Bacterial community structure across environmental gradients in permafrost thaw ponds: Methanotroph-rich ecosystems

Frontiers in Microbiology

Volumn 6, Issue MAR, 2015, Pages

  Crevecoeur, Sophie ^a,b   Vincent, Warwick F ^a,b   Comte, Jérôme ^a,b   Lovejoy, Connie ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b CENTRE D ÉTUDES NORDIQUES   (Canada)

Author keywords

16S rRNA; Bacterial diversity; Methanotrophs; Permafrost; Pyrosequencing; Thaw ponds

Indexed keywords

COMPLEMENTARY DNA; ORGANIC CARBON; RNA 16S;

AQUATIC ENVIRONMENT; ARTICLE; BACTERIAL GENETICS; CARBON FOOTPRINT; ENVIRONMENTAL FACTOR; METHANOTROPHIC BACTERIUM; MICROBIAL COMMUNITY; NONHUMAN; OXYGEN CONCENTRATION; PERMAFROST; PH; PHYSICAL CHEMISTRY; POND; PROTEOBACTERIA; PYROSEQUENCING; QUANTITATIVE ANALYSIS; RNA EXTRACTION; SEQUENCE ANALYSIS; TAXONOMIC IDENTIFICATION; TEMPERATURE; THAWING; VARIOVORAX; WATER SAMPLING;

BACTERIA (MICROORGANISMS);

EID: 84927521025     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00192     Document Type: Article

References (88)

