expected in the features may be the first detectable traces of oxygen exhaled zones of highest photosynthetic activity. Moreover, processes under an anoxic atmosphere that forever changed the surface such as microbial iron and sulfate reduction and fermentation environment on our planet. would be energetically better poised to degrade of organic matter close to the photosynthetic layer in the thin bubble- enclosing laminae, diminishing the likelihood of abundant methane production. Although further search for cone-building and gas-producing anaerobic photosynthetic communities is war- ranted, such communities are not known currently. We also note MICROBIOLOGY that hydrogen-based anoxygenic photosynthesis would take up H2 and CO2, thereby reducing the local concentration of gases needed to form bubbles. Overall, stromatolite growth in the presence of strongly phototactic cyanobacteria best accounts for the presence of inferred fossil bubbles at the tips of nondivergent conical stromatolites. Gas-bubble entrapment has been suggested as the origin of GEOLOGY axial porosity in the central zone of some Proterozoic stromatolites (13). Here, we explicitly link the photosynthetic production of oxygen to the deformed laminae commonly observed in the central zones of Proterozoic conical stromatolites (12, 13, 20, 21). Cyanobacteria were thus involved in the formation of some Fig. 3. Some of the oldest conical stromatolites with possible bubble-like features in the central zone. (A) Central zone of a conical stromatolite from well-preserved Paleoproterozoic and Mesoproterozoic cones as Lime Acres Formation at Lime Acres, Griqualand, South Africa (2.52–2.55 Ga) well as some much younger Neoproterozoic conical stromato- (21) (Scale bar, 2 mm.) (B) Small diapirs surrounded by contorted laminae at lites (22). Intriguingly, features consistent with fossil bubbles and the crests of a conical stromatolite from the Meentheena Member of the contorted laminae in the crestal zone may be present in rare Tumbiana Formation, Australia (Ϸ2.7 Ga) (25).

Bosak et al. PNAS ͉ July 7, 2009 ͉ vol. 106 ͉ no. 27 ͉ 10941 Downloaded by guest on October 4, 2021 Materials and Methods diameter tip with a guard cathode (32) at an irradiance of 180 ␮E/m2/s. The Culturing Media and Growth Conditions. Cone-forming cyanobacteria from microsensors were calibrated at the experimental temperature (45 °C) and Yellowstone National Park were obtained under the permit number YELL- salinity. Diffusive flux of oxygen was calculated by using Fick’s first law of 2008-SCI-5758 from National Park Services. Two cyanobacterial clones domi- 1-dimensional diffusion and steady-state profile of oxygen (33). nate the 16s rDNA clone libraries from our enrichment cultures. One of these ϭ sequences (GenBank accession no. FJ933259) is 99% similar to a sequence Jz DedCz/dz found in cone-forming mats in Yellowstone National Park (29), whereas the where D is an effective diffusion coefficient and dC /dz is the slope of the other one is 97% similar to a sequence reported from mats growing at e z microprofile at depth z. D in the bacterial colony was assumed to be 1.6 ϫ 50–55 °C in Yellowstone (30). The cultures were grown on solid substrate e 10Ϫ5 cm2/s (34). Therefore, the net photosynthetic rate in a specific layer can (agar, silica sand, or aragonite sand) at 45 °C in modified Castenholz D medium Ϫ be determined from the balance between oxygen fluxes through the overly- (31) containing lower concentration of nitrate and phosphate (2.3 mM NO3 Ϫ ing and underlying areas. and 0.8 mM PO3 , respectively) at pH 8. The medium was initially in equilib- 4 Gross photosynthetic rate was measured by using the same sensor and the rium with an atmosphere of 5% CO ,5%H, and 90% N , although cone- 2 2 2 light–dark shift method (35). In the steady state, the photosynthetic oxygen forming cultures grow well even in the medium equilibrated with air. The production is equal to the loss of oxygen due to respiration and to diffusion. cultures were grown at various distances from a fluorescent