Free Iron and Iron-Reducing Microorganisms in Permafrost and Permafrost-Affected Soils of Northeastern Siberia


An agreement between the content of amorphous (oxalate-extractable) iron and morphochromatic features of gley attests to the modern activity of gleyzation processes in tundra soils of the Kolyma Lowland, especially within lower parts of gentle and steep slopes. A suprapermafrost reduced gley horizon thawing out in the warmest years is considered a relic of the warmer and wetter stage of soil formation. An integrated analysis of data on the contents of mobile iron and annotated metagenomes indicates that microorganisms affiliated with the Proteobacteria phylum capable of iron reduction predominate in sediments formed under hydromorphic conditions and in modern mineral soil. In laboratory experiments, the process of microbial iron reduction was more active at 5°C than at 20°C. Therefore, it can be assumed that the majority of cultivated communities of iron-reducing bacteria have been adapted to low Arctic temperatures. Under conditions of climate warming and an increase in precipitation, permafrost temperature, and thickness of the seasonally thawed layer, iron reduction processes in the soils rich in the total iron will play an even greater role and create favorable redox conditions for the formation of methane, one of the most important greenhouse gases.

This is a preview of subscription content, access via your institution.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.


  1. 1

    E. V. Arinushkina, Manual for the Chemical Analyses of Soils (Moscow State Univ., Moscow, 1970) [in Russian].

    Google Scholar 

  2. 2

    S. V. Gubin and A. V. Lupachev, “Suprapermafrost horizons of the accumulation of raw organic matter in tundra cryozems of Northern Yakutia,” Eurasian Soil Sci. 51, 772–781 (2018).

    Article  Google Scholar 

  3. 3

    Z. V. Zonn, Iron in Soils: Genetic and Geographical Aspects (Nauka, Moscow, 1982) [in Russian].

    Google Scholar 

  4. 4

    A. V. Lupachev and S. V. Gubin, “Suprapermafrost organic–accumulative horizons in the tundra cryozems of Northern Yakutia,” Eurasian Soil Sci. 45, 45–55 (2012).

    Article  Google Scholar 

  5. 5

    E. P. Mulikovskaya, A. A. Reznikov, and I. Yu. Sokolov, Analysis of Natural Waters (Nedra, Moscow, 1970) [in Russian].

    Google Scholar 

  6. 6

    E. M. Rivkina, G. N. Kraev, K. V. Krivushin, K. S. Laurinavizhyus, D. G. Fedorov-Davydov, A. L. Kholodov, V. A. Shcherbakova, and D. A. Gilichinskii, “Methane in permafrost of the northeastern sector of Arctic,” Kriosfera Zemli 10 (3), 23–41 (2006).

    Google Scholar 

  7. 7

    D. G. Fedorov-Davydov, S. V. Gubin, and O. V. Makeev, “The content of mobile iron and gleyzation process in soils of the Kolyma Lowland,” Eurasian Soil Sci. 37, 131–142 (2004).

    Google Scholar 

  8. 8

    D. G. Fedorov-Davydov, N. S. Mergelov, and M. M. Morozov, “Soil cover of the Kolyma Lowland coastal yedomas,” in Proceedings of the International Conference “Cryogenic Resources of Polar Regions,” Salekhard, June, 2007 (Salekhard, 2007), Vol. 2, pp. 113–116.

  9. 9

    D. G. Fedorov-Davydov, S. P. Davydov, A. I. Davydova, V. E. Ostroumov, A. L. Kholodov, V. A. Sorokovikov, and D. G. Shmelev, “Temperature regime of soils of Northern Yakutia,” Kriosfera Zemli 22 (4), 15–24 (2018).

    Google Scholar 

  10. 10

    A. Abramov, S. Davydov, A. Ivashchenko, D. Karelin, A. Kholodov, G. Kraev, A. Lupachev, et al., “Two decades of active layer thickness monitoring in northeastern Asia,” Polar Geogr., 1–17 (2019).

  11. 11

    J. P. Bowman, S. A. McCammon, D. S. Nichols, J. H. Skerratt, S. M. Rea, P. D. Nichols, and T. A. McMeekin, “Shewanella gelidimarina sp. nov., Shewanella frigidimarina sp. nov., novel Antarctic species with the ability to produce eicosapentaenoic acid (20: 5ω3) and grow anaerobically by dissimilatory Fe (III) reduction,” Int. J. Syst. Evol. Microbiol. 47 (4), 1040–1047 (2005).

    Google Scholar 

  12. 12

    D. Canfield, E. Kristensen, and B. Thamdrup, Aquatic Geomicrobiology (Elsevier, Amsterdam, 2005), Vol. 48. ISBN 9780080575407

    Google Scholar 

  13. 13

    R. E. Cowart, “Reduction of iron by extracellular iron reductases: implications for microbial iron acquisition,” Arch. Biochem. Biophys. 2, 273–281 (2002).

    Article  Google Scholar 

  14. 14

    D. G. Fyodorov-Davydov, A. L. Kholodov, V. E. Ostroumov, G. N. Kraev, V. A. Sorokovikov, S. P. Davydov, and A. A. Merekalova, “Seasonal thaw of soils in the North Yakutian ecosystems,” in Proceedings of the Ninth International Conference on Permafrost, University of Alaska, Fairbanks, June 29–July 3, 2008 (Fairbanks, 2008), Vol. 1, pp. 481–486.

