Advertisement

Prokaryotic community in Pleistocene ice wedges of Mammoth Mountain

  • Andrey RakitinEmail author
  • Aleksey Beletsky
  • Andrey Mardanov
  • Natalya Surgucheva
  • Vladimir Sorokin
  • Mariya Cherbunina
  • Anatoli Brouchkov
  • Andrey Mulyukin
  • Svetlana Filippova
Original Paper
  • 26 Downloads

Abstract

Ice wedges differ from other types of surface and underground glacial bodies and are widely spread in perennially frozen sub-Arctic regions, but the bacterial and archaeal diversity in these permafrost features remains poorly studied. Here, we compared the prokaryotic community composition in the active layer and ancient, 13–19 kyr BP and ~ 40 kyr BP, ice wedge horizons from the same exposure profile of the Mammoth Mountain, using pyrosequencing 16S rRNA gene. The most abundant OTUs in the active layer were affiliated with Acidobacteria (31.81%) followed by Actinobacteria (18.29%), Proteobacteria (18.14%), Gemmatimonadetes (7.3%), Parcubacteria (7.13%) and Bacteroidetes (6.49%). The prokaryotic community in 13–19 kyr BP ice wedge differed at the phylum level by the predominance of Actinobacteria (29.15%) over Acidobacteria (19.52%), Proteobacteria (18.45%), Verrumicrobia (5.88%), Firmicutes (2.98%) and Gemmatimonadetes (2.87%). In contrast, the oldest (~ 40 kyr BP) ice wedge prokaryotic community was rather poor, and only three phyla Firmicutes (54.48%), Proteobacteria (31.42%) and Bacteroidetes (7.92%) constituted the major fraction of reads. Archaeal sequences contributed with no more than 0.6% to total reads in all studied samples. Apparently, the Mammoth Mountain exposure profile harbors insular microbial communities with specific structure that reflects the stratigraphy, properties and age.

Keywords

Microbial community Pyrosequencing Ice wedge Permafrost Mammoth mountain 

Notes

Acknowledgements

This study was supported by funding from the Russian Federation Ministry of Higher Education within the State assignment to Research Center of Biotechnology of the Russian Academy of Sciences.

Supplementary material

792_2019_1138_MOESM1_ESM.docx (115 kb)
Supplementary file1 (DOCX 114 kb)
792_2019_1138_MOESM2_ESM.docx (189 kb)
Supplementary file2 (DOCX 188 kb)
792_2019_1138_MOESM3_ESM.docx (21 kb)
Supplementary file3 (DOCX 21 kb)
792_2019_1138_MOESM4_ESM.docx (15 kb)
Supplementary file4 (DOCX 14 kb)
792_2019_1138_MOESM5_ESM.docx (16 kb)
Supplementary file5 (DOCX 15 kb)
792_2019_1138_MOESM6_ESM.docx (15 kb)
Supplementary file6 (DOCX 14 kb)