cold light source After the termination of illumination, the photosynthesis stops instanta- with a 12-h day–12-h night cycle, and the medium was exchanged periodically neously, whereas diffusion and respiration are initially unchanged. This as- (every week). Lithification in the medium was promoted by lowering phos- sumption should be valid as long as the decrease in oxygen concentration is ␮ Ϫ phate concentration to 80 M and 0.23 mM NO3 and increasing calcium and linear with time (36). We measured the decrease in oxygen concentration magnesium concentration to 3.5 mM and 4 mM, respectively, by the addition within 5 s after the darkening and calculated the oxygen uptake (respiration) of CaCl2 and MgCl2. The initial pH of the lithifying medium was 7.6, and sterile rates from the difference between the net and gross photosynthetic rates. medium prepared in this manner did not contain visible precipitates. Supporting Information. For more information, see SI Text. Microscopy. Samples were removed from actively growing cultures by a sterile surgical blade, fixed with 2.5% glutaraldehyde dissolved in 0.1 M sodium ACKNOWLEDGMENTS. A. Maloof (Princeton University) and S. Ono (Massa- cacodylate (pH 7.4) for 2 h. After the fixative was washed away, the samples chusetts Institute of Technology) provided the samples of Proterozoic and were embedded in Sakura TissueTek O.C.T. compound (VWR), frozen for at Archean conical stromatolites; A. Theriault and J. Dougherty enabled the least 2 h, and sectioned to a thickness of 30–50 ␮matϪ20 °C by using a analysis of the Geological Survey of Canada samples; G. Geesey and S. Gunther cryostat (Leica). O.C.T. was washed away by 0.1 M sodium cacodylate buffer assisted with field work in Yellowstone National Park; S.-H.D. Shim and G. and imaged by using epifluorescence, differential interference contrast and Brent helped with Raman spectroscopy; D. Rothman, H. Hofmann, S. Golubic, phase contrast modules on an Axio Imager M1 epifluorescence microscopy B. Weiss, J. Kirschvink, V. Sergeev, 3 anonymous reviewers, and members of the Massachusetts Institute of Technology Laboratory for Geomicrobiology (Zeiss). and Microbial Sedimentology provided useful comments; T. Grove (Massa- chusetts Institue of Technology) and S. Bowring (Massachusetts Institute of Measurement of Oxygen Profiles and Photosynthetic Rate. Oxygen concentra- Technology) provided the rock saw and the petrographic microscopes; and J. tion was determined by using a Clark-type oxygen microsensor with a 25-␮m- Barr generously assisted with the cutting.

1. Buick R (1992) The antiquity of oxygenic photosynthesis: Evidence from stromatolites 19. Harada N, Nishiyama M, Matsumoto S (2001) Inhibition of methanogens increases in sulphate-deficient Archaean lakes. Science 255:74–77. photo-dependent nitrogenase activities in anoxic paddy soil amended with rice straw. 2. Brocks JJ, Buick R, Summons RE, Logan GA (2003) A reconstruction of Archean biolog- FEMS Microbiol Ecol 35:231–238. ical diversity based on molecular fossils from the 2.78 to 2.45 billion-year-old Mount 20. Grey K (1994) Stromatolites from the Paleoproterozoic Earaheedy Group, Earaheady Bruce Supergroup, Hamersley Basin, Western Australia. Geochim Cosmochim Acta Basin, Western Australia. Alcheringa 18:187–218. 67:4321–4335. 21. Grey K (1984) Biostratigraphic Studies of Stromatolites from the Proterozoic Eara- 3. Kopp RE, Kirschvink JL, Hilburn IA, Nash CZ (2005) The paleoproterozoic snowball heedy Group, Naberru Basin, Western Australia (Geological Survey of Western Aus- Earth: A climate disaster triggered by the evolution of oxygenic photosynthesis. Proc tralia, Perth, Australia). Natl Acad Sci USA 102:11131–11136. 22. Schopf JW, Sovietov YK (1976) Microfossils in Conophyton from the Soviet Union and 4. Rasmussen B, Fletcher IR, Brocks JJ, Kilburn MR (2008) Reassessing the first appearance their bearing on Precambrian biostratigraphy. Science 193:143–146. of eukaryotes and cyanobacteria. Nature 455:1101–1104. 