Carbon fixation by basalt-hosted microbial communities

Frontiers in Microbiology

Volumn 6, Issue SEP, 2015, Pages

  Orcutt, Beth N ^a,b   Sylvan, Jason B ^b   Rogers, Daniel R ^c,d   Delaney, Jennifer ^c   Lee, Raymond W ^e   Girguis, Peter R ^c  

^a BIGELOW LABORATORY FOR OCEAN SCIENCES   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c HARVARD UNIVERSITY   (United States)

^d STONEHILL COLLEGE   (United States)

^e WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Basalt; Biogeochemistry; Carbon fixation; Deep biosphere; Geomicrobiology; Microbial ecology; Ocean crust

Indexed keywords

RNA 16S;

ARTICLE; BASALT; BIOFILM; CARBON CYCLE; CARBON FIXATION; CITRIC ACID CYCLE; CONTROLLED STUDY; GENE DOSAGE; GENE EXPRESSION; GENE SEQUENCE; GEOGRAPHIC DISTRIBUTION; ISOTOPE LABELING; MICROBIAL COMMUNITY; NONHUMAN; PENTOSE PHOSPHATE CYCLE; POLYMERASE CHAIN REACTION;

EID: 84946750553     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00904     Document Type: Article

References (49)

1. Alt, J. C., and Mata, P. (2000). On the role of microbes in the alterations of submarine basaltic glass: a TEM study. Earth Planetary Sci. Lett. 181, 301-313. doi: 10.1016/S0012-821X(00)00204-1
2. Alt, J. C., and Teagle, D. A. H. (1999). The uptake of carbon during alteration ocean crust. Geochim. Cosmochim. Acta 63, 1527-1535. doi: 10.1016/S0016-7037(99)00123-4
3. Ashida, H., Danchin, A., and Yokota, A. (2005). Was photosynthetic RuBisCO recruited by acquisitive evolution from RuBisCO-like proteins involved in sulfur metabolism? Res. Microbiol. 156, 611-618. doi: 10.1016/j.resmic.2005.01.014
4. Bach, W., and Edwards, K. J. (2003). Iron and sulfide oxidation within the basaltic ocean crust: implications for chemolithoautotrophic microbial biomass production. Geochim. Cosmochim. Acta 67, 3871-3887. doi: 10.1016/s0016-7037(00)00304-301
5. Bach, W., Humphris, S., and Fisher, A. T. (2004). Fluid flow and fluid-rock interaction within ocean crust: reconciling geochemical, geological, and geophysical observations. Am. Geophys. Union 144, 99-117.
6. Campbell, B. J., and Cary, S. C. (2004). Abundance of reverse tricarboxylic acid cycle genes in free-living microorganisms at deep-sea hydrothermal vents. Appl. Environ. Microbiol. 70, 6282-6289. doi: 10.1128/AEM.70.10.6282-6289.2004
7. Edmond, J. M., and Von Damm, K. L. (1983). Hot springs on the ocean floor. Sci. Am. 248, 78-93. doi: 10.1038/scientificamerican0483-78
8. Edwards, K. J., Bach, W., and Mccollom, T. M. (2005). Geomicrobiology in oceanography: microbe-mineral interactions at and below the seafloor. Trends Microbiol. 13, 449-456. doi: 10.1016/j.tim.2005.07.005
9. Edwards, K. J., Mccollom, T. M., Konishi, H., and Buseck, P. R. (2003a). Seafloor bioalteration of sulfide minerals: results from in-situ incubation studies. Geochim. Cosmochim. Acta 67, 2843-2856. doi: 10.1016/S0016-7037(03)00089-9
10. Edwards, K. J., Rogers, D. R., Wirsen, C. O., and Mccollom, T. M. (2003b). Isolation and characterization of novel, psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic alpha-and gamma-Proteobacteria from the deep sea. Appl. Environ. Microbiol. 69, 2906-2913. doi: 10.1128/AEM.69.5.2906-2913.2003
