Organic carbon and microbiome in tundra and forest–tundra permafrost soils, southern Yamal, Russia

  • Ivan Alekseev Faculty of Biology, Department of Applied Ecology, Saint Petersburg State University, Saint Petersburg, Russia https://orcid.org/0000-0002-0512-3849
  • Aleksei Zverev Faculty of Biology, Department of Applied Ecology, Saint Petersburg State University, Saint Petersburg, Russia; All-Russian Research Institute for Agricultural Microbiology, Saint Petersburg, Russia
  • Evgeny Abakumov Faculty of Biology, Department of Applied Ecology, Saint Petersburg State University, Saint Petersburg, Russia https://orcid.org/0000-0002-5248-9018
Keywords: Arctic ecosystems, climate change, pedogenesis, soil organic carbon, soil microbial communities, Yamal Peninsula

Abstract

Permafrost soils differ significantly from other soils because they serve as a huge reservoir for organic carbon accumulated during the Quaternary Period, which is at risk of being released as the Arctic warms. This study aimed to characterize existing carbon pools, delineate possible mineralization risks of soil organic matter and assess microbial communities in the tundra and forest–tundra permafrost soils of the southern Yamal region of Russia. The profile distribution of carbon, nitrogen and the C:N ratio showed non-gradual changes with depth due to the manifestation of cryopedogenesis in soil profiles, which lead to cryogenic mass transfer. Mean carbon stocks for the study area were 7.85 ± 2.24 kg m−2 (0–10 cm layer), 14.97 ± 5.53 kg m−2 (0–30 cm) and 23.99 ± 8.00 kg m−2 (0–100 cm). The analysis of the humus type revealed a predominance of fulvic type and low-molecular-weight fragments in the fulvic acid fraction, which indicates high mineralization risk of humic substances under Arctic warming conditions. The taxonomic analysis of soil microbiomes revealed 48 bacterial and archaeal phyla, among which proteobacteria (27%) and actinobacteria (20%) were predominant. The pH range and nitrogen accumulation were the main environmental determinants of microbial community diversity and composition in the studied soils.

Downloads

Download data is not yet available.

References


Abakumov E. & Mukhametova N. 2014. Microbial biomass and basal respiration of selected Sub-Antarctic and Antarctic soils in the areas of some Russian polar stations. Solid Earth 5, 705–712, doi: 10.5194/se-5-705-2014.


Alekseev I. & Abakumov E. 2018. Permafrost-affected former agricultural soils of the Salekhard city (central part of Yamal region). Czech Polar Reports 8, 119–131, doi: 10.5817/CPR2018-1-9.


Alekseev I., Abakumov E., Shamilishvili G. & Lodygin E. 2016. Soderzhanie tyazhelyh metallov i uglevodorodov v počvakh naselennyh punktov Yamalo-Neneckogo avtonomnogo okruga. (Heavy metals and hydrocarbons content in soils of settlements of the Yamal-Nenets autonomous region.) Gigiyena i Sanitariya 9, 818–821.


Alekseev I., Dinkelaker N., Oripova A., Sem’ina G., Morozova A. & Abakumov E. 2017. Ocenka ekotoksikologičeskogo sostojanija počhv Polyarnogo Urala i yuzhnogo Yamala. (Assessment of ecotoxicological state of soils of the Polar Ural and southern Yamal.) Gigiyena i sanitariya 10, 941–945.


Alekseev I., Kostecki J. & Abakumov E. 2017. Vertical electrical resistivity sounding (VERS) of tundra and forest tundra soils of Yamal region. International Agrophysics 31, 1–8, doi: 10.1515/intag-2016-0037.


Alekseev I., Shamilishvilly G. & Abakumov E. 2019. Content of trace elements in selected permafrost-affected soils of Yamal region with different functional load. Polarforschung 88, 125–133, doi: 10.2312/polarforschung.88.2.125.


Alekseev I., Zverev A. & Abakumov E. 2020. Microbial communities in permafrost soils of Larsemann Hills, eastern Antarctica: environmental controls and effect of human impact. Microorganisms 8, article no. 1202, doi: 10.3390/microorganisms8081202.


Aronesty E. 2013. Comparison of sequencing utility programs. The Open Bioinformatics Journal 7, 1–8, doi: 10.2174/1875036201307010001.


Bailey V., Bolton H. & Smith J. 2008. Substrate-induced respiration and selective inhibition as measures of microbial biomass in soils. In M. Carter & E. Gregorich (eds.): Soil sampling and methods of analysis. Pp. 515–527. Boca Raton, FL: CRC Press.