23. Hofmann HJ, Masson M (1994) Archean stromatolites from Abitibi greenstone belt, 5. Waldbauer JR, Sherman LS, Sumner DY, Summons RE (2009) Late Archean molecular Quebec, Canada. Geol Soc Am Bull 106:424–429. fossils from the Transvaal Supergroup record the antiquity of microbial diversity and 24. Hofmann HJ, Sage RP, Berdusco EN (1991) Archean stromatolites in Michipicoten aerobiosis. Precambrian Res 169:28–47. Group siderite ore at Wawa, Ontario. Econ Geol 86:1023–1030. 6. Eigenbrode JL, Freeman K, Summons RE (2008) Methylhopane biomarker hydrocar- 25. Van Kranendonk MJ, Philippot P, Lepot K (2006) The Pilbara Drilling Project: c. 2.72 Ga bons in Hamersley Province sediments provide evidence for Neoarchean aerobiosis. Tumbiana Formation and c. 3.49 Ga Dresser Formation Pilbara Craton, Western Earth Planet Sci Lett 273:323–331. Australia (Geological Survey of Western Australia, Perth, Australia). 7. Eigenbrode JL, Freeman KH (2006) Late Archean rise of aerobic microbial ecosystems. 26. Beukes NJ (1987) Facies relations, depositional environments and diagenesis in a major Proc Natl Acad Sci USA 103:15759–15764. early Proterozoic stromatolitic carbonate platform to basinal sequence, Campbellrand 8. Farquhar J, Bao HM, Thiemens M (2000) Atmospheric influence of Earth’s earliest sulfur subgroup, Transvaal Supergroup, Southern Africa. Sediment Geol 54:1–46. cycle. Science 289:756–758. 27. Altermann W (2008) Accretion, Trapping and binding of sediment in Archean stroma- 9. Allwood AC, Walter MR, Kamber BS, Marshall CP, Burch IW (2006) Stromatolite reef tolites—Morphological expression of the antiquity of life. Space Sci Rev 135:55–79. from the Early Archaean era of Australia. Nature 441:714–718. 28. Hofmann HJ (2000) in Microbial Sediments, eds Riding RE, Awramik SM (Springer, 10. Walter MR, Bauld J, Brock TD (1976) in Stromatolites, ed Walter MR (Elsevier, Amster- Berlin), pp 315–327. dam), pp 273–310. 29. Lau E, Nash CZ, Vogler DR, Cullings KW (2005) Molecular diversity of cyanobacteria 11. Batchelor MT, Burne RV, Henry BI, Jackson MJ (2004) A case for biotic morphogenesis inhabiting coniform structures and surrounding mat in a Yellowstone hot spring. of coniform stromatolites. Physica A 337:319–326. Astrobiology 5:83–92. 12. Komar A, Raaben ME, Semikhatov MA (1965) in Trudy Geol Inst Acad Sci USSR 30. Weller R, Bateson MM, Heimbuch BK, Kopczynski ED, Ward DM (1992) Uncultivated (Leningrad), p 122. cyanobacteria, Chloroflexus-like inhabitants, and spirochete-like inhabitants of a hot 13. Donaldson JA (1976) in Stromatolites, ed Walter MR (Elsevier, Amsterdam), pp 523– spring microbial mat. Appl Environ Microbiol 58:3964–3969. 534. 31. Castenholz RW (1988) in Methods in Enzymology, eds Packer L and Glazer AN (Aca- 14. Jones B, Renaut RW, Rosen MR (1998) Microbial biofacies in hot-spring sinters: A model demic, San Diego), pp 68–93. based on Ohaaki Pool, North Island, New Zealand. J Sediment Res 68:413–434. 32. Revsbech NP (1989) An oxygen microsensor with a guard cathode. Limnol Oceanogr 15. Monty CLV (1976) in Stromatolites, ed Walter MR (Elsevier, Amsterdam), pp 193–250. 34:474–478. 16. Ostrovsky I (2003) Methane bubbles in Lake Kinneret: Quantification and temporal and 33. Jorgensen BB, Revsbech NP (1985) Diffusive boundary layers and the oxygen uptake of spatial heterogeneity. Limnol Oceanogr 48:1030–1036. sediments and detritus. Limnol Oceanogr 30:111–120. 17. Campbell KA (2006) Hydrocarbon seep and hydrothermal vent paleoenvironments and 34. Grotzschel S, de Beer D (2002) Effect of oxygen concentration on photosynthesis and paleontology: Past developments and future research directions. Palaeogeogr Palaeo- respiration in two hypersaline microbial mats. Microbial Ecol 44:208–216. climat Palaeoecol 232:362–407. 35. Revsbech NP, Jorgensen BB (1983) Photosynthesis of benthic microflora measured with 18. Shields GA, Veizer J (2002) Precambrian marine carbonate isotope database: Version high spatial resolution by the oxygen microprofile method: Capabilities and limitations 1.1. Geochem Geophys Geosyst 3:1031. of the method. Limnol Oceanogr 28:749–756.