11. Expedition 336 Scientists. (2012a). "Methods," in Proceedings of the Integrated Ocean Drilling Program, Vol. 336, eds K. J. Edwards, W. Bach, A. Klaus, and Expedition 336 Scientists (Tokyo: Integrated Ocean Drilling Program Management International, Inc.). doi: 10.2204/iodp.proc.336.102.2012
12. Expedition 336 Scientists. (2012b). "Sediment and basement contact coring," in: Proceeding of the Integrated Ocean Drilling program, Vol. 336, eds K. J. Edwards, W. Bach, A. Klaus, and Expedition 336 Scientists (Tokyo: Integrated Ocean Drilling Program Management International, Inc.).
13. Expedition 336 Scientists. (2012c). "Site U1382," in Proceedings of the Integrated Ocean Drilling Program, Vol. 336, eds K. J. Edwards, W. Bach, A. Klaus, and Expedition 336 Scientists (Tokyo: Integrated Ocean Drilling Program Management International, Inc.).
14. Expedition 336 Scientists. (2012d). "Site U1383," in Proceedings of the Integrated Ocean Drilling Program, Vol. 336, eds K. J. Edwards, W. Bach, A. Klaus, and Expedition 336 Scientists (Tokyo: Integrated Ocean Drilling Program Management International, Inc.).
15. Fisher, A. T., and Becker, K. (2000). Channelized fluid flow in oceanic crust reconciles heat-flow and permeability data. Nature 403, 71-74. doi: 10.1038/47463
16. Goltsman, D. S., Denef, V. J., Singer, S. W., Ver Berkmoes, N. C., Lefsrud, M., Mueller, R. S., et al. (2009). Community genomic and proteomic analyses of chemoautotrophic iron-oxidizing Leptospirillum rubrum (Group II) and Leptospirillum ferrodiazotrophum (Group III) bacteria in acid mine drainage biofilms. Appl. Environ. Microbiol. 75, 4599-4615. doi: 10.1128/AEM.02943-08
17. Jacobsen Meyers, M. E., Sylvan, J. B., and Edwards, K. J. (2014). Extracellular enzyme activity and microbial diversity measured on seafloor exposed basalts from Loihi Seamount indicate importance of basalts to global biogeochemical cycling. Appl. Environ. Microbiol. doi: 10.1128/AEM.01038-1014
18. Kuever, J., Rainey, F. A., and Widdel, F. (2005). "Class IV. Deltaproteobacteria class nov.," in Bergey's Manual of Systematic Bacteriology, 2nd Edn, eds D. J. Brenner, N. R. Krieg, and J. T. Staley (New York, NY: Springer-Verlag), 922-1144.
19. Lever, M. A., Rouxel, O. J., Alt, J. C., Shimizu, N., Ono, S., Coggon, R. M., et al. (2013). Evidence for microbial carbon and sulfur cycling in deeply buried ridge flank basalt. Science 339, 1305-1308. doi: 10.1126/science.1229240
20. Levicán, G., Ugaide, J. A., Ehrenfeld, N., Maass, A., and Parada, P. (2008). Comparative genomic analysis of carbon and nitrogen assimilation mechanisms in three indigenous bioleaching bacteria: predictions and validation. BMC Genomics 9:581. doi: 10.1186/1471-2164-9-581
21. Lin, H.-T. (2013). Biogeochemistry of Basement Fluids From the Sediment-Buried Juan de Fuca Ridge flanks. Ph.D., University of Hawaii, Hilo, HI.
22. Lin, H.-T., Cowen, J. P., Olson, E. J., Amend, J. P., and Lilley, M. D. (2012). Inorganic chemistry, gas compositions and dissolved organic carbon in fluids from sedimented young basaltic crust on the Juan de Fuca Ridge flanks. Geochim. Cosmochim. Acta 85, 213-227. doi: 10.1016/j.gca.2012.02.017
