Abstract
The fate of the carbon stocked in permafrost following global warming and permafrost thaw is of major concern in view of the potential for increased CH4 and CO2 emissions from these soils. Complex carbon compound degradation and greenhouse gas emissions are due to soil microbial communities, but no comprehensive study has yet addressed their composition and functional potential in permafrost. Here, a 2-m deep permafrost sample and its overlying active layer soil were subjected to metagenomic sequencing, quantitative PCR (qPCR) and microarray analyses. The active layer soil and the 2-m permafrost microbial community structures were very similar, with Actinobacteria being the dominant phylum. The two samples also possessed a highly similar spectrum of functional genes, especially when compared with other already published metagenomes. Key genes related to methane generation, methane oxidation and organic matter degradation were highly diverse for both samples in the metagenomic libraries and some (for example, pmoA) showed relatively high abundance in qPCR assays. Genes related to nitrogen fixation and ammonia oxidation, which could have important roles following climatic change in these nitrogen-limited environments, showed low diversity but high abundance. The 2-m permafrost showed lower abundance and diversity for all the assessed genes and taxa. Experimental biases were also evaluated using qPCR and showed that the whole-community genome amplification technique used caused representational biases in the metagenomic libraries by increasing the abundance of Bacteroidetes and decreasing the abundance of Actinobacteria. This study describes for the first time the detailed functional potential of permafrost-affected soils.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
Accession codes
References
Abulencia CB, Wyborski DL, Garcia JA, Podar M, Chen W, Chang SH et al. (2006). Environmental whole-genome amplification to access microbial populations in contaminated sediments. Appl Environ Microbiol 72: 3291–3301.
Bae S, Wuertz S . (2009). Discrimination of viable and dead fecal Bacteroidales with PMA-qPCR. Appl Environ Microbiol 75: 2940–2944.
Bodelier PLE, Kamst M, Meima-Franke M, Stralis-Pavese N, Bodrossy L . (2009). Whole-community genome amplification (WCGA) leads to compositional bias in methane-oxidizing communities as assessed by pmoA-based microarray analyses and QPCR. Environ Microbiol Rep 1: 434–441.
Edgar R, Domrachev M, Lash AE . (2002). Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucl Acids Res 30: 207–210.
Ganzert L, Jurgens G, Munster U, Wagner D . (2007). Methanogenic communities in permafrost-affected soils of the Laptev Sea coast, Siberian Arctic, characterized by 16S rRNA gene fingerprints. FEMS Microbiol Ecol 59: 476–488.
Gilichinsky DA, Wilson GS, Friedmann EI, McKay CP, Sletten RS, Rivkina EM et al. (2007). Microbial populations in Antarctic permafrost: biodiversity, state, age, and implication for astrobiology. Astrobiology 7: 275–311.
Gomez-Alvarez V, Teal TK, Schmidt TM . (2009). Systematic artifacts in metagenomes from complex microbial communities. ISME J 3: 1314–1317.
Hoj L, Rusten M, Haugen LE, Olsen RA, Torsvik VL . (2006). Effects of water regime on archaeal community composition in Arctic soils. Environ Microbiol 8: 984–996.
Johnson SS, Hebsgaard MB, Christensen TR, Mastepanov M, Nielsen R, Munch K et al. (2007). Ancient bacteria show evidence of DNA repair. Proc Natl Acad Sci USA 104: 14401–14405.
Juck DF, Whissell G, Steven B, Pollard W, McKay CP, Greer CW et al. (2005). Utilization of fluorescent microspheres and a green fluorescent protein-marked strain for assessment of microbiological contamination of permafrost and ground ice core samples from the Canadian High Arctic. Appl Environ Microbiol 71: 1035–1041.
Kobabe S, Wagner D, Pfeiffer EM . (2004). Characterisation of microbial community composition of a Siberian tundra soil by fluorescence in situ hybridisation. FEMS Microbiol Ecol 50: 13–23.
Lawrence DM, Slater AG . (2005). A projection of severe near-surface permafrost degradation during the 21st century. Geophys Res Lett 32: L24401.
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW et al. (2006). Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806–809.
Liebner S, Harder J, Wagner D . (2008). Bacterial diversity and community structure in polygonal tundra soils from Samoylov Island, Lena Delta, Siberia. Int Microbiol 11: 195–202.
Liebner S, Wagner D . (2007). Abundance, distribution and potential activity of methane oxidizing bacteria in permafrost soils from the Lena Delta, Siberia. Environ Microbiol 9: 107–117.
Mack MC, Schuur EAG, Bret-Harte MS, Shaver GR, Chapin FS . (2004). Ecosystem carbon storage in Arctic tundra reduced by long-term nutrient fertilization. Nature 431: 440–443.
Martineau C, Whyte LG, Greer CW . (2010). Stable isotope probing analysis of the diversity and activity of methanotrophic bacteria in soils from the Canadian high Arctic. Appl Environ Microbiol Accepted pending revision.
Meyer F, Paarmann D, D′Souza M, Olson R, Glass EM, Kubal M et al. (2008). The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9: 386.
Nocker A, Sossa-Fernandez P, Burr MD, Camper AK . (2007). Use of propidium monoazide for live/dead distinction in microbial ecology. Appl Environ Microbiol 73: 5111–5117.