Bates S.T., Berg-Lyons D., Caporaso J.G., Walters W.A., Knight R. & Fierer N. 2010. Examining the global distribution of dominant archaeal populations in soil. ISME Journal 5, 908–917, doi: 10.1038/ismej.2010.171.


Bolger A.M., Lohse M. & Usadel B. 2014. Trimmomatic, a flexible trimmer for illumina sequence data. Bioinformatics 30, 2114–2120, doi: 10.1093/bioinformatics/btu170.


Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Pena A.G., Goodrich J.K., Gordon J.I., Huttley G.A., Kelley S., Knights D., Koenig J., Ley R., Lozupone C., McDonald D., Muegge B., Pirrung M., Reeder J., Sevinsky J., Turnbaugh P., Walters W., Wildmann J., Yatsunenko T., Zaneveld J. & Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336, doi: 10.1038/nmeth.f.303.


Čestnyh O.V., Zamolodčikov D.G. & Karelin D.V. 1999. Zapasy organičeskogo ugleroda v počvakh tundrovyh i lesotundrovyh ekosistem Rossii. (Organic matter reserves in the soils of tundra and forest–tundra ecosystems of Russia.) Ecologia 6, 426–432.


Clark R.B. & Baligar V.C. 2000. Acidic and alkaline soil constraints on plant mineral nutrition. In R.E. Wilkinson (ed.): Plant–environment interactions. Pp. 133–177. New York: Marcel Dekker Inc.


DeSantis T.Z., Hugenholts P., Larsen N., Rojas M., Brodie E.L., Keller K., Dalevi D., Hu P. & Andersen G.L. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology 72, 5069–5072, doi: 10.1128/AEM.03006-05.


Dobrinskij L.N. 1995. Priroda Jamala. (Nature of Yamal.) Ekaterinburg: Nauka.


Evgrafova S. & Mukhortova L. 2015. Linking microbial community features and biodegradability of organic matter in Siberian permafrost affected soils. Ecology & Safety 9, 207–215.


FAO (Food and Agriculture Organization) 2015. World Reference Base for Soil Resources 2014. International soil classification system for naming soils and creating legends for soil maps. Update 2015. World Soil Resources Reports 106. Rome: Food and Agriculture Organization.


Fierer N. & Jackson R.B. 2006. The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America 103, 626–631, doi: 10.1073/pnas.0507535103.


Forbes B.C. & Kumpula T. 2009. The ecological role and geography of reindeer (Rangifer tarandus) in northern Eurasia. Geographical Compass 3, 1356–1380, doi: 10.1111/j.1749-8198.2009.00250.x.


Freeman C., Evans C.D., Monteith D.T., Reynolds B. & Fenner N. 2001. Export of organic carbon from peat soils. Nature 412, 785–785, doi: 10.1038/35090628.


Gillespie A.W., Sanei H., Diochon A., Ellert B.H., Regier T.Z., Chevrier D., Dynes J.J., Tarnocai C. & Gregorich E.G. 2014. Perennially and annually frozen soil carbon differ in their susceptibility to decomposition: analysis of Subarctic earth hummocks by bioassay, XANES and pyrolysis. Soil Biology and Biochemistry 68, 106–116, doi: 10.1016/j.soilbio.2013.09.021.


Goryačkin S.V. 2014. Počvenny pokrov Severa (struktura, genezis, ekologija, evoljucija). (Soil cover of the north [patterns, genesis, ecology, evolution].) Moscow: GEOS.


Gubin S.V. & Lupachev A.V. 2008. Soil formation and the underlying permafrost. Eurasian Soil Science 41, 574–585, doi: 10.1134/S1064229308060021.


Gundelwein A., Müller-Lupp T., Sommerkorn M., Haupt E.T., Pfeiffer E.M. & Wiechmann H. 2007. Carbon in tundra soils in the Lake Labaz region of Arctic Siberia. Eurasian Journal of Soil Science 58, 1164–1174, doi: 10.1111/j.1365-2389.2007.00908.x.


Hao X., Ball B., Culley J., Carter M. & Parkin G. 2008. Soil density and porosity. In M. Carter & E. Gregorich (eds.): Soil sampling and methods of analysis. Pp. 743–761. Boca Raton, FL: CRC Press.


Hugelius G. & Kuhry P. 2009. Landscape partitioning and environmental gradient analyses of soil organic carbon in a permafrost environment. Global Biogeochemical Cycles 23, GB3006, doi: 10.1029/2008GB003419.