23. Lücker, S., Wagner, M., Maixner, F., Pelletier, E., Koch, H., Vacherie, B., et al. (2010). A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc. Natl. Acad. Sci. U.S.A. 107, 13479-13484. doi: 10.1073/pnas.1003860107
24. Luton, P. E., Wayne, J. M., Sharp, R. J., and Riley, P. W. (2002). The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148, 3521-3530.
25. Lysnes, K., Thorseth, I. H., Steinsbu, B. O., Øvreås, L., Torsvik, T., and Pedersen, R. B. (2004). Microbial community diversity in seafloor basalt from the Arctic spreading ridges. FEMS Microbiol. Ecol. 50, 13-230. doi: 10.1016/j.femsec.2004.06.014
26. Markowitz, V. M., Korzeniewski, F., Palaniappan, K., Szeto, E., Werner, G., Padki, A., et al. (2006). The integrated microbial genomes (IMG) system. Nucleic Acids Res. 34, D344-D348. doi: 10.1093/nar/gkj024
27. Mason, O. U., Di Meo-Savoie, C. A., Van Nostrand, J. D., Zhou, J., Fisk, M. R., and Giovannoni, S. J. (2009). Prokaryotic diversity, distribution, and insights into their role in biogeochemical cycling in marine basalts. ISME J. 3, 231-242. doi: 10.1038/ismej.2008.92
28. Mason, O. U., Nakagawa, T., Rosner, M., Van Nostrand, J. D., Zhou, J., Maruyama, A., et al. (2010). First investigation of the microbiology of the deepest layer of ocean crust. PLoS ONE 5:e15399. doi: 10.1371/journal.pone.0015399
29. McCarthy, M. D., Beaupré, S. R., Walker, B. D., Voparil, I., Guilderson, T. P., and Druffel, E. R. M. (2011). Chemosynthetic origin of 14C-depleted dissolved organic matter in a ridge-flank hydrothermal system. Nat. Geosci. 4, 32-36. doi: 10.1038/ngeo1015
30. Nagata, T., Tamburini, C., Arístegui, J., Baltar, F., Bochdansky, A. B., Fonda-Umani, S., et al. (2010). Emerging concepts on microbial processes in the bathypelagic ocean-ecology, biogeochemistry, and genomics. Deep Sea Res. Part II Top. Stud. Oceanogr. 57, 1519-1536. doi: 10.1016/j.dsr2.2010.02.019
31. Orcutt, B. N., Bach, W., Becker, K., Fisher, A. T., Hentscher, M., Toner, B. M., et al. (2011a). Colonization of subsurface microbial observatories deployed in young ocean crust. ISME J. 5, 692-703. doi: 10.1038/ismej.2010.157
32. Orcutt, B. N., Sylvan, J. B., Knab, N. J., and Edwards, K. J. (2011b). Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol. Mol. Biol. Rev. 75, 361-422. doi: 10.1128/MMBR.00039-10
33. Orcutt, B. N., Wheat, C. G., Rouxel, O. J., Hulme, S., Edwards, K. J., and Bach, W. (2013). Oxygen consumption rates in subseafloor basaltic crust derived from a reaction transport model. Nat. Commun. 4, 2539. doi: 10.1038/ncomms3539
34. Robador, A., Jungbluth, S. P., Larowe, D. E., Bowers, R. M., Rappé, M. S., Amend, J. P., et al. (2014). Activity and phylogenetic diversity of sulfate-reducing microorganisms in low-temperature subsurface fluids with the upper oceanic crust. Front. Microbiol. 5:748. doi: 10.3389/fmicb.2014.00748
35. Rouxel, O. J., Ono, S., Alt, J., Rumble, D., and Ludden, J. (2008). Sulfur isotope evidence for microbial sulfate reduction in altered oceanic basalts at ODP Site 801. Earth Planetary Sci. Lett. 268, 110-123. doi: 10.1016/j.epsl.2008.01.010
36. Ryan, W. B. F., Carbotte, S. M., Coplan, J. O., O'hara, S., Melkonian, A., Arko, R., et al. (2009). Global multi-resolution topograpjy synthesis. Geochem. Geophys. Geosyst. 10:Q03014. doi: 10.1029/2008GC002332