References

  1. Abyzov SN, Duxbury S, Bobin NE, Fukuchi M, Hoover RB, Kanda H, Mitskevich IN, Mulyukin AL, Naganuma T, Poglazova MN, Inanov MV (2006) Super-long anabiosis of ancient microorganisms in ice and terrestrial models for development of methods to search for life on Mars. Europa and other planetary bodies. Adv Space Res 38:1191–1197.  https://doi.org/10.1016/j.asr.2005.05.034 CrossRefGoogle Scholar
  2. Belova SE, Ravin NV, Pankratov TA, Rakitin AL, Ivanova AA, Beletsky AV, Mardanov AV, Sinninghe Damsté JS, Dedysh SN (2018) Hydrolytic capabilities as a key to environmental success: chitinolytic and cellulolytic Acidobacteria from acidic sub-arctic soils and boreal peatlands. Front Microbiol 9:2775.  https://doi.org/10.3389/fmicb.2018.02775 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Brouchkov A, Kabilov M, Filippova S, Baturina O, Rogov V, Galchenko V, Mulyukin A, Fursova O, Pogorelko G (2017) Bacterial community in ancient permafrost alluvium at the Mammoth Mountain (Eastern Siberia). Gene 636:48–53.  https://doi.org/10.1016/j.gene.2017.09.021 CrossRefPubMedGoogle Scholar
  4. Dedysh SN, Sinninghe Damsté JS (2018) Acidobacteria. In: eLS. John Wiley & Sons, Ltd., pp 1–10. https://doi.org/10.1002/9780470015902.a0027685
  5. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461.  https://doi.org/10.1093/bioinformatics/btq461 CrossRefGoogle Scholar
  6. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200.  https://doi.org/10.1093/bioinformatics/btr381 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Caporaso JG (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci USA 109:21390–21395.  https://doi.org/10.1073/pnas.1215210110 CrossRefPubMedGoogle Scholar
  8. Filippova SN, Surgucheva NA, Sorokin VV, My Cherbunina, Karnysheva EA, Brushkov AV, Galchenko VF (2014) Diversity of bacterial forms in ice wedge of the Mamontova Gora glacial complex (central Yakutiya). Microbiology 83:225–235.  https://doi.org/10.1134/S0026261714020076 CrossRefPubMedGoogle Scholar
  9. Filippova SN, Surgucheva NA, Kolganova TV, Cherbunina MYu, Brushkov AV, Mulyukin AL, Galchenko VF (2019) Isolation and identification of bacteria from ice wedge of the Mamontova Gora glacial complex (central Yakutiya). Biol Bull 46:234–241.  https://doi.org/10.1134/S1062359019030026 CrossRefGoogle Scholar
  10. Friedmann EI (1994) Permafrost as microbial habitat. In: Gilichinsky DA (ed) Viable microorganisms in permafrost. Russian Academy of Sciences, Pushchino Reseach Centre, Pushchino, pp 21–26Google Scholar
  11. Fritz M, Opel T, Tanski G, Herzschuh U, Meyer H, Eulenburg A, Lantuit H (2015) Dissolved organic carbon (DOC) in Arctic ground ice. Cryosphere 9:737–752.  https://doi.org/10.5194/tc-9-737-2015 CrossRefGoogle Scholar
  12. Gilichinsky DA (2002) Permafrost model of extraterrestrial habitat. In: Horneck G, Baumstark-Khan C (eds) Astrobiology. The quest for the conditions of life. Springer, Heidelberg, Berlin, pp 125–142. https://doi.org/10.1007/978-3-642-59381-9_9 CrossRefGoogle Scholar
  13. Gilichinsky DA, Khlebnikova GM, Zvyagintsev DG, Fedorov-Davydov DG, Kudryavtseva NN (1989) Microbiology of sedimentary materials in the permafrost zone. Int Geol Rev 31:847–858.  https://doi.org/10.1080/00206818909465938 CrossRefGoogle Scholar
  14. Gilichinsky D, Vishnivetskaya T, Petrova M, Spirina E, Mamykin V, Rivkina E (2008) Bacteria in the permafrost. In: Margesin R, Schinner F, Marx JC, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Heidelberg, Berlin, pp 83–102. https://doi.org/10.1007/978-3-540-74335-4_6 CrossRefGoogle Scholar