1. Allgaier, M., and Grossart, H. (2006). Diversity and seasonal dynamics of Actinobacteria populations in four lakes in northeastern Germany. Appl. Environ. Microbiol. 72, 3489-3497. doi: 10.1128/AEM.72.5.3489.
2. Arlen-Pouliot, Y., and Bhiry, N. (2005). Palaeoecology of a palsa and a filled thermokarst pond in a permafrost peatland, subarctic Québec, Canada. Holocene 15, 408-419. doi: 10.1191/0959683605hl818rp.
3. Bhiry, N., Delwaide, A., Allard, M., Bégin, Y., Filion, L., Lavoie, M., et al. (2011). Environmental change in the Great Whale River Region, Hudson Bay: five decades of multidisciplinary research by Centre d'études Nordiques (CEN). Ecoscience 18, 182-203. doi: 10.2980/18-3-3469.
4. Blazewicz, S. J., Barnard, R. L., Daly, R. A., and Firestone, M. K. (2013). Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J. 7, 2061-2068. doi: 10.1038/ismej.2013.102.
5. Bodelier, P. L., Meima-Franke, M., Hordijk, C. A., Steenbergh, A. K., Hefting, M. M., Bodrossy, L., et al. (2013). Microbial minorities modulate methane consumption through niche partitioning. ISME J. 7, 2214-2228. doi: 10.1038/ismej.2013.99.
6. Bogard, M. J., Del Giorgio, P. A., Boutet, L., Chaves, M. C. G., Prairie, Y. T., Merante, A., et al. (2014). Oxic water column methanogenesis as a major component of aquatic CH4 fluxes. Nat. Commun. 5:5350. doi: 10.1038/ncomms6350.
7. Bonilla, S., Villeneuve, V., and Vincent, W. F. (2005). Benthic and planktonic algal communities in a high Arctic lake: pigment structure and contrasting responses to nutrient enrichment. J. Phycol. 41, 1120-1130. doi: 10.1111/j.1529-8817.2005.00154.x.
8. Borcard, D., Gillet, F., and Legendre, P. (2011). Numerical Ecology with R. New York: Springer. doi: 10.1007/978-1-4419-7976-6.
9. Börjesson, G., Sundh, I., and Svensson, B. (2004). Microbial oxidation of CH4 at different temperatures in landfill cover soils. FEMS Microbiol. Ecol. 48, 305-312. doi: 10.1016/j.femsec.2004.02.006.
10. Borrel, G., Jézéquel, D., Biderre-Petit, C., Morel-Desrosiers, N., Morel, J.-P., Peyret, P., et al. (2011). Production and consumption of methane in freshwater lake ecosystems. Res. Microbiol. 162, 832-847. doi: 10.1016/j.resmic.2011.06.004.
11. Boscaro, V., Felletti, M., Vannini, C., Ackerman, M. S., Chain, P. S. G., Malfatti, S., et al. (2013). Polynucleobacter necessarius, a model for genome reduction in both free-living and symbiotic bacteria. Proc. Natl. Acad. Sci. U.S.A. 110, 18590-18595. doi: 10.1073/pnas.1316687110.
12. Bouchard, F., Francus, P., Pienitz, R., and Laurion, I. (2014). Subarctic thermokarst ponds: investigating recent landscape evolution and sediment dynamics in thawed permafrost of northern Québec (Canada). Arct. Antarc. Alp. Res. 46, 251-271. doi: 10.1657/1938-4246-46.1.251.
13. Breton, J., Vallières, C., and Laurion, I. (2009). Limnological properties of permafrost thaw ponds in northeastern Canada. Can. J. Fish. Aquat. Sci. 66, 1635-1648. doi: 10.1139/F09-108.
14. Calmels, F., Allard, M., and Delisle, G. (2008). Development and decay of a lithalsa in Northern Québec: a geomorphological history. Geomorphology 97, 287-299. doi: 10.1016/j.geomorph.2007.08.013.
15. Campbell, B. J., and Kirchman, D. L. (2013). Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient. ISME J. 7, 210-220. doi: 10.1038/ismej.2012.93.
16. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336. doi: 10.1038/nmeth.f.303.
17. Cardinale, B. J., Srivastava, D. S., Duffy, J. E., Wright, J. P., Downing, A. L., Sankaran, M., et al. (2006). Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443, 989-992. doi: 10.1038/nature05202.
18. Casamayor, E. O., Schäfer, H., Bañeras, L., Pedrós-Alió, C., and Muyzer, G. (2000). Identification of and spatio-temporal differences between microbial assemblages from two neighboring sulfurous lakes: comparison by microscopy and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 66, 499-508. doi: 10.1128/AEM.66.2.499-508.2000.
