Grain Trapping by Microbial Mats: Implications for Stromatolites

Grain trapping by microbial mats: Implications for stromatolites

Frank Corsetti Department of Earth Sciences University of Southern California Rocks = Time Rocks = Environment Rocks = History of Life Stromatolite

sharkbay.org Stromatolite Textbook Definition

• laminated

• organo-sedimentary structure

• built by microbes (CCALA)

Cyanobacteria Cyanobacteria

microbial mat (“pond scum”) Stromatolite Textbook Definition

Trapping and Binding

100 microns Stromatolite courtesy of Y. Ibarra Textbook Definition

Mineral Precipitation

Stromatolite Signiﬁcance

• Macroscopic from Microscopic Stromatolite Signiﬁcance putative • Oldest fossils in the world ^ Warrawoona Fm Western Australia 3.5 Ga

2 cm Ancient Life: Greatest Hits

Cambrian explosion

Hadean Archean Proterozoic Phan. 4.0 3.0 2.0 1.0 0 billions of years LETTERS NATURE | Vol 457 | 5 February 2009

Masirah Bay Fm. soft-body parts, as detected in Doushantuo phosphorites19,22, is rare in ααα S ααα R

αββ the geological record. Siliceous sponge spicules are metastable and C (17%) they can be difficult to isolate and identify unambiguously in clastic 26 sediments. Moreover, several orders of Demospongiae completely *** * 358 → 217 lack mineral skeletons. On the other hand, the studies of the lipid ααα R

ααα S compositions of Porifera show a remarkable diversity of distinctive αββ C (21%) 27 structures with abundance patterns aligned to phylogeny13,27,28 372 → 217 The demosponge biomarker record for the Huqf Supergroup supports the hypothesis that Metazoa first achieved ecological 1 αββ ααα S ααα R prominence in shallow marine waters of the Cryogenian . It has been C28 (16%) 386 → 217 proposed that Neoproterozoic sponges and rangeomorphs feeding on reactive dissolved or particulate marine organic matter29 may have progressively oxygenated their benthic environments as they moved ααα R ααα S

αββ 24 C29 (39%) from shallow water into deeper waters . Consistent with this, our 400 → 217 data (Table 1 and Suplementary Table 1) show that, on average, C30 Signal intensity (a.u.) steranes comprised 2.7% of total C27–C30 extractable steranes in Huqf samples and 63% of the summed C30 compounds were 24- C30 (5%) (24-i/24-n) = 1.35 ++ isopropylcholestanes, suggesting that demosponges must have made ° ° + + 414 → 217 ° a significant contribution to preserved sedimentary organic matter and, therefore, environmental biomass24. In contrast, lack of significant sponge steranes in deepwater shales from the Ediacaran Rodda Bed Formation in the Officer basin, Australia15, and from the late Cryogenian Aralka Formation (Supplementary Information) sug- Ghadir Manquil Fm.

ααα S gests that it took longer to colonize deepwater environments. ααα R αββ Neoproterozoic sponges would have been at least partly responsible for the ultimate respiration and removal of dissolved organic C26 (9%) ** 24,29 * * (*) 358 → 217 carbon , aiding ventilation of the global ocean and shifts in the

ααα R modes of carbon and sulphur cycling evident from Ediacaran iso- αββ ααα S topic and geochemical records3,30. C27 (17%) 372 → 217 METHODS SUMMARY

αββ Solvent-rinsed core rock fragments and cuttings were crushed to a fine powder ααα R ααα S C28 (12%) using an alumina ceramic puck mill housed in a SPEX 8510 shatterbox. Rock 386 → 217 powders were extracted with a mixture of dichloromethane and methanol (9:1, v/v) using a Dionex Accelerator Solvent Extractor ASE-200 operated under αββ ααα R ααα S 1,000 p.s.i. at 100 uC. Asphaltenes were precipitated from the resulting organic C (55%) 29 extracts (bitumens) using n-pentane. The maltenes (n-pentane solubles) were