  15. 15

    S. Hedrich, M. Schlömann, and D. B. Johnson, “The iron-oxidizing proteobacteria,” Microbiology 157 (6), 1551–1564 (2011).

    Article  Google Scholar 

  16. 16

    F. Meyer, D. Paarmann, M. D’Souza, R. Olson, E. M. Glass, M. Kubal, T. Paczian, A. Rodriguez, R. Stevens, A. Wilke, and J. Wilkening, “The metagenomics RAST server–a public resource for the automatic phylogenetic and functional analysis of metagenomes,” BMC Bioinf. 9, 386 (2008).–2105–9–386

  17. 17

    S. L. Nixon, J. P. Telling, J. L. Wadham, and C. S. Cockel, “Viable cold-tolerant iron-reducing microorganisms in geographically diverse subglacial environments,” Biogeosciences 14 (6), 1445–1455 (2017).

    Article  Google Scholar 

  18. 18

    S. A. Pecheritsyn, E. M. Rivkina, V. N. Akimov, and V. A. Shcherbakova, “Desulfovibrio arcticus sp. nov., a psychrotolerant sulphate-reducing bacterium from a cryopeg,” Int. J. Syst. Evol. Microbiol. 62 (1), 33–37 (2012).

    Article  Google Scholar 

  19. 19

    E. Rivkina, D. Gilichinsky, S. Wagener, J. Tiedje, and J. McGrath, “Biogeochemical activity of anaerobic microorganisms from buried permafrost sediments,” Geomicrobiol. J. 15 (3), 187–193 (1998).

    Article  Google Scholar 

  20. 20

    E. Rivkina, L. Petrovskaya, T. Vishnivetskaya, K. Krivushin, L. Shmakova, M. Tutukina, A. Meyers, and F. Kondrashov, “Metagenomic analyses of the late Pleistocene permafrost-additional tools for reconstruction of environmental conditions,” Biogeosciences 13 (7), 2207–2219 (2016).

    Article  Google Scholar 

  21. 21

    Y. Ryzhmanova, T. Abashina, D. Petrova, and V. Shcherbakova, “Desulfovibrio gilichinskyi sp. nov., a cold-adapted sulfate-reducing bacterium from a Yamal Peninsula cryopeg,” Int. J. Syst. Evol. Microbiol. 69 (4), 1081–1086 (2019).

    Article  Google Scholar 

  22. 22

    T. Shi, R. H. Reeves, D. A. Gilichinsky, and E. I. Friedmann, “Characterization of viable bacteria from Siberian permafrost by 16S rDNA sequencing,” Microb. Ecol. 33 (3), 169–179 (1997).

    Article  Google Scholar 

  23. 23

    A. I. Slobodkin and J. Wiegel, “Fe (III) as an electron acceptor for H2 oxidation in thermophilic anaerobic enrichment cultures from geothermal areas,” Extremophiles 1 (2), 106–109 (1997).

    Article  Google Scholar 

  24. 24

    V. Vandieken, M. Mussmann, H. Niemann, and B. B. Jørgensen, “Desulfuromonas svalbardensis sp. nov., Desulfuromusa ferrireducens sp. nov., psychrophilic, Fe (III)–reducing bacteria isolated from Arctic sediments, Svalbard,” Int. J. Syst. Evol. Microbiol. 56 (5), 1133–1139 (2006).

    Article  Google Scholar 

  25. 25

    B. A. Ventura, F. González, A. Ballester, M. L. Blázquez, and J. A. Muñoz, “Bioreduction of iron compounds by Aeromonas hydrophila,” Int. Biodeter. Biodegrad. 103, 69–76 (2015).

    Article  Google Scholar 

  26. 26

    E. Viollier, P. W. Inglett, K. Hunter, A. N. Roychoudhury, and P. van Cappellen, “The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters,” Appl. Geochem. 15 (6), 785–790 (2000).

    Article  Google Scholar 

  27. 27

    K. A. Weber, L. A. Achenbach, and J. D. Coates, “Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction,” Nat. Rev. Microbiol. 4 (10), 752–764 (2006).

    Article  Google Scholar 

  28. 28

    E. A. Wolin, M. Wolin, and R. S. Wolfe, “Formation of methane by bacterial extracts,” J. Biol. Chem. 238 (8), 2882–2886 (1963).

    Article  Google Scholar 

  29. 29

    C. Zhang, R. D. Stapleton, J. Zhou, A. V. Palumbo, and T. J. Phelps, “Iron reduction by psychrotrophic enrichment cultures,” FEMS Microbiol. Ecol. 30 (4), 367–371 (1999).

    Article  Google Scholar 

Download references


We are grateful to A.V. Lupachev for assistance in carrying out field researches.


This study was performed within the framework of state assignment no. AAAA-A18-118013190181-6 and was supported by the Russian Foundation for Basic Research (project nos. 19-29-05003-mk and 19-04-00831) and, partly, by the National Science Foundation (grant NSF DEB-1442262).

Author information



Corresponding author

Correspondence to E. M. Rivkina.

Ethics declarations

The authors declare that they have no conflict of interest.

Additional information

Translated by T. Chicheva

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rivkina, E.M., Fedorov-Davydov, D.G., Zakharyuk, A.G. et al. Free Iron and Iron-Reducing Microorganisms in Permafrost and Permafrost-Affected Soils of Northeastern Siberia. Eurasian Soil Sc. 53, 1455–1468 (2020).

Download citation


  • iron
  • metagenome
  • microorganisms
  • iron reduction