The Environmental Importance of Microbial Sulfate Reduction and Disproportionation: Insights from SIMS-Based Δ34s Measurements David A

The Environmental Importance of Microbial Sulfate Reduction and Disproportionation: Insights from SIMS-based δ34S Measurements David A. Fike Washington University, St. Louis, MO 63130, USA

Metabolism

Environment Acknowledgments

SUPPORT: Geobiology time

space Geobiology

Metabolism time

Metabolism Environment

Environment

space Geobiology time

Metabolism

Depositional Conditions Depositional EnvironmentConditions

space Geobiology time Lithification & Diagenesis

Metabolism

Lithification & Depositional Conditions Diagenesis Environment

space Motivation 1) understand modern biogeochemical cycling 2) understand how geochemical signals are preserved 3) paleoenvironmental reconstruction 2 2

Metabolism 1 3 Environment The Utility of Stable Isotopes 1) metabolic activity generates large isotopic fractionations • which depend upon environmental & ecological conditions 2) isotopic composition of sedimentary phases: best record of ancient biogeochemical cycling over Earth history. S isotopes: 32S: 95.02%; 33S: 0.76%; 34S: 4.20%; 36S: 0.02%

Canonically measure 34S/32S ratio: 34 34 32 34 32 3 δ S = [( S/ S)sample/( S/ S)std-1]*10 , ‰ (V-CDT) Sulfate reduction

What is it? (S6+→S2-) • Microbial reduction of sulfate to sulfide coupled to oxidation of H2 or organic C

2- + - SO4 + 4H2 + H → HS + 4H2O or 2- - - + SO4 + 2CH2O → HS + 2HCO3 + H

Why do we care? • Dominant pathway for organic C remineralization in modern marine sediments • impacts global carbon cycling • Inferred to be among oldest metabolic pathways • Isotopic evidence(?) at ca 3.5 Gyr Fractionation during sulfate reduction

Controlled by: • sulfate reduction rate - sulfate concentrations - electron donor concentrations

Additional factors: • electron donor • H2 vs. Corg • temperature • microbial species

Sim et al. 2011 Sulfur cycling: Not just sulfate reduction

Sulfate Reduction 2- + -

SO4 + 4H2 + H → HS + 4H2O

~0 Sulfide Oxidation ‰

- 2- + ‰?

HS + 2O2 → SO4 + H ~25-50

Sulfur Disproportionation* 0 2- - + 4S + 4H2O → SO4 + 3HS + 5H

2- 2- *SO3 or S2O3 can also be used Environmental δ34S fractionation: impact of disproportionation

Canfield & Teske, 1996 Sulfur Isotopes Over Earth History

80 34 1) Increase in depletion of δ Spyrite w/ time 60 34 34 2) Occasional δ Spyrite > δ Ssulfate

) 20 Sulfate ‰ S ( 34 δ 0

-20 Pyrite -40

-60 0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 Time (Ga) Vignettes

1) Nature of Environment-Microbe Feedbacks at the Chemocline (Oxic-Anoxic Interface) • Modern Microbial Mats

2) How Depositional Environment Impacts Signals Preserved in Sediments • Modern Shallow Marine Sediments Modern Microbial Mats Simple community structure Guerrero Negro, Baja California, Mexico • lack macrofauna

• lack bioturbation mm • lack detrital input VIS • essentially 1D systems

Complex spatial organization • Phylogenetically diverse • Metabolically diverse

• Intense metabolic coupling: Sulfide Image: N. Pace • photosynthesis/respiration • sulfate reduction/sulfide oxidation Sulfate Reducers Amidst Cyanobacteria

Fike et al. GCA 2009 A New Approach…

Spatial complexity of microbial mats: • metabolism 7f-GEO instrument • phylogeny • substrate availability

Need means to capture spatial diversity in isotopes: Secondary Ion Mass Spectrometry (SIMS) Instrument Schematic

Cs+ source

secondary ions collectors collectors

sample 1: Modern microbial mats: Guerrero Negro Microbial Mat Cross Section Quantifying active sulfate reduction: 35 2- SO4 radiolabel

Cross section of Radiograph of 35 active stromatolite S-labeled Ag2S

Visscher et al. 2000 Incubation of silver disk in a microbial mat 2D Analysis Improved Spatial Resolution

1 10 0 Max. -1 0 Vertical -2 sampling -3 -10 resolution -4 -20 -5 Depth (mm) -6 -30 -7 1 cm -8 -40 Typical lateral sample size -9 0.9 mm Photosynthetic Redox Forcing Photosynthetic Impact on δ34S?

