Microbial Ecology

, Volume 78, Issue 1, pp 70–84 | Cite as

Prokaryotic Diversity and Distribution in Different Habitats of an Alpine Rock Glacier-Pond System

  • I. ManiaEmail author
  • R. Gorra
  • N. Colombo
  • M. Freppaz
  • M. Martin
  • A. M. Anesio
Environmental Microbiology


Rock glaciers (RG) are assumed to influence the biogeochemistry of downstream ecosystems because of the high ratio of rock:water in those systems, but no studies have considered the effects of a RG inflow on the microbial ecology of sediments in a downstream pond. An alpine RG-pond system, located in the NW Italian Alps has been chosen as a model, and Bacteria and Archaea 16S rRNA genes abundance, distribution and diversity have been assessed by qPCR and Illumina sequencing, coupled with geochemical analyses on sediments collected along a distance gradient from the RG inflow. RG surface material and neighbouring soil have been included in the analysis to better elucidate relationships among different habitats.

Our results showed that different habitats harboured different, well-separated microbial assemblages. Across the pond, the main variations in community composition (e.g. Thaumarchaeota and Cyanobacteria relative abundance) and porewater geochemistry (pH, DOC, TDN and NH4+) were not directly linked to RG proximity, but to differences in water depth. Some microbial markers potentially linked to the presence of meltwater inputs from the RG have been recognised, although the RG seems to have a greater influence on the pond microbial communities due to its contribution in terms of sedimentary material.


Rock glacier Alpine pond Sediments Microbial ecology 16S rRNA 



We would like to thank Danilo Godone and Davide Viglietti for their help in field work activities and laboratory analyses, and the family Beck-Peccoz, Consorzio di Miglioramento Fondiario di Gressoney (Aosta) and MonteRosa-ski for allowing the access to the study site. This study was partially financed by the UK NERC grant (NE/J02399X/1) to A. M. Anesio.

Supplementary material

248_2018_1272_MOESM1_ESM.pdf (91 kb)
ESM 1 (PDF 91 kb)
248_2018_1272_MOESM2_ESM.pdf (269 kb)
ESM 2 (PDF 268 kb)
248_2018_1272_MOESM3_ESM.pdf (124 kb)
ESM 3 (PDF 123 kb)
248_2018_1272_MOESM4_ESM.pdf (309 kb)
ESM 4 (PDF 309 kb)
248_2018_1272_MOESM5_ESM.xlsx (94 kb)
ESM 5 (XLSX 94 kb)