  15. Harris SA, Brouchkov A, Guodong C (2017) Ice-wedges. Primary and secondary wedges. Part II Permafrost landforms. In: Geocryology. Characteristics and use of frozen ground and permafrost landforms. CRC Press/Balkema, Leiden, pp 153–156. https://doi.org/10.4324/9781315166988 CrossRefGoogle Scholar
  16. Ivanova TI, Kuzmina NP, Chevychelov AP (2008) The number of microorganisms and the microbiological activity of human-modified cryogenic pale soils of Yakutia. Eurasian Soil Sci 41:1213–1220.  https://doi.org/10.1134/S1064229308110100 CrossRefGoogle Scholar
  17. Juck DF, Whissell G, Steven B, Pollard W, McKay CP, Greer CW, Whyte LG (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.  https://doi.org/10.1128/AEM.71.2.1035-1041.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Kaszubkiewicz J, Wilczewski W, Novák TJ, Woźniczka P, Faliński K, Belowski J, Kawałko D (2017) Determination of soil grain size composition by measuring apparent weight of floats submerged in suspension. Int Agrophys 31:61–72.  https://doi.org/10.1515/intag-2016-0027 CrossRefGoogle Scholar
  19. Katayama T, Tanaka M, Moriizumi J, Nakamura T, Brouchkov A, Douglas TA, Fukuda M, Tomita F, Asano K (2007) Phylogenetic analysis of bacteria preserved in a permafrost ice wedge for 25,000 years. Appl Environ Microbiol 73:2360–2363.  https://doi.org/10.1128/AEM.01715-06 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Khlebnikova GM, Gilichinsky DA, Fedorov-Davydov DC, Vorobyova EA (1990) Quantitative evaluation of microorganisms in permafrost deposits and buried soils. Mikrobiology 59:106–112Google Scholar
  21. Kielak AM, Barreto CC, Kowalchuk GA, van Veen JA, Kuramae EE (2016) The ecology of Acidobacteria: moving beyond genes and genomes. Front Microbiol 7:744.  https://doi.org/10.3389/fmicb.2016.00744 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kim HM, Jung JY, Yergeau E, Hwang CY, Hinzman L, Nam S, Hong SG, Kim OS, Chun J, Lee YK (2014) Bacterial community structure and soil properties of a subarctic tundra soil in Council, Alaska. FEMS Microbiol Ecol 89:465–475.  https://doi.org/10.1111/1574-6941.12362 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lacelle D, Radtke K, Clark ID, Fisher D, Lauriol B, Utting N, Whyte LG (2011) Geomicrobiology and occluded O2–CO2–Ar gas analyses provide evidence of microbial respiration in ancient terrestrial ground ice. Earth Planet Sci Lett 306:46–54.  https://doi.org/10.1016/j.epsl.2011.03.023 CrossRefGoogle Scholar
  24. Mackelprang R, Burkert A, Haw M, Mahendrarajah T, Conaway CH, Douglas TA, Waldrop MP (2017) Microbial survival strategies in ancient permafrost: insights from metagenomics. ISME J 11:2305–2318.  https://doi.org/10.1038/ismej.2017.93 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Madden TL, Tatusov RL, Zhang J (1996) Applications of network BLAST server. Method Enzymol 266:131–141.  https://doi.org/10.1016/S0076-6879(96)66011-X CrossRefGoogle Scholar
  26. Männistö MK, Kurhela E, Tiirola M, Häggblom MM (2013) Acidobacteria dominate the active bacterial communities of Arctic tundra with widely divergent winter-time snow accumulation and soil temperatures. FEMS Microbiol Ecol 84:47–59.  https://doi.org/10.1111/1574-6941.12035 CrossRefPubMedGoogle Scholar
  27. Margesin R, Schinner F (1997) Efficiency of indigenous and inoculated cold-adapted microorganisms for biodegradation of diesel oil in alpine soils. Appl Environ Microbiol 63:2660–2664PubMedPubMedCentralGoogle Scholar
  28. Pankratov TA (2012) Acidobacteria in microbial communities of the bog and tundra lichens. Microbiology 81:51–58.  https://doi.org/10.1134/S0026261711060166 CrossRefGoogle Scholar
