Microbial communities on seafloor basalts at Dorado Outcrop reflect level of alteration and highlight global lithic clades

Frontiers in Microbiology

Volumn 6, Issue DEC, 2015, Pages

  Lee, Michael D ^a   Walworth, Nathan G ^a   Sylvan, Jason B ^a,b   Edwards, Katrina J ^a   Orcutt, Beth N ^c  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c BIGELOW LABORATORY FOR OCEAN SCIENCES   (United States)

Author keywords

Basalt; Biogeography; Geomicrobiology; Microbe mineral interactions; Oceanic crust

Indexed keywords

RNA 16S;

ARTICLE; BASALT; CHEMOLITHOAUTOTROPH; CLADISTICS; DELTAPROTEOBACTERIA; DNA EXTRACTION; GENE SEQUENCE; GENETIC VARIABILITY; HYDROTHERMAL VENT; MICROBIAL COMMUNITY; NONHUMAN; PHYLOGENETIC TREE; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; THAUMARCHAEOTA;

EID: 84954207328     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01470     Document Type: Article

References (68)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410. doi: 10.1016/S0022-2836(05)80360-2.
2. Amoozegar, M. A., Makhdoumi-Kakhki, A., Ramezani, M., Nikou, M. M., Fazeli, S. A., Schumann, P., et al. (2013). Limimonas halophila gen. nov., sp. nov., an extremely halophilic bacterium in the family Rhodospirillaceae. Int. J. Syst. Evol. Microbiol. 63, 1562-1567. doi: 10.1099/ijs.0.041236-0.
3. Bach, W., and Edwards, K. J. (2003). Iron and sulfide oxidation within basalt ocean crust: implications for chemolithoautotrophic microbial biomass production. Geochim. Cosmochim. Acta 67, 3871-3887. doi: 10.1016/S0016-7037(03)00304-1.
4. Bessette, S., Fagervold, S. K., Romano, C., Martin, D., Le Bris, N., and Galand, P. E. (2014). Diversity of bacterial communities on sunken woods in the mediterranean sea. J. Mar. Sci. Technol. 22, 60-66. doi: 10.6119/JMST-013-0829-2.
5. Bokulich, N. A., Subramanian, S., Faith, J. J., Gevers, D., Gordon, J. I., Knight, R., et al. (2013). Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10, 57-59. doi: 10.1038/NMETH.2276.
6. Brochier-Armanet, C., Boussau, B., Gribaldo, S., and Forterre, P. (2008). Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245-252. doi: 10.1038/nrmicro1852.
7. Caporaso, J. G., Lauber, C. L., Walters, W., Berg-Lyons, D., Huntley, J., Fierer, N., et al. (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621-1624. doi: 10.1038/ismej.2012.8.
8. Champlot, S., Berthelot, C., Pruvost, M., Bennett, E. A., Grange, T., and Maria Geigl, E. M. (2010). An efficient multistrategy DNA decontamination procedure of PCR reagents for hypersensitive PCR applications. PLoS ONE 5:e13042. doi: 10.1371/journal.pone.0013042.
9. Choi, D. H., Hwang, C. Y., and Cho, B. C. (2009). Pelagibius litoralis gen. nov., sp. nov., a marine bacterium in the family Rhodospirillaceae isolated from coastal seawater. Int. J. Syst. Evol. Microbiol. 59, 818-823. doi: 10.1099/ijs.0.002774-0.
10. Daughney, C., Rioux, J., Fortin, D., and Pichler, T. (2004). Laboratory investigation of the role of bacteria in the weathering of basalt near deep sea hydrothermal vents. Geomicrobiol. J. 21, 21-31. doi: 10.1080/01490450490253437.
11. Edgar, R. C. (2004). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113. doi: 10.1186/1471-2105-5-113.
12. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200. doi: 10.1093/bioinformatics/btr381.
13. 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.
14. Edwards, K. J., Bach, W., McCollom, T. M., and Rogers, D. R. (2004). Neutrophilic iron-oxidizing bacteria in the ocean: their habitats, diversity, and roles in mineral deposition, rock alteration, and biomass production in the deep-sea. Geomicrobiol. J. 21, 393-404. doi: 10.1080/01490450490485863.