Signal intensity (a.u.) Ancient Life: Greatest 400Hits → 217 then fractionated by silica gel adsorption chromatography, eluting successively with hexane, hexane/CH2Cl2 (v/v: 4:1) and CH2Cl2/CH3OH (v/v: 3:1) to yield saturated hydrocarbons, aromatic hydrocarbons and resin fractions, respectively. C (7%) 30 Continuous-flow hydropyrolysis experiments were conducted on 100– 414 → 217 (+) 2,000 mg of catalyst-loaded pre-extracted sediments or kerogen concentrates (24-i/24-n) = 1.31 + + + as described previously7 ° ° °+ . Hydropyrolysates were fractionated on silica gel col- umns, as for rock bitumens. GC-MS analyses of saturated hydrocarbon fractions were performed on a Love et al., 2009 Retention time (min) Micromass AutoSpec Ultima equipped with a HP6890 gas chromatograph and Figure 2 MRM GC-MS ion chromatograms of C –C desmethylsteranes a DB-1MS coated capillary column (60 m 3 0.25 mm i.d., 0.25-mm film thick- | 26Sponge30 Biomarkers released from catalytic hydropyrolysis of a Masirah(Oldest Bay Formation Animal) (JF-1) ness) using He as carrier gas. Hopane and sterane biomarkers were analysed by and a Ghadir Manquil Formation (GM-1) kerogen. For each sterane carbon MRM GC-MS with a total cycle time of 1.3 s per scan for 26 transitions, including number,Hadean four diastereoisomersArchean are detectedProterozoic (aaa20R, abb20R,Phan.abb20S, the m/z 414 to 217 transition for C30 desmethylsteranes. The GC oven was 21 aaa20R), indicating4.0 a mature3.0 geoisomer2.0 distribution.1.0 Demosponge 0 programmed at 60 uC (2 min), heated to 150 uCat10uC min , further heated contributions are evident from abundantbillions of years 24-isopropylcholestanes (‘plus’ to 315 uCat3uC min21 and held at final temperature for 24 min. signs). 24-n-propylcholestanes (open circles) are markers of marine 50 ng of deuterated C29 sterane standard [d4-aaa-24-ethylcholestane (20R)] pelagophyte algae and this confirms a marine depositional setting for each was typically added to 1 mg saturates to quantify the polycyclic biomarker con- formation in the SOSB. Stars mark a series of 27-norcholestanes. At right, tent. Yields assume equal mass spectral response factors between analytes. values in parentheses represent a measure of relative signal intensity for the Analytical errors for individual hopanes and steranes concentrations are esti- C26–C30 steranes in acquired MRM chromatograms (though absolute mated at 630%. Average uncertainties in hopane and sterane biomarker ratios abundances are determined from individual peak areas) and the numbers are 68% as calculated from multiple analyses of a saturated hydrocarbon frac- beneath are the masses (in daltons) of the ion transitions (molecular weight tion from an AGSO standard oil (n 5 30). R fragment ion) used in MRM GC-MS in each case. y axis, signal intensity; x axis, retention time in min (52 to 68 min shown for all traces). Full Methods and any associated references are available in the online version of the paper at www.nature.com/nature. biomarker appearance corresponds well to divergence estimates for Received 23 September; accepted 27 November 2008. the last common ancestor of all living demosponges obtained from molecular clocks25,26, and indeed can now be used to more robustly 1. Peterson, K. J., Cotton, J. A., Gehling, J. G. & Pisani, D. The Ediacaran emergence of calibrate the molecular clock at the base of the animal tree1. bilaterians: Congruence between the genetic and the geological fossil records. Phil. Trans. R. Soc. B 363, 1435–1443 (2008). The use of recalcitrant lipid biomarkers offers a promising 2. Bowring, S. A. et al. Geochronologic constraints on the chronostratigraphic approach for tracking the earliest sponge contributions to framework of the Neoproterozoic Huqf Supergroup, Sultanate of Oman. Am. J. Sci. Precambrian sedimentary rocks because outstanding preservation of 307, 1097–1145 (2007). 720 ©2009 Macmillan Publishers Limited. All rights reserved Ancient Life: Greatest Hits Grypania