19. Charvet, S., Vincent, W. F., Comeau, A., and Lovejoy, C. (2012). Pyrosequencing analysis of the protist communities in a High Arctic meromictic lake: DNA preservation and change. Front. Microbiol. 3:422. doi: 10.3389/fmicb.2012.00422.
20. Chowdhury, T. R., and Dick, R. P. (2013). Ecology of aerobic methanotrophs in controlling methane fluxes from wetlands. Appl. Soil Ecol. 65, 8-22. doi: 10.1016/j.apsoil.2012.12.014.
21. Colwell, R. K. (2012). "Biodiversity: concepts, patterns, and measurement, "in The Princeton Guide to Ecology, ed. S. A. Levin (Princeton, NJ: Princeton University Press), 257-263.
22. Comeau, A. M., Harding, T., Galand, P. E., Vincent, W. F., and Lovejoy, C. (2012). Vertical distribution of microbial communities in a perennially stratified Arctic lake with saline, anoxic bottom waters. Sci. Rep. 2:604. doi: 10.1038/srep00604.
23. Comeau, A. M., Li, W. K. W., Tremblay, J.-é., Carmack, E. C., and Lovejoy, C. (2011). Arctic Ocean microbial community structure before and after the 2007 record sea ice minimum. PLoS ONE 6:e27492. doi: 10.1371/journal.pone.0027492.
24. Costello, A. M., and Lindström, M. E. (1999). Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl. Environ. Microbiol. 65, 5066-5074.
25. Crump, B. C., Armbrust, E. V., and Baross, J. A. (1999). Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean. Appl. Environ. Microbiol. 65, 3192-3204.
26. Edgar, R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996-998. doi: 10.1038/nmeth.2604.
27. Eller, G., Känel, L., and Krüger, M. (2005). Cooccurrence of aerobic and anaerobic methane oxidation in the water column of Lake Plußsee. Appl. Environ. Microbiol. 71, 8925-8928. doi: 10.1128/AEM.71.12.8925.
28. Falge, E., Baldocchi, D., Tenhunen, J., Aubinet, M., Bakwin, P., Berbigier, P., et al. (2002). Seasonality of ecosystem respiration and gross primary production as derived from FLUXNET measurements. Agric. For. Meteorol. 113, 53-74. doi: 10.1016/S0168-1923(02)00102-8.
29. Fierer, N., and Jackson, R. B. (2006). The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. U.S.A. 103, 626-631. doi: 10.1073/pnas.0507535103.
30. Galand, P. E., Lovejoy, C., Pouliot, J., and Vincent, W. F. (2008). Heterogeneous archaeal communities in the particle-rich environment of an arctic shelf ecosystem. J. Marine Syst. 74, 774-782. doi: 10.1016/j.jmarsys.2007.12.001.
31. Garcia, S. L., Salka, I., Grossart, H.-P., and Warnecke, F. (2013). Depth-discrete profiles of bacterial communities reveal pronounced spatio-temporal dynamics related to lake stratification. Environ. Microbiol. Rep. 5, 549-555. doi: 10.1111/1758-2229.12044.
32. Gich, F. B., Borrego, C. M., Martinez-Planells, A., Steensgaard, D. B., Garcia-Gil, J., and Holzwarth, A. R. (2001). Variability of the photosynthetic antenna of a Pelodictyon clathratiforme population from a freshwater holomictic pond. FEMS Microbiol. Ecol. 37, 11-19. doi: 10.1111/j.1574-6941.2001.tb00848.x.
33. Graef, C., Hestnes, A. G., Svenning, M. M., and Frenzel, P. (2011). The active methanotrophic community in a wetland from the High Arctic. Environ. Microbiol. Rep. 3, 466-472. doi: 10.1111/j.1758-2229.2010.00237.x.
34. Grossart, H.-P., Frindte, K., Dziallas, C., Eckert, W., and Tang, K. W. (2011). Microbial methane production in oxygenated water column of an oligotrophic lake. Proc. Natl. Acad. Sci. U.S.A. 108, 19657-19661. doi: 10.1073/pnas.1110716108.
35. Gurney, S. D. (2001). Aspects of the genesis, geomorphology and terminology of palsas: perennial cryogenic mounds. Prog. Phys. Geogr. 25, 249-260. doi: 10.1177/030913330102500205.
36. Hahn, M. W. (2003). Isolation of strains belonging to the cosmopolitan Polynucleobacter necessarius cluster from freshwater habitats located in three climatic zones. Appl. Environ. Microbiol. 69, 5248-5254. doi: 10.1128/AEM.69.9.5248-5254.2003.