15. Edwards, K. J., Rogers, D. R., Wirsen, C. O., and McCollom, T. M. (2003). 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.
16. Einen, J., Thorseth, I. H., and Ovreås, L. (2008). Enumeration of archaea and bacteria in seafloor basalt using real-time quantitative PCR and fluorescence microscopy. FEMS Microbiol. Lett. 282, 182-187. doi: 10.1111/j.1574-6968.2008.01119.x.
17. Elderfield, H., and Schultz, A. (1996). Mid-ocean ridge hydrothermal fluxes and the chemical composition of the ocean. Annu. Rev. Earth Planet. Sci. 24, 191-224. doi: 10.1146/annurev.earth.24.1.191.
18. Emerson, D., Rentz, J. A., Lilburn, T. G., Davis, R. E., Aldrich, H., Chan, C., et al. (2007). A novel lineage of proteobacteria involved in formation of marine fe-oxidizing microbial mat communities. PLoS ONE 2:e667. doi: 10.1371/journal.pone.0000667.
19. Etnoyer, P., John, W., and Shirley, T. (2010). How large is the seamount biome? Oceanography 23, 206-209. doi: 10.5670/oceanog.2010.96.
20. German, C. R., Von Damm, K. L. (2004). Hydrothermal processes. Treat. Geochem. 6, 181-222. Available online at: http://www.sciencedirect.com/science/referenceworks/9780080437514.
21. Hutnak, M., Fisher, A. T., Harris, R., Stein, C., Wang, K., Spinelli, G., et al. (2008). Large heat and fluid fluxes driven through mid-plate outcrops on ocean crust. Nat. Geosci. 1, 611-614. doi: 10.1038/ngeo264.
22. Karner, M. B., DeLong, E. F., and Karl, D. M. (2001). Archaeal dominance in the mesopelagic zone of the pacific ocean. Nature 409, 507-510. doi: 10.1038/35054051.
23. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., et al. (2012). Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649. doi: 10.1093/bioinformatics/bts199.
24. Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., and Schloss, P. D. (2013). Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the Miseq Illumina sequencing platform. Appl. Environ. Microbiol. 79, 5112-5120. doi: 10.1128/AEM.01043-13.
25. Lane, D. J. (1991). "16S/23S rRNA Sequencing," in Nucleic Acid Techniques in Bacterial Systematics (Wiley), 125-175. Available online at: http://ci.nii.ac.jp/naid/10008470323/en/.
26. Legendre, P., and Gallagher, E. D. (2001). Ecologically meaningful transformations for ordination of species data. Oecologia 129, 271-280. doi: 10.1007/s004420100716.
27. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, A., et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371. doi: 10.1093/nar/gkh293.
28. 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, 213-230. doi: 10.1016/j.femsec.2004.06.014.
29. 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.
30. Mason, O. U., Stingl, U., Wilhelm, L. J., Moeseneder, M. M., Di Meo-Savoie, C. A., Fisk, M. R., et al. (2007). The phylogeny of endolithic microbes associated with marine basalts. Environ. Microbiol. 9, 2539-2550. doi: 10.1111/j.1462-2920.2007.01372.x.
31. Matsen, F. A., Kodner, R. B., and Armbrust, E. V. (2010). Pplacer: linear time maximum-likelihood and bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics 11:538. doi: 10.1186/1471-2105-11-538.
32. Mero, J. (1962). Ocean-floor manganese nodules. Econ. Geol. 57, 747-767. doi: 10.2113/gsecongeo.57.5.747.
33. Mori, K., Ichiro Suzuki, K., Urabe, T., Sugihara, M., Tanaka, K., Hamada, M., et al. (2011). Thioprofundum hispidum sp. nov., an obligately chemolithoautotrophic sulfur-oxidizing Gammaproteobacterium isolated from the hydrothermal field on Suiyo Seamount, and proposal of Thioalkalispiraceae fam. nov. in the order Chromatiales. Int. J. Syst. Evol. Microbiol. 61, 2412-2418. doi: 10.1099/ijs.0.026963-0.