Pinard R, de Winter A, Sarkis GJ, Gerstein MB, Tartaro KR, Plant RN et al. (2006). Assessment of whole genome amplification-induced bias through high-throughput, massively parallel whole genome sequencing. BMC Genomics 7: 216.
Ping CL, Michaelson GJ, Jorgenson MT, Kimble JM, Epstein H, Romanovsky VE et al. (2008). High stocks of soil organic carbon in the North American Arctic region. Nat Geosci 1: 615–619.
Pisz JM, Lawrence JR, Schafer AN, Siciliano SD . (2007). Differentiation of genes extracted from non-viable versus viable micro-organisms in environmental samples using ethidium monoazide bromide. J Microbiol Meth 71: 312–318.
Post WM, Emanuel WR, Zinke PJ, Stangenberger AG . (1982). Soil carbon pools and world life zones. Nature 298: 156–159.
Rivkina E, Shcherbakova V, Laurinavichius K, Petrovskaya L, Krivushin K, Kraev G et al. (2007). Biogeochemistry of methane and methanogenic archaea in permafrost. FEMS Microbiol Ecol 61: 1–15.
Shaver GR, Chapin FS . (1980). Response to fertilization by various plant-growth forms in an Alaskan tundra—nutrient accumulation and growth. Ecology 61: 662–675.
Steven B, Briggs G, McKay CP, Pollard WH, Greer CW, Whyte LG . (2007). Characterization of the microbial diversity in a permafrost sample from the Canadian high Arctic using culture-dependent and culture-independent methods. FEMS Microbiol Ecol 59: 513–523.
Steven B, Leveille R, Pollard WH, Whyte LG . (2006). Microbial ecology and biodiversity in permafrost. Extremophiles 10: 259–267.
Steven B, Niederberger TD, Whyte LG . (2009). Bacterial and archaeal diversity in permafrost. In: Margesin R (ed). Permafrost Soils. Springer-Verlag: Berlin. pp 59–72.
Steven B, Pollard WH, Greer CW, Whyte LG . (2008). Microbial diversity and activity through a permafrost/ground ice core profile from the Canadian high Arctic. Environ Microbiol 10: 3388–3403.
Trotsenko YA, Khmelenina VN . (2005). Aerobic methanotrophic bacteria of cold ecosystems. FEMS Microbiol Ecol 53: 15–26.
Wagner D . (2008). Microbial communities and processes in Arctic permafrost environments. In: Dion P, Nautiyal CS (eds). Microbiology of Extreme Soils. Springer-Verlag: Berlin. pp 133–154.
Wagner D, Gattinger A, Embacher A, Pfeiffer EM, Schloter M, Lipski A . (2007). Methanogenic activity and biomass in Holocene permafrost deposits of the Lena Delta, Siberian Arctic and its implication for the global methane budget. Glob Change Biol 13: 1089–1099.
Wagner D, Kobabe S, Liebner S . (2009). Bacterial community structure and carbon turnover in permafrost-affected soils of the Lena Delta, northeastern Siberia. Can J Microbiol 55: 73–83.
Wagner D, Lipski A, Embacher A, 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.
Willerslev E, Hansen AJ, Rønn R, Brand TB, Barnes I, Wiuf C et al. (2004). Long-term persistence of bacterial DNA. Current Biol 14: R9–R10.
Williams PJ, Smith MW . (1989). The Frozen Earth: Fundamentals of Geocryobiology. Cambridge University Press: Cambridge, 306pp.
Yergeau E, Arbour M, Brousseau R, Juck D, Lawrence JR, Masson L et al. (2009a). Microarray and real-time PCR analyses of the responses of high Arctic soil bacteria to hydrocarbon pollution and bioremediation treatments. Appl Environ Microbiol 75: 6258–6267.
Yergeau E, Newsham KK, Pearce DA, Kowalchuk GA . (2007). Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environ Microbiol 9: 2670–2682.
Yergeau E, Schoondermark-Stolk SA, Brodie EL, Déjean S, DeSantis TZ, Gonçalves O et al. (2009b). Environmental microarray analyses of Antarctic soil microbial communities. ISME J 3: 340–351.
Acknowledgements
Etienne Yergeau was supported by a NSERC postdoctoral research fellowship.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supplementary Information accompanies the paper on The ISME Journal website
Supplementary information
Rights and permissions
About this article
Cite this article
Yergeau, E., Hogues, H., Whyte, L. et al. The functional potential of high Arctic permafrost revealed by metagenomic sequencing, qPCR and microarray analyses. ISME J 4, 1206–1214 (2010). https://doi.org/10.1038/ismej.2010.41
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2010.41
Keywords
This article is cited by
-
Permafrost microbial communities and functional genes are structured by latitudinal and soil geochemical gradients
The ISME Journal (2023)
-
Effects of Alpine Grassland Degradation on Soil Microbial Communities in Qilian Mountains of China
Journal of Soil Science and Plant Nutrition (2023)
-
Vertical distribution patterns and drivers of soil bacterial communities across the continuous permafrost region of northeastern China
Ecological Processes (2022)
-
In-depth characterization of denitrifier communities across different soil ecosystems in the tundra
Environmental Microbiome (2022)
-
Soil degradation influences soil bacterial and fungal community diversity in overgrazed alpine meadows of the Qinghai-Tibet Plateau
Scientific Reports (2021)