! Absolute value and profile of δ34S indep. of photosynthesis ! Enrichment in δ34S toward chemocline -where disproportionation would be expected to occur Sippewissett Salt Marsh Pink Berry consortia: purple S bacteria & sulfate reducing bacteria

Wilbanks et al. 2014 Sippewissett Salt Marsh Pink Berry consortia: purple S bacteria & sulfate reducing bacteria

wire sulfide deposition

! Enrichment in δ34S toward chemocline Wilbanks et al. 2014 -where disproportionation would be expected to occur Environmental δ34S fractionation: disproportionation? csSRR?

Canfield & Teske, 1996 2 . Modern Depositional 34 Environments & δ Spyrite Papua New Guinea 144E Kikori River 145E 146E

Turama River Purari River Australia

Bamu River GH-8 GH-14 8S GS-48

GH-50 G SE Trades 25 km H NW Fly T8-18 Monsoon River

0 9S 20 50 40

Depth (m) 80 G H 0 20 40 60 80 Distance ofshore (km) 34 Depositional Environment & δ Spyrite 0

2 shallowing

4 Water Depth 8 m 14 m sediment depth (m) sediment sediment depth (m) sediment 6 18 m 48 m 50 m seawater sulfate seawater 8 sulfate seawater -40 -30 -20 -10 0 10 20 30 40 δ34Spyr (‰) [V-CDT] 34 Depositional Environment & δ Spyrite

0 Deeper water 34 • Highly negative δ Spyr shallowing 2 • Large fractionations • Low stratigraphic variability 4 Water Depth 8 m Shallow water 14 m

sediment depth (m) sediment 6 18 m • Generally positive 48 m 34 50 m δ Spyr 8 sulfate seawater • Small (even negative!) -40 -30 -20 -10 0 10 20 30 40 δ34Spyr (‰) [V-CDT] fractionations • High stratigraphic

variability Oxidative Reworking Mechanism(?) seaseasea levellevellevel reworkingreworking eventevent sedimentsedimentsediment surfacesurfacesurface

oxicoxicoxic OOO222/H/H/H222OOO --- NONONO333/N/N/N222 4+4+4+ 2+2+2+

suboxic depth suboxicsuboxicsuboxic MnMnMn /Mn/Mn/Mn depth depth depth sediment sediment FeFeFe3+3+3+/Fe/Fe/Fe2+2+2+ sediment sediment sediment remobilized remobilized remobilized partialpartial HH2SS remobilized oxidationoxidation22 Fe-sulfde formation anoxic anoxic anoxic anoxic sulsulsulfffdicdicdic 3434 2-2-2- increasedincreased increasedincreased δ S SO /H S 3434 pyrpyr SOSOSO444 /H/H/H222SSS δδ SSH2SH2S methanicmethanicmethanic COCOCO222/CH/CH/CH444 tt 00 timetime

Aller et al. 2010 Imagined Impact across a Depositional Gradient

sea level

sediment surface

O2/H2O 0 NO -/N 3 2 4+ Mn /Mn 2+ 2 shallowing 3+ Fe /Fe2+ LEGEND SO 2-/H 4 magnitude of 4 2S CO /CH recycling fux 2 4 depth below depth below 6 water depth 14 m sediment surfacesediment (m)

seawater sulfate seawater 50 m -40 -30 -20 -10 0 10 20 30 34 δ Spyr (‰) Wild Extrapolation t3 δ34S isotopic gradient LEGEND magnitude of recycling fux Facies topset deposits foreset deposits bottomset deposits

34 δ S isotopic range

-30 -20 -10 0 10 20 δ34S t3 Highstand 34 δ S (‰) TST MFS

-30 -20 -10 0 10 20 t2 Lowstand

LST

-30 -20 -10 0 10 20 t1 Highstand sea level

HST

-30 -20 -10 0 10 20 Preliminary Observations

Spatial δ34S variability pervasive in modern/ ancient microbial/sedimentary systems: • No isotopic evidence for widespread disproportionation across oxic-anoxic transition • Physical reworking and oxidation likely play key 34 role in generating elevated δ Spyrite records Modern studies provide key insights into interpreting ancient isotopic records. • Essential to incorporate depositional environment and stratigraphic context into interpretations Looking forward: Much to be done to understand the long-term S isotopic record 80

60 Thank you very much for your attention!

) 20 Sulfate ‰ S ( 34 δ 0

-20 Pyrite -40

-60 0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 Time (Ga)