Hugelius G., Kuhry P., Tarnocai C. & Virtanen T. 2010. Soil organic carbon pools in a periglacial landscape: a case study from the central Canadian Arctic. Permafrost and Periglacial Processes 21, 16–29, doi: 10.1002/ppp.677.


Hugelius G., Strauss J., Zubrzycki S., Harden J.W., Schuur E.A., Ping C.-L., Schirrmeister L., Grosse G., Michaelson G.J., Koven C.D., O’Donnell J.A., Elberling B., Mishra U., Camill P., Yu Z., Palmtag J. & Kuhry P. 2014. Estimated stocks of circumpolar permafrost carbon with quantified uncertainty ranges and identified data gaps. Biogeosciences 11, 6573–6593, doi: 10.5194/bg-11-6573-2014.


Kačinskij N.A. 1970. Fizika počv. (Soil physics.) Moscow: Vysšhaja škola.


Kaiser C., Fuchslueger L., Koranda M., Gorfer M., Stange C.F., Kitzler B., Rasche F., Strauss J., Sessitsch A., Zechmeister-Boltenstern S. & Richter A. 2011. Plants control the seasonal dynamics of microbial N cycling in a beech forest soil by belowground C allocation. Ecology 92, 1036–1051, doi: 10.1890/10-1011.1.


Kitrsidelli I.Y., Vlasov D.Y., Barantsevich E.P., Krylenkov V.A. & Sokolov V.T. 2014. Kompleksy mikroskopičeskih gribov v počvah i gruntah poljarnogo ostrovo Izvestija Cik (Karskoje more). (Microfungi from soil of polar Island Izvestia tsik [Kara Sea].) Mikologiya i Fitopatologiya 48, 365–371.


Köchy M., Hiederer R. & Freibauer A. 2015. Global distribution of soil organic carbon—part 1: masses and frequency distributions of SOC stocks for the tropics, permafrost regions, wetlands, and the world. Soil 1, 351–365, doi: 10.5194/soil-1-351-2015.


Kolchugina T.P., Vinston T.S., Gaston G. G. Rozhkov V.A. & Shwidenko A.Z. 1995. Carbon pools, fluxes and sequestration potential in soils of the former Soviet Union. In R. Lal (ed.): Soil management and greenhouse effect. Pp. 25–40. Boca Raton, FL: Lewis Publishers.


Koyama A., Wallenstein M.D., Simpson R.T. & Moore J.C. 2014. Soil bacterial community composition altered by increased nutrient availability in Arctic tundra soils. Frontiers in Microbiology 5, article no. 516, doi: 10.3389/fmicb.2014.00516.


Kuzyakov Y. 2011. How to link soil C pools with CO2 fluxes? Biogeosciences 8, 1523–1537, doi: 10.5194/bg-8-1523-2011.


Lantz T., Gergel S. & Henry G. 2010. Response of green alder (Alnus viridis subsp. fruticosa) patch dynamics and plant community composition to fire and regional temperature in north-western Canada. Journal of Biogeography 37, 1597–1610, doi: 10.1111/j.1365-2699.2010.02317.x.


Lauber C.L., Hamady M., Knight R. & Fierer N. 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Applied and Environmental Microbiology 75, 5111–5120, doi: 10.1128/AEM.00335-09.


Li F., Chen L., Zhang J.B., Yin J. & Huang S.M. 2017. Bacterial community structure after long-term organic and inorganic fertilization reveals important associations between soil nutrients and specific taxa involved in nutrient transformations. Frontiers in Microbiology 8, article no. 187, doi: 10.3389/fmicb.2017.00187.


Lubbe A. & Smith R.V. 2012. Field soil respiration rate on a Subantarctic Island: its relation to site characteristics and response to added C, N and P. Open Journal of Soil Science 2, 187–195, doi: 10.4236/ojss.2012.22023.


Lupachev A.V., Gubin, S.V., Veremeeva, A.A., Kaverin, D.A., Pastukhov, A.V. & Yakimov A.S. 2016. Microrelief of the permafrost table: structure and ecological functions. Kriosphera Zemli 20(2), 3–14.


Malard L., Anwar M., Jacobsen C. & Pearce D. 2019. Biogeographical patterns in soil bacterial communities across the Arctic region. FEMS Microbiology Ecology 95(9), article no. fiz128, doi: 10.1093/femsec/fiz128.


Matsuura Y. & Yefremov D.P. 1995. Carbon and nitrogen storage of soils in a forest–tundra area of northern Sakha, Russia. In K. Takahashi et al. (eds.): Proceedings of the third symposium on the joint Siberian permafrost studies between Japan and Russia in 1994. Pp. 97–101. Sapporo: Forest and Forest Products Research Unit.