  1. 1.
    Barsch D (1996) Rockglaciers: indicators for the present and former geoecology in high mountain environments. Springer-Verlag, Berlin-HeidelbergCrossRefGoogle Scholar
  2. 2.
    Haeberli W, Hallet B, Arenson L, Elconin R, Humlum O, Kääb A, Kaufmann V, Ladanyi B, Matsuoka N, Springman S, Mühll V (2006) Permafrost creep and rock glacier dynamics. Permafr. Periglac. Process. 17:189–214. CrossRefGoogle Scholar
  3. 3.
    Berthling I (2011) Beyond confusion: rock glaciers as cryo-conditioned landforms. Geomorphology 131:98–106. CrossRefGoogle Scholar
  4. 4.
    Frey KE, McClelland JW (2009) Impacts of permafrost degradation on arctic river biogeochemistry. Hydrol. Process. 23:169–182. CrossRefGoogle Scholar
  5. 5.
    Colombo N, Salerno F, Gruber S, Freppaz M, Williams M, Fratianni S, Giardino M (2018) Review: impacts of permafrost degradation on inorganic chemistry of surface fresh water. Glob. Planet. Change. 162:69–83. CrossRefGoogle Scholar
  6. 6.
    Giardino JR, Vitek JD, Demorett JL (1992) A model of water movement in rock glaciers and associated water characteristics. In: proceedings of the 22nd annual Binghamton symposium in geomorphology, pp. 159–184Google Scholar
  7. 7.
    Williams MW, Knauf M, Caine N, Liu F, Verplanck PL (2006) Geochemistry and source waters of rock glacier outflow, Colorado Front Range. Permafr. Periglac. Process. 17:13–33. CrossRefGoogle Scholar
  8. 8.
    Fegel TS, Baron JS, Fountain AG Johnson GF, Hall EK (2016) The differing biogeochemical and microbial signatures of glaciers and rock glaciers. J. Geophys. Res. Biogeosci. 121:919–932. CrossRefGoogle Scholar
  9. 9.
    Thies H, Nickus U, Tolotti M, Tessadri R, Krainer K (2013) Evidence of rock glacier melt impacts on water chemistry and diatoms in high mountain streams. Cold Reg. Sci. Technol. 96:77–85. CrossRefGoogle Scholar
  10. 10.
    Williams MW, Knauf M, Cory R, Caine N, Liu F (2007) Nitrate content and potential microbial signature of rock glacier outflow, Colorado Front Range. Earth Surf. Process. Landf. 32:1032–1047. CrossRefGoogle Scholar
  11. 11.
    Millar CI, Westfall RD (2008) Rock glaciers and related periglacial landforms in the Sierra Nevada, CA, USA; inventory, distribution and climatic relationships. Quat. Int. 188:90–104. CrossRefGoogle Scholar
  12. 12.
    Woo M (2012) Permafrost hydrology. Springer Science & Business Media, BerlinCrossRefGoogle Scholar
  13. 13.
    Slemmons KEH, Saros JE, Simon K (2013) The influence of glacial meltwater on alpine aquatic ecosystems: a review. Environ. Sci. Process. Impacts 15:1794–1806. CrossRefPubMedGoogle Scholar
  14. 14.
    Ilyashuk BP, Ilyashuk EA, Psenner R, Tessadri R, Koinig KA (2014) Rock glacier outflows may adversely affect lakes: lessons from the past and present of two neighboring water bodies in a crystalline-rock watershed. Environ. Sci. Technol. 48:6192–6200. CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Ilyashuk BP, Ilyashuk EA, Psenner R, Tessadri R, Koinig KA (2017) Rock glaciers in crystalline catchments: hidden permafrost-related threats to alpine headwater lakes. Glob. Chang. Biol. 24:1548–1562. CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Tolotti M, Albanese D, Cerasino L, Donati C, Pindo M, Rogora M, Seppi M (2018) First insights in bacteria diversity in headwaters emerging from alpine rock glaciers. In: proceedings of the 5th European conference on permafrost. Pp 1038–1039Google Scholar
  17. 17.
    Colombo N, Sambuelli L, Comina C, Colombero C, Giardino M, Gruber S, Viviano G, Vittori Antisari L, Salerno F (2018) Mechanisms linking active rock glaciers and impounded surface water formation in high-mountain areas. Earth Surf Process Landforms. 43(2):417–431. CrossRefGoogle Scholar
  18. 18.
    Buraschi E, Salerno F, Monguzzi C, Barbiero G, Tartari G (2005) Characterization of the Italian lake-types and identification of their reference sites using anthropogenic pressure factors. J. Limnol. 64(1):75–84CrossRefGoogle Scholar
  19. 19.
    Hamerlík L, Svitok M, Novikmec M, Očadlík M, Bitušík P (2014) Local, among-site, and regional diversity patterns of benthic macroinvertebrates in high altitude waterbodies: do ponds differ from lakes? Hydrobiologia 723:41–52. CrossRefGoogle Scholar
  20. 20.
    Colombo N, Gruber S, Martin M, Malandrino M, Magnani A, Godone D, Freppaz M, Fratianni S, Salerno F (2018) Rainfall as primary driver of discharge and solute export from rock glaciers: the Col d’Olen Rock Glacier in the NW Italian Alps. Sci. Total Environ. 639:316–330. CrossRefPubMedGoogle Scholar
  21. 21.
    Classen AT, Sundqvist MK, Henning JA, Newman GS, Moore JAM, Cregger MA, Moorhead LC, Patterson CM (2015) Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: what lies ahead? Ecosphere 6(8):130. CrossRefGoogle Scholar
  22. 22.
    Crooke WM, Simpson WE (1971) Determination of ammonium in Kjeldahl digests of crops by an automated procedure. J. Sci. Food Agric. 22:9–10. CrossRefGoogle Scholar
  23. 23.
    Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide Biol. Chem. 5:62–71. CrossRefGoogle Scholar