  29. Petrova M, Kurakov A, Shcherbatova N, Mindlin S (2014) Genetic structure and biological properties of the first ancient multiresistance plasmid pKLH80 isolated from a permafrost bacterium. Microbiology 160:2253–2263.  https://doi.org/10.1099/mic.0.079335-0 CrossRefPubMedGoogle Scholar
  30. Pikuta EV, Marsic D, Bej A, Tang J, Krader P, Hoover RB (2005) Carnobacterium pleistocenium sp. nov., a novel psychrotolerant, facultative anaerobe isolated from permafrost of the Fox Tunnel in Alaska. Int J Syst Evol Microbiol 55:473–478.  https://doi.org/10.1099/ijs.0.63384-0 CrossRefPubMedGoogle Scholar
  31. Prosser JI, Head IM, Stein LY (2014) The family Nitrosomonadaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Alphaproteobacteria and Betaproteobacteria, 4th Edition. Springer, Heidelberg, New York, Dordrecht, London, pp 901–918. https://doi.org/10.1007/978-3-642-30197-1
  32. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596.  https://doi.org/10.1093/nar/gks1219 CrossRefPubMedGoogle Scholar
  33. Rivkina E, Petrovskaya L, Vishnivetskaya T, Krivushin K, Shmakova L, Tutukina M, Meyers A, Kondrashov F (2016) Metagenomic analyses of the late Pleistocene permafrost—additional tools for reconstruction of environmental conditions. Biogeosciences 13:12091–12119.  https://doi.org/10.5194/bg-13-2207-2016 CrossRefGoogle Scholar
  34. Schirrmeister L, Grosse G, Wetterich S, Overduin PP, Strauss J, Schuur EAG, Hubberten HW (2011) Fossil organic matter characteristics in permafrost deposits of the northeast Siberian. J Geophys Res-Biogeo 116:2.  https://doi.org/10.1029/2011JG001647 CrossRefGoogle Scholar
  35. Schirrmeister L, Froese D, Tumskoy V, Grosse G, Wetterich S (2013) Yedoma: Late Pleistocene ice-rich syngenetic permafrost of Beringia. In: Elias S, Mock C, Murton J (eds) Encyclopedia of quaternary science. 2nd edition. Permafrost and periglacial features. Elsevier, Amsterdam, pp 542–552. https://doi.org/10.1016/B978-0-444-53643-3.00106-0 CrossRefGoogle Scholar
  36. Schloss PD, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541.  https://doi.org/10.1128/AEM.01541-09 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Skladnev DA, Mulyukin AL, Filippova SN, Kulikov EE, Letarova MA, Yuzbasheva EA, Karnysheva EA, Brushkov AV, Galchenko VF (2016) Modeling of dissemination of microbial cells and phages from the sites of permafrost thawing. Microbiology 85:614–619.  https://doi.org/10.1134/S0026261716050167 CrossRefGoogle Scholar
  38. Spielmeyer WK, McMeekin TA, Miller JM, Franzmann PD (1993) Phylogeny of the Antarctic bacterium Carnobacterium alterfundicum. Polar Biol 13:501–503.  https://doi.org/10.1007/BF00233142 CrossRefGoogle Scholar
  39. Spring S, Merkhoffer B, Weiss N, Kroppenstedt RM, Hippe H, Stackebrandt E (2003) Characterization of novel psychrophilic clostridia from an Antarctic microbial mat: description of Clostridium frigoris sp. nov., Clostridium lacusfryxellense sp. nov., Clostridium bowmanii sp. nov. and Clostridium psychrophilum sp. nov. and reclassification of Clostridium laramiense as Clostridium estertheticum subsp. laramiense subsp. nov. Int J Syst Evol Microbiol 53:1019–1029.  https://doi.org/10.1099/ijs.0.02554-0 CrossRefPubMedGoogle Scholar
  40. 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.  https://doi.org/10.1111/j.1462-2920.2008.01746.x CrossRefPubMedGoogle Scholar
  41. Toju H, Tanabe AS, Yamamoto S, Sato H (2012) High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS ONE 7:e40863.  https://doi.org/10.1371/journal.pone.0040863 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Vasil'chuk YK (2013) Syngenetic ice wedges: Cyclical formation, radiocarbon age and stable isotope records. Permafrost Periglac 24:82–93.  https://doi.org/10.1002/ppp.1764 CrossRefGoogle Scholar