37. Han, J.-I., Choi, H.-K., Lee, S.-W., Orwin, P. M., Kim, J., LaRoe, S. L., et al. (2011). Complete genome sequence of the metabolically versatile plant growth-promoting endophyte Variovorax paradoxus S110. J. Bacteriol. 193, 1183-1190. doi: 10.1128/JB.00925-10.
38. Hollibaugh, J., Wong, P., Bano, N., Pak, S., Prager, E., and Orrego, C. (2001). Stratification of microbial assemblages in Mono Lake, California, and response to a mixing event. Hydrobiologia 466, 45-60. doi: 10.1023/A:1014505131859.
39. Jones, S. E., and Lennon, J. T. (2010). Dormancy contributes to the maintenance of microbial diversity. Proc. Natl. Acad. Sci. U.S.A. 107, 5881-5886. doi: 10.1073/pnas.0912765107.
40. Judd, K. E., Crump, B. C., and Kling, G. W. (2006). Variation in dissolved organic matter controls bacterial production and community composition. Ecology 87, 2068-2079. doi: 10.1890/0012-9658(2006)87[2068:VIDOMC]2.0.CO;2.
41. Kankaala, P., Huotari, J., Peltomaa, E., Saloranta, T., and Ojala, A. (2006). Methanotrophic activity in relation to methane efflux and total heterotrophic bacterial production in a stratified, humic, boreal lake. Limnol. Oceanogr. 51, 1195-1204. doi: 10.4319/lo.2006.51.2.1195.
42. Koch, J. C., Gurney, K., and Wipfli, M. S. (2014). Morphology-dependent water budgets and nutrient fluxes in arctic thaw ponds. Permafrost Periglacial Process. 25, 79-93. doi: 10.1002/ppp.1804.
43. Kritzberg, E. S., Langenheder, S., and Lindström, E. S. (2006). Influence of dissolved organic matter source on lake bacterioplankton structure and function-implications for seasonal dynamics of community composition. FEMS Microbiol. Ecol. 56, 406-417. doi: 10.1111/j.1574-6941.2006.00084.x.
44. Laanbroek, H. J. (2010). Methane emission from natural wetlands: interplay between emergent macrophytes and soil microbial processes. A mini-review. Ann. Bot. 105, 141-153. doi: 10.1093/aob/mcp201.
45. Lapoussière, A., Michel, C., Starr, M., Gosselin, M., and Poulin, M. (2011). Role of free-living and particle-attached bacteria in the recycling and export of organic material in the Hudson Bay system. J. Mar. Syst. 88, 434-445. doi: 10.1016/j.jmarsys.2010.12.003.
46. Laurion, I., and Mladenov, N. (2013). Dissolved organic matter photolysis in Canadian arctic thaw ponds. Environ. Res. Lett. 8:035026. doi: 10.1088/1748-9326/8/3/035026.
47. Laurion, I., Vincent, W. F., MacIntyre, S., Retamal, L., Dupont, C., Francus, P., et al. (2010). Variability in greenhouse gas emissions from permafrost thaw ponds. Limnol. Oceanogr. 55, 115-133. doi: 10.4319/lo.2010.55.1.0115.
48. Lindström, E. S., Agterveld, M. P. K., and Zwart, G. (2005). Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl. Environ. Microbiol. 71, 8201-8206. doi: 10.1128/AEM.71.12.8201.
49. Lindström, E. S., and Leskinen, E. (2002). Do neighboring lakes share common taxa of bacterioplankton? Comparison of 16S rDNA fingerprints and sequences from three geographic regions. Microb. Ecol. 44, 1-9. doi 10.1007/s00248-002-0007-6.
50. Lozupone, C. A., and Knight, R. (2007). Global patterns in bacterial diversity. Proc. Natl. Acad. Sci. U.S.A. 104, 11436-11440. doi: 10.1073/pnas.0611525104.
51. Mohanty, S. R., Bodelier, P. L. E., and Conrad, R. (2007). Effect of temperature on composition of the methanotrophic community in rice field and forest soil. FEMS Microbiol. Ecol. 62, 24-31. doi: 10.1111/j.1574-6941.2007.00370.x.
52. Mohit, V., Archambault, P., Toupoint, N., and Lovejoy, C. (2014). Phylogenetic differences in summer attached and free-living bacterial communities in a temperate coastal lagoon, revealed via high throughput 16S rRNA gene sequencing. Appl. Environ. Microbiol. 80, 2071-2083. doi: 10.1128/AEM.02916-13.
53. Mou, X., Jacob, J., Lu, X., Robbins, S., Sun, S., and Ortiz, J. D. (2013). Diversity and distribution of free-living and particle-associated bacterioplankton in Sandusky Bay and adjacent waters of Lake Erie Western Basin. J. Great Lakes Res. 39, 352-357. doi: 10.1016/j.jglr.2013.03.014.