Matyshak G., Bogatyreb L., Goncharova O. & Bobrik A. 2017. Specific features of the development of soils of hydromorphic ecosystems in the northern taiga of western Siberia under conditions of cryogenesis. Eurasian Soil Science 50, 1115–1124, doi: 10.1134/S1064229317100064.


McGuire A.D., Anderson L.G., Christensen T.R., Dallimore S., Guo L., Hayes D.J., Heimann M., Lorenson T.D., Macdonald R.W. & Roulet, N. 2009. Sensitivity of the carbon cycle in the Arctic to climate change. Ecological Monographs 79, 523–555, doi: 10.1890/08-2025.1.


Moore T.R. & Basiliko N. 2006. Decomposition in boreal peatlands. In R.K. Wieder & D.H. Vitt (eds.): Boreal peatland ecosystems. Pp. 125–143. Heidelberg: Springer.


Nadelhoffer K.J., Giblin A.E. & Shaver A.E. 1992. Microbial processes and plant nutrient availability in Arctic soils. In F.S. Chapin III et al. (eds.): Arctic ecosystems in a changing climate: an ecophysiological perspective. Pp. 281–300. San Diego, CA: Academic Press.


Parry M., Canziani O., Palutikof J., van der Linden P. & -Hanson C. (eds.) 2007. Climate change 2007. Impacts, adaptations and vulnerability. Working Group II contribution to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press.


Ping C.L., Michaelson G.J., Jorgenson M.T., Kimble J.M., Epstein H., Romanovsky V.E. & Walker D.A. 2008. High stocks of soil organic carbon in the North American Arctic region. Nature Geoscience 1, 615–619, doi: 10.1038/ngeo284.


Ping C.L., Michaelson G.J. & Kimble J.M. 1997. Carbon storage along a latitudinal transect in Alaska. Nutrient Cycling in Agroecosystems 49, 235–242, doi: 10.1023/A:1009731808445.


Post W.M., Emanuel W.R., Zinke P.J. & Stangenberger A.G. 1982. Soil carbon pools and world life zones. Nature 298, 156–159, doi: 10.1038/298156a0.


Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., Peplies J. & Glöckner F.O. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41(D1), D590–D596, doi: 10.1093/nar/gks1219.


Racine C., Jandt R., Meyers C. & Dennis J. 2004. Tundra fire and vegetation change along a hillslope on the Seward Peninsula, Alaska, USA. Arctic, Antarctic, and Alpine Research 36, 1–10, http://doi.org/10.1657/1523-0430.


Rognes T., Flouri T., Nichols B., Quince C. & Mahé F. 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584, doi: 10.7717/peerj.2584.


Rousk J., Baath E., Brookes P.C., Lauber C.L., Lozupone C., Caporaso J.G., Knight R. & Fierer N. 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME Journal 4, 1340–1351, doi: 10.1038/ismej.2010.58.


Schepaschenko D.G., Mukhortova L.V., Shvidenko A.Z. & Vedrova E.F. 2013. The pool of organic carbon in the soils of Russia. Eurasian Soil Science 46, 107–116, doi: 10.1134/S1064229313020129.


Schimel J.P., Reynolds J.F., Tenhunen J.D., Kielland K. & Chapin F.S. III 1996. Nutrient availability and uptake by tundra plants. In J. Reynolds & J. Tenhunen (eds.): Ecological studies analysis and synthesis: landscape function and disturbance in Arctic tundra. Pp. 203–221. New York: Springer-Verlag.


Schnitzer M. 1982. Organic matter characterization. In A.L. Page et al. (eds.): Methods of soil analysis, part 2: chemical and microbiological properties. Pp.581–594. Madison, WI: American Society of Agronomy.


Schütz K., Kandeler E., Nagel P., Scheu S. & Ruess L. 2010. Functional microbial community response to nutrient pulses by artificial groundwater recharge practice in surface soils and subsoils. FEMS Microbiology Ecology 72, 445–455, doi: 10.1111/j.1574-6941.2010.00855.x.


Shaver G.R., Bret-Harte M.S., Jones M. H., Johnstone J., Gough L. Laundre J. & Chapin F.S. III 2001. Species composition interacts with fertilizer to control long-term change in tundra productivity. Ecology 82, 3163–3181, doi: 10.1890/00129658.


Siewert M.B., Hugelius G., Heim B. & Faucherre S. 2016. Landscape controls and vertical variability of soil organic carbon storage in permafrost-affected soils of the Lena River Delta. Catena 147, 725–741, doi: 10.1016/j.catena.2016.07.048.