  43. Vasil'chuk YK, Kim J-Ch, Vasil'chuk AC (2004) AMS14C dating and stable isotope plots of Late Pleistocene ice-wedge ice. Nucl Instrum Meth B 223:650–654.  https://doi.org/10.1016/j.nimb.2004.04.120 CrossRefGoogle Scholar
  44. Vishnivetskaya TA, Petrova MA, Urbance J, Ponder M, Moyer CL, Gilichinsky DA, Tiedje JM (2006) Bacterial community in ancient Siberian permafrost as characterized by culture and culture-independent methods. Astrobiology 6:400–414.  https://doi.org/10.1089/ast.2006.6.400 CrossRefPubMedGoogle Scholar
  45. Vorobyova Soina V, Gorlenko M, Minkovskaya N, Zalinova N, Mamukelashvili A, Gilichinsky DA, Rivkina E, Vishnivetskaya T (1997) The deep cold biosphere: facts and hypothesis. FEMS Microbiol Rev 20:277–290.  https://doi.org/10.1111/j.1574-6976.1997.tb00314.x CrossRefGoogle Scholar
  46. Wang QG, Garrity M, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267.  https://doi.org/10.1128/AEM.00062-07 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Wilhelm RC, Radtke KJ, Mykytczuk NC, Greer CW, Whyte LG (2012) Life at the wedge: the activity and diversity of arctic ice wedge microbial communities. Astrobiology 12:347–360.  https://doi.org/10.1089/ast.2011.0730 CrossRefPubMedGoogle Scholar
  48. Yang S, Xi Wen, Jin H, Wu Q (2012) Pyrosequencing investigation into the bacterial community in permafrost soils along the China-Russia crude oil pipeline (CRCOP). PLoS ONE 7:e52730.  https://doi.org/10.1371/journal.pone.0052730 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Yergeau E, Hogues H, Whyte LG, Greer CW (2010) The functional potential of high Arctic permafrost revealed by metagenomic sequencing, qPCR and microarray analyses. ISME J 4:1206–1214.  https://doi.org/10.1038/ismej.2010.41 CrossRefPubMedGoogle Scholar
  50. Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89:670–679.  https://doi.org/10.1002/bit.20347 CrossRefPubMedGoogle Scholar
  51. Yu Z, Gunn L, Brennan E, Reid R, Wall PG, Gaora PÓ, Hurley D, Bolton D, Fanning S (2016) Complete genome sequence of Clostridium estertheticum DSM 8809, a microbe identified in spoiled vacuum packed beef. Front Microbiol 11:1764.  https://doi.org/10.3389/fmicb.2016.01764 CrossRefGoogle Scholar
  52. Yuzbasheva EYu, Yuzbashev TV, Gvilava IT, Sineoky SP (2012) Protein display on the Yarrowia lipolytica yeast cell surface using the cell wall protein YlPir1. Appl Biochem Microbiol 48:650–655.  https://doi.org/10.1134/S0003683812070058 CrossRefGoogle Scholar
  53. Zhang DC, Brouchkov A, Griva G, Schinner F, Margesin R (2013) Isolation and characterization of bacteria from ancient Siberian permafrost sediment. Biology 2:85–106.  https://doi.org/10.3390/biology2010085 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Zinjarde S, Apte M, Mohite P, Kumar AR (2014) Yarrowia lipolytica and pollutants: interactions and applications. Biotechnol Adv 32(5):920–933CrossRefGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Andrey Rakitin
    • 1
    Email author
  • Aleksey Beletsky
    • 1
  • Andrey Mardanov
    • 1
  • Natalya Surgucheva
    • 2
  • Vladimir Sorokin
    • 2
  • Mariya Cherbunina
    • 3
  • Anatoli Brouchkov
    • 3
    • 4
  • Andrey Mulyukin
    • 2
  • Svetlana Filippova
    • 2
  1. 1.Institute of Bioengineering, Research Center of BiotechnologyRussian Academy of SciencesMoscowRussia
  2. 2.Winogradsky Institute of Microbiology, Research Center of BiotechnologyRussian Academy of SciencesMoscowRussia
  3. 3.Moscow State UniversityMoscowRussia
  4. 4.Tyumen State UniversityTyumenRussia

Personalised recommendations