54. Negandhi, K., Laurion, I., Whiticar, M. J., Galand, P. E., Xu, X. M., and Lovejoy, C. (2013). Small thaw ponds: an unaccounted source of methane in the Canadian High Arctic. PLoS ONE 8:e78204. doi: 10.1371/journal.pone.0078204.
55. Newton, R. J., Jones, S. E., Eiler, A., McMahon, K. D., and Bertilsson, S. (2011). A guide to the natural history of freshwater lake bacteria. Microbiol. Mol. Biol. Rev. 75, 14-49. doi: 10.1128/MMBR.00028-10.
56. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., et al. (2013). Vegan: Community Ecology Package. Version 2.0-10. Available at: http://vegan.r-forge.r-project.org.
57. Parveen, B., Reveilliez, J.-P., Mary, I., Ravet, V., Bronner, G., Mangot, J. F., et al. (2011). Diversity and dynamics of free-living and particle-associated Betaproteobacteria and Actinobacteria in relation to phytoplankton and zooplankton communities. FEMS Microbiol. Ecol. 77, 461-476. doi: 10.1111/j.1574-6941.2011.01130.x.
58. Payette, S., Delwaide, A., Caccianiga, M., and Beauchemin, M. (2004). Accelerated thawing of subarctic peatland permafrost over the last 50 years. Geophys. Res. Lett. 31:L18208. doi: 10.1029/2004GL020358.
59. Pienitz, R., Doran, P. T., and Lamoureux, S. F. (2008). "Origin and geomorphology of lakes in the polar regions, "in Polar Lakes and Rivers: Limnology of Arctic and Antarctic Aquatic Ecosystems, eds W. F. Vincent and J. Laybourn-Parry (Oxford: Oxford University Press), 25-41.
60. Pruesse, E., Quast, C., Knittel, K., Fuchs, B., Ludwig, W., Peplies, J., et al. (2007). SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188-7196. doi: 10.1093/nar/gkm864.
61. Ptacnik, R., Solimini, A. G., Andersen, T., Tamminen, T., Brettum, P., Lepisto, L., et al. (2008). Diversity predicts stability and resource use efficiency in natural phytoplankton communities. Proc. Natl. Acad. Sci. U.S.A. 105, 5134-5138. doi: 10.1073/pnas.0708328105.
62. Qu, J. H., and Yuan, H. L. (2008). Sediminibacterium salmoneum gen. nov., sp. nov., a member of the phylum Bacteroidetes isolated from sediment of a eutrophic reservoir. Int. J. Syst. Evol. Microbiol. 58, 2191-2194. doi: 10.1099/ijs.0.65514-0.
63. Rahbek, C. (1995). The elevational gradient of species richness-a uniform pattern? Ecography 18, 200-205. doi: 10.1111/j.1600-0587.1995.tb00341.x.
64. R Core Team. (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. Available at: http://www. R-project.org/.
65. Rossi, P., Laurion, I., and Lovejoy, C. (2013). Distribution and identity of bacteria in subarctic permafrost thaw ponds. Aquat. Microb. Ecol. 69, 231-245. doi: 10.3354/ame01634.
66. 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.
67. Shade, A., Jones, S. E., and McMahon, K. D. (2008). The influence of habitat heterogeneity on freshwater bacterial community composition and dynamics. Environ. Microbiol. 10, 1057-1067. doi: 10.1111/j.1462-2920.2007.01527.x.
68. Smith, L. C., Sheng, Y., MacDonald, G. M., and Hinzman, L. D. (2005). Disappearing Arctic lakes. Science 308:1429. doi: 10.1126/science.1108142.
69. Sowers, K. R. (2009). "Methanogenesis, "in Encyclopedia of Microbiology, 3rd Edn, ed. M. Schaechter (San Diego, CA: Academic Press), 265-286.
70. Stainton, M., Capel, M. J., and Armstrong, F. A. (1977). The Chemical Analysis of Fresh Water. Winnipeg: Canadian Fisheries and Marine Service. Special Publication 25, 1-168.
71. Steven, B., Lionard, M., Kuske, C. R., and Vincent, W. F. (2013). High bacterial diversity of biological soil crusts in water tracks over permafrost in the high arctic polar desert. PLoS ONE 8:e71489. doi: 10.1371/journal.pone.0071489.
72. Taipale, S., Jones, R. I., and Tiirola, M. (2009). Vertical diversity of bacteria in an oxygen-stratified humic lake, evaluated using DNA and phospholipid analyses. Aquat. Microb. Ecol. 55, 1-16. doi: 10.3354/ame01277.