34. Nitahara, S., Kato, S., Urabe, T., Usui, A., and Yamagishi, A. (2011). Molecular characterization of the microbial community in hydrogenetic ferromanganese crusts of the Takuyo-Daigo Seamount, Northwest Pacific. FEMS Microbiol. Lett. 321, 121-129. doi: 10.1111/j.1574-6968.2011.02323.x.
35. Northup, D. E., Barns, S. M., Yu, L. E., Spilde, M. N., Schelble, R. T., Dano, K. E., et al. (2003). Diverse microbial communities inhabiting ferromanganese deposits in lechuguilla and spider caves. Environ. Microbiol. 5, 1071-1086. doi: 10.1046/j.1462-2920.2003.00500.x.
36. Oksanen, J. (2015). Vegan: Community Ecology Package. Available online at: http://cran.r-project.org/package=vegan.
37. Orcutt, B. N., Sylvan, J. B., Rogers, D. R., Delaney, J., Lee, R. W., and Girguis, P. R. (2015). Carbon fixation by basalt-hosted microbial communities. Front. Microbiol. 6:904. doi: 10.3389/fmicb.2015.00904.
38. Park, B. J., Park, S. J., Yoon, D. N., Schouten, S., Damsté, J. S. S., and Rhee, S. K. (2010). Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl. Environ. Microbiol. 76, 7575-7587. doi: 10.1128/AEM.01478-10.
39. Park, S.-J., Kim, J.-G., Jung, M.-Y., Kim, S.-J., Cha, I.-T., Kwon, K., et al. (2012). Draft genome sequence of an ammonia-oxidizing archaeon, 'Candidatus Nitrosopumilus Koreensis' AR1, from marine sediment. J. Bacteriol. 194, 6940-6941. doi: 10.1128/JB.01857-12.
40. Pruesse, E., Peplies, J., and Glöckner, F. O. (2012). SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823-1829. doi: 10.1093/bioinformatics/bts252.
41. Racine, J. (2012). RSTUDIO: a platform-independent IDE for R and Sweave. J. Appl. Econ. 27, 36-37. doi: 10.1002/jae.1278.
42. Rogers, D. R., Santelli, C. M., and Edwards, K. J. (2003). Geomicrobiology of deep-sea deposits: estimating community diversity from low-temperature seafloor rocks and minerals. Geobiology 1, 109-117. doi: 10.1046/j.1472-4669.2003.00009.x.
43. 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.
44. 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.
45. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541. doi: 10.1128/AEM.01541-09.
46. Stamatakis, A. (2014). RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313. doi: 10.1093/bioinformatics/btu033.
47. Staudigel, H., Chastain, R. A., Yayanos, A., and Bourcier, W. (1995). Biologically mediated dissolution of glass. Chem. Geol. 126, 147-154. doi: 10.1016/0009-2541(95)00115-X.
48. Staudigel, H., Furnes, H., McLoughlin, N., Banerjee, N. R., Connell, L. B., and Templeton, A. (2008). 3.5 Billion years of glass bioalteration: volcanic rocks as a basis for microbial life? Earth Sci. Rev. 89, 156-176. doi: 10.1016/j.earscirev.2008.04.005.
49. Staudigel, H., Yayanos, A., and De Baar, H. (1998). Biologically Mediated dissolution of volcanic glass in seawater. Earth Planet. Sci. Lett. 164, 233-244. doi: 10.1016/S0012-821X(98)00207-6.
50. Sudek, L., Templeton, A. S., Tebo, B. M., and Staudigel, H. (2009). Microbial ecology of Fe (hydr)oxide mats and basaltic rock from Vailulu'u seamount, American Samoa. Geomicrobiol. J. 26, 581-596. doi: 10.1080/01490450903263400.
51. 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.
52. Takai, K., Miyazaki, M., Hirayama, H., Nakagawa, S., Querellou, J., and Godfroy, A. (2009). Isolation and physiological characterization of two novel, piezophilic, thermophilic chemolithoautotrophs from a deep-sea hydrothermal vent chimney. Environ. Microbiol. 11, 1983-1997. doi: 10.1111/j.1462-2920.2009.01921.x.