37. Santelli, C. M., Edgcomb, V. P., Bach, W., and Edwards, K. J. (2009). The diversity and abundance of bacteria inhabiting seafloor lavas positively correlate with rock alteration. Environ. Microbiol. 11, 86-98. doi: 10.1111/j.1462-2920.2008.01743.x
38. Santelli, C. M., Orcutt, B. N., Banning, E., Bach, W., Moyer, C. L., Sogin, M. L., et al. (2008). Abundance and diversity of microbial life in ocean crust. Nature 453, 653-656. doi: 10.1038/nature06899
39. Smith, D. C., Spivack, A. J., Fisk, M. R., Haveman, S. A., Staudigel, H., and Party, L. S. S. (2000). Methods for quantifying potential microbial contamination during deep ocean coring. ODP Technical. Note 28. doi: 10.2973/odp.tn.28.2000
40. Stevens, T. O., and McKinley, J. P. (1995). Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270, 450-454. doi: 10.1126/science.270.5235.450
41. Suzuki, M. T., Béjà, O., Taylor, L. T., and Delong, E. F. (2001). Phylogenetic analysis of ribosomal RNA operons from uncultivated coastal marine bacterioplankton. Environ. Microbiol. 3, 323-331. doi: 10.1046/j.1462-2920.2001.00198.x
42. Sylvan, J. B., Sia, T. Y., Haddad, A. G., Briscoe, L. J., Toner, B. M., Girguis, P. R., et al. (2013). Low temperature geomicrobiology follows host rock composition along a geochemical gradient in Lau Basin. Front. Microbiol. 4:61. doi: 10.3389/fmicb.2013.00061
43. Takai, K., Campbell, B. J., Cary, S. C., Suzuki, M., Oida, H., Nunoura, T., et al. (2005). Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria. Appl. Environ. Microbiol. 71, 7310-7320. doi: 10.1128/AEM.71.11.7310-7320.2005
44. Takai, K., and Horikoshi, K. (2000). Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl. Environ. Microbiol. 66, 5066-5072. doi: 10.1128/AEM.66.11.5066-5072.2000
45. Templeton, A. S., Knowles, E. J., Eldridge, D. L., Arey, B. W., Dohnalkova, A. C., Webb, S. M., et al. (2009). A seafloor microbial biome hosted within incipient ferromanganese crusts. Nat. Geosci. 2, 872-876. doi: 10.1038/NGEO696
46. Toner, B. M., Santelli, C. M., Marcus, M. A., Wirth, R., Chan, C. S., Mccollom, T. M., et al. (2009). Biogenic iron oxyhydroxide formation at mid-ocean ridge hydrothermal vents: juan de Fuca Ridge. Geochim. Cosmochim. Acta 73, 388-403. doi: 10.1016/j.gca.2008.09.035
47. Ver Eecke, H. C., Butterfield, D. A., Huber, J. A., Lilley, M. D., Olson, E. J., Roe, K. K., et al. (2012). Hydrogen-limited growth of hyperthermophilic methanogens at deep-sea hydrothermal vents. Proc. Natl. Acad. Sci. U.S.A. 109, 13674-13679. doi: 10.1073/pnas.1206632109
48. Wheat, C. G., Jannasch, H. W., Fisher, A. T., Becker, K., Sharkey, J., and Hulme, S. (2010). Subseafloor seawater-basalt-microbe reactions: continuous sampling of borehole fluids in a ridge flank environment. Geochem. Geophys. Geosyst. 11:Q07011. doi: 10.1029/2010GC003057
49. Wheat, C. G., Jannasch, H. W., Kastner, M., Plant, J. N., and Decarlo, E. H. (2003). Seawater transport and reaction in upper oceanic basaltic basement: chemical data from continuous monitoring of sealed boreholes in a ridge flank environment. Earth Planetary Sci. Lett. 216, 549-564. doi: 10.1016/S0012-821X(03)00549-1