Oldest putative eukaryote

Hadean Archean Proterozoic Phan. 4.0 3.0 2.0 1.0 0 billions of years 244 Ancient Life:K. SugitaniGreatest et al. / Precambrian Hits Research 158 (2007) 228–262

20 microns Sugitani et al., 2007 Oldest putative microfossils

Hadean Archean Proterozoic Phan. 4.0 3.0 2.0 1.0 0 billions of years

Fig. 11. Photomicrographs of spheroidal microstructures. Scale bar: 20 ␮m (a, c–n); 10 ␮m (b). (a), (b) and (l–n) from Mount Grant and others from Mount Goldsworthy. Also see Supplementary Fig. III.(a)Colony-likeaggregationofsmallspheroidalmicrostructures.SlideNORW1,Position L-J50/2. (b) Magniﬁcation of (a). I, Nearly completely hollow sphere; II, distorted sphere; III, ruptured sphere; IV, cluster of opaque particles. (c) and (d) Polar and equatorial views of a large hollow spheroidal microstructures. Arrow shows the deepening focal depths. Slide GWM11A-sub2, Position L-R35. (e) Hollow spheroidal microstructures. Slide GWM11A-sub1, Position L-S46/4. (f–h) Views of hollow spheroidal microstructures with possible inner spheroidal object. The arrow shows the deepening focal depths. Slide NGWM1X, Position R-N40/1. (i) Slightly distorted hollow spheroidal microstructures with partially wrinkled wall. Slide NGWM3, Position R-L37/3. (j) Broken? spheroidal microstructure. Slide NGWM1X, Position R-F40/1. (k) Non-hollow spheroidal microstructure. Slide GWM11A-EX1, Position L-E38/3. (l and m) Distorted spheroid. Slide NORW1X-1’, Position L-O59. (n) Semi-hollow spheroid with partly broken left margin. Slide GFWE3-1, Position L-O61. Ancient Life: Greatest Hits

OMin OR Oldest “Uncontroversial” Stromatolite

Hadean Archean Proterozoic Phan. 4.0 3.0 2.0 1.0 0 billions of years Pondering Geologic Time

The rest of Geologic Time (~886 more sheets) A Microbial World!

Hadean Archean Proterozoic Phan. 4.0 3.0 2.0 1.0 0 billions of years Us

1 million years

2 million years Lucy

3 million years

4 million years

Hadean Archean Proterozoic Phan. 4.0 3.0 2.0 1.0 0 billions of years Modern stromatolites as analogues for ancient stromatolites?

Grain size >250 µm

4 cm

Bahamas Shark Bay Modern Modern Grain-Size Conundrum Stromatolite grain size through time

coarse-grained stromatolitescoarse-grained & thrombolites stromatolites Stromatolite grain size through time fine-grained stromatolites & thrombolites

coarse-grained stromatolites & thrombolites ArcheanStromatolite grain sizeProterozoic through time Phan. 3.5 2.5 1.5 0.5 fine-grainedbillions stromatolites of years & thrombolites coarse-grained stromatolites & thrombolites Archean Proterozoic Phan. 3.5 fine-grained2.5 stromatolites &1.5 thrombolites 0.5 billions of years Archean Proterozoic Phan. 3.5 1 mm 2.5 1.51 mm after Awramik and Riding0.5 (1988) 1 mm billions of years after Riding, 2011

1 mm 1 mm after Awramik and Riding (1988) 1 mm

1 mm 1 mm after Awramik and Riding (1988) 1 mm Stromatolite Conundrums

P1: APR/SAT/spd P2: NBL/plb QC: NBL/anil T1: NBL March 26, 1999 14:40 Annual Reviews AR081-10

• Grain-size conundrum: PRECAMBRIAN STROMATOLITES 333 –Are modern examples good analogues? –What is the conundrum trying to tell us?