53. Tanaka, N., Romanenko, L. A., Kurilenko, V. V., Svetashev, V. I., Kalinovskaya, N. I., and Mikhailov, V. V. (2014). Loktanella maritima sp. nov. isolated from shallow marine sediments. Int. J. Syst. Evol. Microbiol. 64, 2370-2375. doi: 10.1099/ijs.0.061747-0.
54. Templeton, A. S., Knowles, E. J., Eldridge, D. L., Arey, B. W., Dohnalkova, A. C., et al. (2009). A seafloor microbial biome hosted within incipient ferromanganese crusts. Nat. Geosci. 2, 872-876. doi: 10.1038/ngeo696.
55. Templeton, A. S., Staudigel, H., and Tebo, B. M. (2005). Diverse Mn(II)-oxidizing bacteria isolated from submarine basalts at loihi seamount. Geomicrobiol. J. 22, 127-139. doi: 10.1080/01490450590945951.
56. Thorseth, I. H., Furnes, H., and Tumyr, O. (1995). Textural and chemical effects of bacterial activity on basaltic glass: an experimental approach. Chem. Geol. 119, 139-160. doi: 10.1016/0009-2541(94)00098-S.
57. Thorseth, I. H., Torsvik, T., and Torsvik, V. (2001). Diversity of life in ocean floor basalt. Earth Planet. 194, 31-37. doi: 10.1016/S0012-821X(01)00537-4.
58. Toner, B. M., Lesniewski, R. A., Marlow, J. J., Briscoe, L. J., Santelli, C. M., Bach, W., et al. (2013). Mineralogy drives bacterial biogeography of hydrothermally inactive seafloor sulfide deposits. Geomicrobiol. J. 30, 313-326. doi: 10.1080/01490451.2012.688925.
59. Verna, C., Ramette, A., Wiklund, H., Dahlgren, T. G., Glover, A. G., Gaill, F., et al. (2010). High symbiont diversity in the bone-eating worm Osedax mucofloris from shallow whale-falls in the north atlantic. Environ. Microbiol. 12, 2355-2370. doi: 10.1111/j.1462-2920.2010.02299.x.
60. Walker, C. B., de la Torre, J. R., Klotz, M. G., Urakawa, H., Pinel, N., Arp, D. J., et al. (2010). Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl. Acad. Sci. U.S.A. 107, 8818-8823. doi: 10.1073/pnas.0913533107.
61. Wessel, P., Sandwell, D., and Kim, S. (2010). The global seamount census. Oceanography 23, 24-33. doi: 10.5670/oceanog.2010.60.
62. Wheat, C. G., and Fisher, A. T. (2008). Massive, low-temperature hydrothermal flow from a basaltic outcrop on 23 Ma seafloor of the cocos plate: chemical constraints and implications. Geochem. Geophys. Geosyst. 9:Q12014. doi: 10.1029/2008GC002136.
63. Wheat, C. G., and Mottl, M. J. (2000). Composition of pore and spring waters from baby bare: global implications of geochemical fluxes from a ridge flank hydrothermal system. Geochim. Cosmochim. Acta 64, 629-642. doi: 10.1016/S0016-7037(99)00347-6.
64. Williams, K. P., Gillespie, J. J., Sobral, B. W., Nordberg, E. K., Snyder, E. E., Shallom, J. M., et al. (2010). Phylogeny of gammaproteobacteria. J. Bacteriol. 192, 2305-2314. doi: 10.1128/JB.01480-09.
65. Wright, E. S., Yilmaz, L. S., and Noguera, D. R. (2012). DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl. Environ. Microbiol. 78, 717-725. doi: 10.1128/AEM.06516-11.
66. Yarza, P., Richter, M., Peplies, J., Euzeby, J., Amann, R., Schleifer, K. H., et al. (2008). The all-species living tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst. Appl. Microbiol. 31, 241-250. doi: 10.1016/j.syapm.2008.07.001.
67. Zimmerman, D. (1987). Comparative power of Student T Test and Mann-Whitney U Test for unequal sample sizes and variances. J. Exp. Edu. 55, 171-174. doi: 10.1080/00220973.1987.10806451.
68. Zinger, L., Gobet, A., and Pommier, T. (2012). Two decades of describing the unseen majority of aquatic microbial diversity. Mol. Ecol. 21, 1878-1896. doi: 10.1111/j.1365-294X.2011.05362.x.