Emerging Views of Sediment-Buried Ocean Basement Biosphere

1. Emerging Views of Sediment-Buried Ocean Basement Biosphere James P. Cowen Department of Oceanography University of Hawaii jcowen@soest.hawaii.edu

2. Emerging Views of the Biosphere w/in Aging Ocean Basement • Ocean basement provinces • Biosphere of aging basement • Access—tough • General physical (e.g., fluid flow; temperature) and chemical characteristics • Evidence of extant biosphere • Speculated metabolic pathways • Challenges and future research directions

3. Why do we care? • Ocean basement is a huge volume • Potential for extensive biomass • Basalt to gabbro rocks • Prone to alteration disequilibria • Fluids circulate even in old basement • Thermal, chemical gradients • Potential for exotic metabolisms/strategies • Analogue for extraterrestrial fluid covered, rocky bodies

4. old old Detrick 2004

5. basement ocean crust Ocean crust Karson et al. 2002

6. Zone I: Ridge axis • — active exchange • — high/low temperature venting; • — sharp thermal / redox / chemical gradients

8. Zone II:Unsedimented ridge flank • — active (advective) exchange, low (to high ?) temperature venting • — poorly explored

9. ~165 m Diffuse upwelling Impenetrable • Zone III: Sedimented ridge flanks (a) and basin (b) • —increasing sediment cover; • —hydrologic seal at ~165 m thickness • —conductive heat / diffusive chemical exchange

10. Zone IV: Exposed rocky outcrops (Seamounts) • — Local advective recharge or discharge; • — Natural access to fluids

11. Access to crustal fluids • ODP/IODP Boreholes • - Sediment and basement cores • - Observatories: CORKs (Circulation Obviation retrofit Kits) • * Engineered access to basement rock and fluids

12. 2600 m 2900 m CORK-I Observatory

13. Biological Diversity Biomass Metabolism Activity/survival Consortia Heat(temp) Basement age Spreading rate Sedimentation Geochemical Redox potential Essential elements Water/rock Rock mineralogy Fluid Flow Permeability Porosity Driving energy

14. Reykajanes JdF Ridge flank Lau Basin MAR west flank Costa Rica Rift South flank Global Ocean Basement

15. Basement temperatures(east flank JFR) 0.8 My 3.5 My 0 20 40 60 80 100 120 Distance from ridge axis (km) from Davis et al. 1999 Cowen, in press

16. JFR, CRR 0 1020 30 40 50 60 Crustal Age (Ma) Wheat et al. 2003

17. Ocean Lithospheric Heat Flux • Total: ~32 TW • Hydrothermal circulation to 65 Ma: • ~11 TW • Off-axis (1-65 Ma) heat flux: • ~9.25 TW • Associated Water Flux • Near ridge (0-1 Ma): ~3.7 x 1016 g/yr • Flanks (1-65 Ma): ~0.2-2 x 1019 g/yr • Flank fluid flow = 50-500 X Axial flow Low Temp Cycle entire ocean through flank basement in 70,000 to 700,000 yrs Schultz and Elderfield 1997 Mottl 2004

18. Bulk Permeabilityof Upper Basement • Crustal Age Suggests a decrease In bulk flow w/in aging basement Consistent with seismic velocity (faster in denser, less porous media), but inconsistent with heat flow obs (signif. advective heat loss to 65 My) Fisher (2004)

19. Diffusive flux Rapid channelized Channelized flow Fluid flows: Tortuous advective

20. Borehole 395A: MAR flanks • Zones of deflection in SP log (10-100 m thick) Suggest: Channelized flow modified from Matthews et al. (1984), Becker et al. (1998) measures pressure differences

21. Basement rock/fluid chemistry • Temperature of rocks (e.g., <2 to >100oC) • How much fluid previously passed • History of fluids • Composition of host rock (primary/secondary mineralogy) • age • water : rock ratios • flow rates (i.e., general and local permeability) • microbial activity

22. Basement mineral alteration (bulk basement rock) JdFR flanks Fe2+ (Fe2++Fe3+) Age of basement Distance from ridge axis Marescotti et al 2000

23. Johnson and Semyan 1994, reploted by Bach and Edwards 2003

24. JdFR Increasing (upper) Basement Age Marescotti et al. 2000

25. FeOOH Olivines Pyrite Celadonite/ saponite Alt and Mata 2000 Bach and Edwards 2003 Alteration Halo within Fracture (fluid conduit)

26. O2 reduction NO3- reduction Fe3+ reduction SO42- reduction + H2 oxidation Fe+2 oxidation S oxidation O2,NO3- + FeOOH Celadonite/ saponite Olivines Pyrite H2 Fe2+ O2 Bach and Edwards 2003 Microbial role ? Furnes and Staudigal1999 estimate 75% of upper basement is microbially altered !?