P1: APR/SAT/spd P2: NBL/plb QC: NBL/anil T1: NBL March 26, 1999 14:40 Annual Reviews AR081-10

• Life conundrum: PRECAMBRIAN STROMATOLITES 333 –How can we tell “real” from “fake”

• Experiments! Figure 7 Stromatolites with similar shape but different origins. (a) Modern domal to columnar stromatolites from Shark Bay, Western Australia. Scale bar is 40 cm. (b) Stromatolites are formed by trapping, binding, and early lithiﬁcation of loose carbonate sediment to form crude lamination. Knife is 7.5 cm long. (c) Domal stromatolites preserved in Neoarchean Campbellrand Subgroup, South Africa. Hammer is 35 cm long. (d ) Stromatolites are formed by growth of crystal fans that trap sediment as it settles into the interstices of growing crystals. This produces a faint but relatively ﬁne lamination along which preferential weathering has exposed domal shapes whose radii of curvature correspond to that of each radiating crystal fan. Scale bar is 20 cm.

Figure 7 Stromatolites withvariations similar shape but in different stromatolite origins. ( form.a) Modern As domal Hofmann to columnar (1987) stated, “...we still have no stromatolites from Shark Bay, Western Australia. Scale bar is 40 cm. (b) Stromatolites are formed by trapping, binding, and earlystromatolite lithification of loose theory, carbonate no sediment model to that form showscrude lamination. which attributes changed in what way Knife is 7.5 cm long. (c) Domalthrough stromatolites time.” preserved Without in Neoarchean a viable Campbellrand theory Subgroup,we are always at risk of misinterpreting South Africa. Hammer is 35 cm long. (d ) Stromatolites are formed by growth of crystal fans that trap sediment as it settlesthe into thegenetic interstices significance of growing crystals. of growth This produces form. a faint This but is well illustrated in Figure 7, relatively fine lamination alongwhere which preferential it is obvious weathering that hasthe exposed present domal is not shapes the whose key to the past—modern domal and radii of curvature correspond tocolumnar that of each radiating structures crystal formed fan. Scale barby is microbial 20 cm. mats (Figure 7a,7b) are mimicked by Neoarchean domal structures formed by radiating crystal fans of calcitized variations in stromatolitearagonite form. As Hofmann (Figure (1987) 7c,7d stated,). Clearly, “...we still two have very no different sets of processes have stromatolite theory, no modelacted that over shows time which to produce attributes changed nearly identical in what way structures. What is missing is a through time.” Without amodel viable theoryin which we are lamina-scale always at risk morphology of misinterpreting can be related to macromorphology the genetic significance of growth form. This is well illustrated in Figure 7, where it is obvious that thethrough present iterationis not the key of to specific the past—modern biological, domal physical, and and chemical processes. columnar structures formed by microbial mats (Figure 7a,7b) are mimicked by Neoarchean domal structures formed by radiating crystal fans of calcitized aragonite (Figure 7c,7d ). Clearly, two very different sets of processes have acted over time to produce nearly identical structures. What is missing is a model in which lamina-scale morphology can be related to macromorphology through iteration of specific biological, physical, and chemical processes. ISSN 1472-4669 · September 2015 · Volume 13 · Issue 5 www.geobiol.com

Cyanobacteria can hold on if it’s not too steep Dr. Carie Frantz Weber State U, Utah