10942 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0900885106 Bosak et al. Downloaded by guest on October 4, 2021 36. Revsbech NP, Jorgensen BB, Brix O (1981) Primary production of microalgae in sedi- 45. Grey K (1981) Small conical stromatolites from the Archean near Kanowna, Western 14 Ϫ ments measured by oxygen microprofile, H CO3 fixation, and oxygen exchange Australia. Annual Report of Geological Survey of Western Australia (Geological Survey methods. Limnol Oceanogr 26:717–730. of Western Australia, Perth, Australia), pp. 90–94. 37. Allwood AC, Walter MR, Burch IW, Kamber BS (2007) 3.43 billion-year-old stromatolite 46. Srinavasan R, Nagvi SM, Kumar BV (1990) Archean shelf-facies and stromatolites reef from the Pilbara Craton of Western Australia: Ecosystem-scale insights to early life proliferation in Dharwar supergoup, North Karnataka, District Karnataka. J Geol Soc on Earth. Precambrian Res 158:198–227. India 35:203–212. 38. Hofmann HJ, Grey K, Hickman AH, Thorpe RI (1999) Origin of 3.45 Ga coniform 47. Walter MR (1983) in Earth’s earliest biosphere, ed Schopf JW (Princeton Univ Press, stromatolites in Warrawoona Group, Western Australia. Geol Soc Am Bull 111:1256– Princeton), pp 187–213. 1262. 48. Abell PI, McClory J, Martin A, Nisbet EG (1985) Archaean stromatolites from the Ngesi 39. Lowe DR (1980) Stromatolites 3,400-Myr old from the Archean of Western Australia. Group, Belingwe greenstone belt, Zimbabwe; Preservation and stable isotopes– Nature 284:441–443. Preliminary results. Precambrian Res 27:357–383. 40. Beukes NJ, Lowe DR (1989) Environmental control on diverse stromatolite morpholo- 49. Lambert MA (1998) Stromatolites of the late Archean Back River stratovolcano, Slave gies in the 3000 Myr Pongola Supergroup, South Africa. Sedimentology 36:383–397. structural province, Northwest Territories, Canada. Can J Earth Sci 35:290–301. 41. Hofmann HJ, Thurston PC, Wallace H (1985) in Evolution of Archean Supracrustal 50. Murphy MA, Sumner DY (2008) Variations in Neoarchean microbialite morphologies: Clues to Sequences, Special Paper, eds Ayres LD, Thurston PC, Card KD, Weber W (Geological controls on microbialite morphologies through time. Sedimentology 55:1189–1202. Association of Canada, Ottawa), pp 125–132. 51. Buck SG (1980) Stromatolite and ooid deposits within the fluvial and lacustrine sediments of 42. Wilks ME, Nisbet EG (1985) Archaean stromatolites from the Steep Rock Group, the Precambrian Ventersdorp Supergroup of South Africa. Precambrian Res 12:311–330. northwestern Ontario, Canada. Can J Earth Sci 22:792–799. 52. Schopf JW (2006) Fossil evidence of Archaean life. Phil Trans R Soc London Ser B 43. Donaldson JA, deKemp EA (1998) Archaean quartz arenites in the Canadian Shield: 361:869–885. Examples from the Superior and Churchill Provinces. Sediment Geol 120:153–176. 53. Bertrand-Sarfati J (1972) Columnar stromatolites from the Upper Precambrian from 44. Sakurai Y, Ito M, Ueno Y, Kitajima K, Maruyama S (2005) Facies architecture and Northwest Sahara (Centre de Recherches sur les Zones Arides, Paris), in French. sequence-stratigraphic features of the Tumbiana Formation in the Pilbara Craton, 54. Fairchild IJ, Marshall JD, Bertrand-Sarfati J (1990) Stratigraphic shifts in carbon isotopes northwestern Australia: Implications for depositional environments of oxygenic stro- from Proterozoic stromatolitic carbonates (Mauritania): Influences of primary miner- matolites during the Late Archean. Precambrian Res 138:255–273. alogy and diagenesis. Am J Sci 290-A:46–79. MICROBIOLOGY GEOLOGY

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