27. in Subseafloor Basement Environments (reduced) organic carbon In situ abiogenic organic carbon Chemoorganotroph (heterotroph) Chemolithoautotroph organic carbon Making a Living Photoautotroph Chemotroph Chemolithoautotrophy: Energy: Oxidation/reduction reactions using inorganic e- donor & e- acceptor pairs C-source: inorganic (CO2)

28. Relevant, microbially meaningful reactions(chemolithoautotrophic) 4FeO + O2 + 6H2O = 4Fe(OH)3,s [5FeO + NO3- + H+ + 7H20 = 5Fe(OH)3,s + 0.5N2] FeS + 2O2 = Fe2+ + SO42- 2 FeO + 4 H2O = 2 Fe(OH)3 + H2 2 FeO + 2 H2O = 2 FeOOH + H2 2 FeO + H2O = Fe2O3 + H2 H2 oxid by O2, NO3-,Fe3+,SO42-, Aerobic Fe2+ oxidation Anaerobic Fe2+ oxidation Sulfide oxidation Low-To, abiogenic anaerobic hydrolysis H2 oxidation

29. Potential metabolic processes active in subseafloor basement Q = activity product? Gr = Gr0 + RT ln(Q)

30. Edwards 2004

31. Fluid Composition EnrichedDepleted Cowen et al. 2003; Wheat et al. in review; M. Lilley, unpubl. data

32. Basement fluid chemistry Depleted Mg2+/ enriched Si, Ca2+, Sr2+, H2 • Reaction with basaltic rocks Enriched H2 • Hydrolysis of ferrous Fe in basalt rocks Depleted sulfate • Sulfate reduction (H2, Org-C) • Diffusion to sediments • Sulfate mineral precipitation (e.g., Jarosite, anhydrite) Elevated ammonia • Nitrate reduction (e.g., e- donor: Org-C, Fe2+, or H2) • N2 fixation • Diffusion from sediments Depleted TCO2, alkalinity • Carbonate precipitation Enriched Si, Fe • Seawater-basalt reactions • Contamination (e.g., drilling ops, borehole casings)

33. Sediments basement Mather and Parkes 2000 Sediment-Basement Exchange:Borehole 1027 (3.5 Mya)

34. Mather and Parkes 2000 Borehole 1027: sediment profiles

35. Inferred Microbial-Produced Alteration Textures BSE-SEM images Lau 3 mbs 4-7 Ma MAR 45 mbs 10 Ma MAR 157 mbs 10 Ma MAR 7 mbs <2 Ma Reykj R 51 mbs 2.3 Ma Reykj R 124 mbs 38 Ma Furnes et al. 2001 mbs: meters below sediments

36. Phase contrast DNA (DAPI) Arch344 Bac388 Phase contrast DNA (DAPI) Bac388 Arch344 Torsvik et al. 1998 Costa Rica Rift ~50 mbs ~120 mbs Fluorescent in situ hybridization— probes specific for Bacteria or Archaea

37. (K) resin in fracture • Costa Rica Rift • ~100 mbs • 5.9 Ma (S) Torsvik et al. 1998 Elemental X-ray maps C P N • Costa Rica Rift • ~100 mbs • 5.9 Ma Other maps: Si, Mg, Ca, Na depleted Ti, Al, Fe, Mn, enriched

38. ‘BioColumn’ basement fluid sampler Cowen et al. 2003

39. 0.5 um Cell products from basement fluids (1026b, JFR) Propidium iodine-stained Giovannoni

40. Borehole 1026b basement fluids:Phylogenetic tree (ssu rRNA): bacterial groups Low G+C 1026B clones’ closest known relations: Sulfate reducers Fermentative heterotrophs Nitrate reducers (NH3 production) N2 fixers? (NH3 production) Thermophilic members -Proteobacteria Cowen et al. 2003

41. Borehole 1026b fluids: Phylogenetic tree (ssu rRNA): Archaea 1026B clones’ closest known relations to: Sulfate reducers Genes from Yellowstone hot springs Thermophiles Cowen et al. 2003

42. recharge Fluid 14C ages: 1ky 9.9ky 4.5ky Basement fluid ages(east flank JFR) 0.8 My 3.5 My 0 20 40 60 80 100 120 Distance from ridge axis (km) from Davis et al. 1999 Cowen, in press

43. Older, reduced Cowen 2004, as modified from Wheat et al. 2002 (partially) Reset time clock and redox conditions Wheat et al. 2002 Fisher et al. 2003

44. Speculated characteristics of buried ocean basement biosphere • Low cell abundance • Slow growing • Highly heterogeneous distributions (& activities) • Localized populations consistent w/ channelized flow • Punctuated by recharge zones • Diverse chemoautolithotrophic and heterotrophic (& unusual) metabolisms • Microbial consortia likely important and associated with biofilm formation

45. Summary • Ocean Basement environments are dynamic and complex • Biosphere within aging basement is predicted: • Favorable temperature ranges, • Active fluid flow (is it enough?) • Reactive basaltic rocks • Existing (preliminary) phylogentic data consistent w/ chemical data • Challenges • Accessibility • Contamination • Life perhaps ubiquitous, but low biomass/activity?

46. Future borehole observatory opportunities • Cores from drilling operations • Short and long-term observations • In situ (downhole) instrumentation • Fluid collections • In situ incubations • Other experiments (e.g., push-pull) (seafloor and downhole)

47. Contamination issues Drilling operations • Drilling muds, bottom seawater, sediments Observatory materials • Packing cement • Borehole casing • Sample delivery tubing

48. CORK-II Observatory

50. Downhole sampling Cowen and Taylor, in development