Dr. Vicky Petryshyn USC

ggbi_13_5_ofc.inddbi_13_5_ofc.indd 1 77/23/2015/23/2015 111:34:451:34:45 AAMM

“Microcoleus” (cyanobacterium) CCALA Fresh mats: No visible filament protrusion

Developed mats: filaments ~1 mm

Mature mats: filaments >2 mm Grain size Fine: 0.125-0.250 mm

Medium: 0.50-1.0 mm

Coarse: 1.0-2.0 mm Mat angles: 0°, 15°, 30°,45°, 60°, 75° Trapping vs. Binding

Trapped Bound

Cyano Grain Trapping glassFine Grainsfine grain 1.0

0.5 Fraction of grains trapped 0 0 15 30 45 60 75 Incline angle (degrees) Cyano Grain Trapping

Fine Grains Medium Grains Coarse Grains 1.0

0.5 Fraction of

grains trapped 0 0 15 30 45 60 75 0 15 30 45 60 75 0 15 30 45 60 75

1.0

0.5 Fraction of

grains trapped 0 0 15 30 45 60 75 0 15 30 45 60 75 0 15 30 45 60 75 Incline angle (degrees) Fraction of grains trapped 0.0 0.5 1.0 Cyano 0 incline angle(degrees) GrainBinding bound after 12hours bound immediately trapped immediately 15 medium grains 30 45 15° medium grain 180x

500 um Cyano Results Summary

• Trapping – Size matters – mat development – Good at Fine – OK/Bad at Medium – Bad at Coarse

• If grains are trapped, Microcoleus will bind Implications

• Large grains trapped beyond the angle of slide constitute a biosignature.

5 mm Coarse-grained stromatolites? Filamentous algal mat Chaetomorpha linum Fine Grains Medium Grains Coarse Grains 1.0

0.5 Filamentous algal mat Fraction of

grains trapped 0 Trapping 0 15 30 45 60 75 0 15 30 45 60 75 0 15 30 45 60 75 Fine Grains Medium Grains Coarse Grains 1.0

0.5 Fraction of Fraction of

grains trapped 0 grains trapped 0 15 30 45 60 75 0 15 30 45 60 75 0 15 30 45 60 75 Incline angle (degrees) Cyano mat Fine Grains TrappingMedium Grains Coarse Grains 1.0

0.5 Fraction of

grains trapped 0 0 15 30 45 60 75 0 15 30 45 60 75 0 15 30 45 60 75

1.0

0.5 Fraction of

grains trapped 0 0 15 30 45 60 75 0 15 30 45 60 75 0 15 30 45 60 75 Incline angle (degrees) Fraction of grains trapped 0.0 0.5 1.0

incline angle(degrees) Fraction of

bound after12 hours bound immediately trapped immediately grains trapped 0.0 0.5 1.0 0 algal mat binding incline angle(degrees) 45 incline angle(degrees) bound after12 hours bound immediately trapped immediately Fraction of 15 bound after12 hours bound immediately trapped immediately grains trapped 0.0 0.5 1.0 medium grains 30 45 cyano mat binding 45 Algal Results Summary

• This one good at trapping

• Bad at binding

800 µm Implications for the rock record

poorly-developed developed mixed community cyanobacterial mat cyanobacterial mat cyanobacteria + algae

fine grains medium grains coarse grains poorly-developed developed mixed community cyanobacterial mat cyanobacterial mat cyanobacteria + algae

fine grains medium grains coarse grains

Bitter Springs Formation ~800 million years poorly-developed developed mixed community cyanobacterial mat cyanobacterial mat cyanobacteria + algae fine grains medium grains coarse grains

Gunflint Formation ~1.9 billion years

5 mm poorly-developed developed mixed community cyanobacterial mat cyanobacterial mat cyanobacteria + algae fine grains medium grains coarse grains

Shark Bay/Bahamas Modern Conclusions Stromatolite grain size through time

coarse-grained stromatolitescoarse-grained & thrombolites stromatolites Stromatolite grain size through time fine-grained stromatolites & thrombolites

1 mm 1 mm after Awramik and Riding (1988) 1 mm

1 mm 1 mm after Awramik and Riding (1988) 1 mm Conclusions Large grains beyond angle of slide constitute a biosignature

5 mm Collaborators William M. Berelson Victoria Petryshyn • International Dylan Wilmeth Geobiology Olivia Piazza Summer Course (USC)

Carie Frantz • Agouron Institute (Weber State U) • NASA Exobiology John R. Spear (Colorado School of Mines)