Šijatov S.G. & Mazepa V.S. 1995. Klimat. (Climate.) In L.N. Dobrinskij (ed.): Priroda Jamala. (Nature of Yamal.) Pp. 32–68. Ekaterinburg: Nauka.


Šišov L.L., Tonkonogov V.D., Lebedeva I.I. & Gerasimova M.I. 2004. Klassifikacija I diagnostika počv Rossii. (Classification and diagnostics of soils of Russia.) Smolensk: Oykumena.


Smith C.A.S. & Veldhuis H. 2004. Cryosols of the boreal, Subarctic, and western Cordillera regions of Canada. In J.M. Kimble (ed.): Cryosols. Permafrost-affected soils. Pp. 119–138. Berlin: Springer Verlag.


Stolbovoi V. 2002. Carbon in Russian soils. Climatic Change 55, 131–156, doi: 10.1023/A:1020289403835.


Tarnocai C., Canadell J.G., Schuur E.A.G., Kuhry P. Mazhitova G. & Zimov S. 2009. Soil organic carbon pools in the northern circumpolar permafrost region. Global Biogeochemical Cycles 23, GB2023, doi: 10.1029/2008GB003327.


Vlasov D., Abakumov E., Tomashunas V., Krylenkov V. & Zelenskaya M. 2014. Micobiota počv i antropogennyh substratov poluostrova Jamal. (Mycobiota of soil and anthropogenic substrates of the Yamal Peninsula.) Gigiena i Sanitarija 5, 49–51.


Walker D., Leibman M., Epstein H., Forbes B., Bhatt U., Raynolds M., Comiso J., Gubarkov A., Khomutov A., Gia J., Kaarlejärvi E., Kaplan J., Kumpula T., Kuss T., Matyshak G., Moskalenko N., Orekhov P., Romanovsky V., Ukraientseva N. & Yu Q. 2009. Spatial and temporal patterns of greenness on the Yamal Peninsula, Russia: interactions of ecological and social factors affecting the Arctic normalized difference vegetation index. Environmental Research Letters 4, article no. 404500, doi: 10.1088/1748-9326/4/4/045004.


Walz J., Knoblauch C., Bohme L. & Pfeiffer E.-M. 2017. Regulation of soil organic matter decomposition in permafrost-affected Siberian tundra soils—impact of oxygen availability, freezing and thawing, temperature, and labile organic matter. Soil Biology & Biochemistry 110, 34–43, doi: 10.1016/j.soilbio.2017.03.001.


Wang Q., Garrity G.M., Tiedje J.M. & Cole J.R. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 5261–5267, doi: 10.1128/AEM.00062-07.


Wolińska A., Kuźniar A., Szafranek-Nakonieczna A., Jastrzębska N., Roguska E. & Stępniewska Z. 2016. Biological activity of autochthonic bacterial community in oil-contaminated soil. Water, Air, and Soil Pollution 227, article no. 130, doi: 10.1007/s11270-016-2825-z.


Wolińska A., Gałazka A., Kuzniar A., Goraj W., Jastrzębska N., Grzadziel J. & Stepniewska Z. 2018. Catabolic fingerprinting and diversity of bacteria in Mollic Gleysol contaminated with petroleum substances. Applied Sciences 8, article no. 1970, doi: 10.3390/app8101970.


Yan Y., Kuramae E.E., Klinkhamer P.G. & van Veen J.A. 2015. Revisiting the dilution procedure used to manipulate microbial biodiversity in terrestrial systems. Applied and Environmental Microbiology 81, 4246–4252, doi: 10.1128/AEM.00958-15.


Zimov S.A., Schuur E.A.G. & Chapin F.S. III 2006. Permafrost and the global carbon budget. Science 312, 1612–1613, doi: 10.1126/science.1128908.


Zubrzycki S., Kutzbach L., Grosse G., Desyatkin A. & Pfeiffer E.-M. 2013. Organic carbon and total nitrogen stocks in soils of the Lena River Delta. Biogeosciences 10, 3507–3524, doi: 10.5194/bg-10-3507-2013.


Zubrzycki S., Kutzbach L. & Pfeiffer E.-M. 2014. Permafrost-affected soils and their carbon pools with a focus on the Russian Arctic. Solid Earth 5, 595–609, doi: 10.5194/se-5-595-2014.
Published
2021-01-08
How to Cite
Alekseev I., Zverev A., & Abakumov E. (2021). Organic carbon and microbiome in tundra and forest–tundra permafrost soils, southern Yamal, Russia. Polar Research, 40. https://doi.org/10.33265/polar.v40.5283
Section
Research Articles