73. Tamames, J., Abellán, J. J., Pignatelli, M., Camacho, A., and Moya, A. (2010). Environmental distribution of prokaryotic taxa. BMC Microbiol. 10:85. doi: 10.1186/1471-2180-10-85.
74. Tranvik, L. J., Downing, J. A., Cotner, J. B., Loiselle, S. A., Striegl, R. G., Ballatore, T. J., et al. (2009). Lakes and reservoirs as regulators of carbon cycling and climate. Limnol. Oceanogr. 54, 2298-2314. doi: 10.4319/lo.2009.54.6_part_2.2298.
75. Trotsenko, Y. A., and Khmelenina, V. N. (2005). Aerobic methanotrophic bacteria of cold ecosystems. FEMS Microbiol. Ecol. 53, 15-26. doi: 10.1016/j.femsec.2005.02.010.
76. Van der Gucht, K., Sabbe, K., and Meester, L. D. (2001). Contrasting bacterioplankton community composition and seasonal dynamics in two neighbouring hypertrophic freshwater lakes. Environ. Microbiol. 3, 680-690. doi: 10.1046/j.1462-2920.2001.00242.x.
77. van Huissteden, J., Berrittella, C., Parmentier, F. J. W., Maximov, T. C., and Dolman, A. J. (2011). Methane emissions from permafrost thaw lakes limited by lake drainage. Nat. Clim. Change 1, 119-123. doi: 10.1038/nclimate1101.
78. Vecherskaya, M. S., Galchenko, V. F., Sokolova, E. N., and Samarkin, V. A. (1993). Activity and species composition of aerobic methanotrophic communities in tundra soils. Curr. Microbiol. 27, 181-184. doi: 10.1007/BF01576018.
79. Vincent, W. F. (2000). "Cyanobacterial dominance in the polar regions, "in The Ecology of Cyanobacteria, eds B. A. Whitton and M. Potts (Dordrecht: Kluwer Academic Publishers), 321-340.
80. Vincent, W. F., Lemay, M., Allard, M., and Wolfe, B. B. (2013). Adapting to permafrost change: a science framework. Eos Trans. Am. Geophys. Union 94, 373-375. doi: 10.1002/ppp.660.
81. Wagner, D., Lipski, A., Embacher, A., and Gattinger, A. (2005). Methane fluxes in permafrost habitats of the Lena Delta: effects of microbial community structure and organic matter quality. Environ. Microbiol. 7, 1582-1592. doi: 10.1111/j.1462-2920.2005.00849.x.
82. Walter, K. M., Smith, L. C., and Chapin, F. S. (2007). Methane bubbling from northern lakes: present and future contributions to the global methane budget. Philos. Trans. A Math. Phys. Eng. Sci. 365, 1657-1676. doi: 10.1098/rsta.2007.2036.
83. Walter, K. M., Zimov, S. A., Grosse, G., Jones, M. C., Anthony, P. M., Chapin, F. S., et al. (2014). A shift of thermokarst lakes from carbon sources to sinks during the Holocene epoch. Nature 511, 452-456. doi: 10.1038/nature13560.
84. Wartiainen, I., Hestnes, A. G., and Svenning, M. M. (2003). Methanotrophic diversity in high arctic wetlands on the islands of Svalbard (Norway)-denaturing gradient gel electrophoresis analysis of soil DNA and enrichment cultures. Can. J. Microbiol. 49, 602-612. doi: 10.1139/w03-080.
85. Watanabe, S., Laurion, I., Chokmani, K., Pienitz, R., and Vincent, W. F. (2011). Optical diversity of thaw ponds in discontinuous permafrost: a model system for water color analysis. J. Geophys. Res. 116:G02003. doi: 10.1029/2010JG001380.
86. Will, C., Thürmer, A., Wollherr, A., Nacke, H., Herold, N., Schrumpf, M., et al. (2010). Horizon-specific bacterial community composition of German grassland soils, as revealed by pyrosequencing-based analysis of 16S rRNA genes. Appl. Environ. Microbiol. 76, 6751-6759. doi: 10.1128/AEM.01063-10.
87. Xie, H., Bélanger, S., Demers, S., Vincent, W. F., and Papakyriakou, T. N. (2009). Photobiogeochemical cycling of carbon monoxide in the southeastern Beaufort Sea in spring and autumn. Limnol. Oceanogr. 54, 234-249. doi: 10.4319/lo.2009.54.1.0234.
88. Yannarell, A. C., and Triplett, E. W. (2004). Within-and between-lake variability in the composition of bacterioplankton communities: investigations using multiple spatial scales. Appl. Environ. Microbiol. 70, 214-223. doi: 10.1128/AEM.70.1.214.