  24. 24.
    Jones RL, Dreher GB (1996) Silicon. In: Bartles JM (ed) Methods in soil analysis. part 3. Chemical Analysis, Soil Society of America Inc., Madison, pp 627–639Google Scholar
  25. 25.
    Gantner S, Andersson AF, Alonso-sáez L, Bertilsson S (2011) Novel primers for 16S rRNA-based archaeal community analyses in environmental samples. J. Microbiol. Methods 84:12–18. CrossRefPubMedGoogle Scholar
  26. 26.
    Muyzer G, Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695–700$02.00/0 PubMedPubMedCentralGoogle Scholar
  27. 27.
    Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18:1403–1414. CrossRefPubMedGoogle Scholar
  28. 28.
    Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864. CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Caporaso GJ, Kuczynski J, Stombaugh J et al (2010a) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336. CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Edgar RC (2016) UCHIME2: improved chimera prediction for amplicon sequencing. doi:
  32. 32.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. CrossRefGoogle Scholar
  33. 33.
    Wang Q, Garrity GM, 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. CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    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. 41:590–596. CrossRefGoogle Scholar
  35. 35.
    Caporaso JG, Bittinger K, Bushman FD, DeSantis T, Andersen GL Knight R (2010b) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267. CrossRefPubMedGoogle Scholar
  36. 36.
    Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71:8228–8235. CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MH, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2.4–3.
  39. 39.
    De Cáceres M, Legendre P (2009) Relationship between species and groups of sites. Ecology 90:3566–3574Google Scholar
  40. 40.
    Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. Third Int AAAI Conf Weblogs Soc Media 361–362.
  41. 41.
    Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New YorkCrossRefGoogle Scholar
  42. 42.
    Bradley JA, Singarayer JS, Anesio AM (2014) Microbial community dynamics in the forefield of glaciers. Proc. R. Soc. B 281:20140882. CrossRefPubMedGoogle Scholar
  43. 43.
    Jansson JK, Taş N (2014) The microbial ecology of permafrost. Nat. Rev. Microbiol. 12:414–425. CrossRefPubMedGoogle Scholar
  44. 44.
    Lazzaro A, Hilfiker D, Zeyer J (2015) Structures of microbial communities in alpine soils: seasonal and elevational effects. Front. Microbiol. 6:1330. CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fieren N (2010) Examining the global distribution of dominant archaeal populations in soil. ISME J. 5:908–917. CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Chroňáková A, Schloter-Hai B, Radl V, Endesfelder D, Quince C, Elhottová D, Šimek M, Schloter M (2015) Response of archaeal and bacterial soil communities to changes associated with outdoor cattle overwintering. PLoS One 10:e0135627. CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Siles JA, Margesin R (2016) Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: what are the driving factors? Microb. Ecol. 72:207–220. CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Zhang J, Yang Y, Zhao L, Li Y, Xie S, Liu Y (2015) Distribution of sediment bacterial and archaeal communities in plateau freshwater lakes. Appl. Microbiol. Biotechnol. 99:3291–3302. CrossRefPubMedGoogle Scholar
  49. 49.
    Auguet J-C, Barberan A, Casamayor EO (2009) Global ecological patterns in uncultured archaea. ISME J. 4:182–190. CrossRefPubMedGoogle Scholar
  50. 50.
    Fan X, Xing P (2016) Differences in the composition of archaeal communities in sediments from contrasting zones of Lake Taihu. Front. Microbiol. 7:1510. CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Liu Y, Priscu JC, Xiong J, Conrad R, Vick-Majors T, Chu H, Hou J (2016) Salinity drives archaeal distribution patterns in high altitude lake sediments on the Tibetan Plateau. FEMS Microbiol Ecol 92:fiw033. doi:
  52. 52.
    Fillol M, Sànchez-Melesió A, Gich F, Borrego CM (2015) Diversity of Miscellaneous Crenarchaeotic Group archaea in freshwater karstic lakes and their segregation between planktonic and sediment habitats. FEMS Microbiol Ecol 91:fiv020. doi:
  53. 53.
    Compte-Port S, Subirats J, Fillol M, Sànchez-Melesió A, Marcé R, Rivas-Ruiz P, Rosell-Melé A, Borrego CM (2017) Abundance and co-distribution of widespread marine archaeal lineages in surface sediments of freshwater water bodies across the Iberian Peninsula. Microb. Ecol. 74:776–787. CrossRefPubMedGoogle Scholar
  54. 54.
    Ortiz-Alvarez R, Casamayor EO (2016) High occurrence of Pacearchaeota and Woesearchaeota (Archaea superphylum DPANN) in the surface waters of oligotrophic high-altitude lakes. Environ. Microbiol. Rep. 8:210–217. CrossRefPubMedGoogle Scholar
  55. 55.
    Mania I, D’Amico M, Freppaz M, Gorra R (2016) Driving factors of soil microbial ecology in alpine, mid-latitude patterned grounds (NW Italian Alps). Biol. Fertil. Soils 52:1135–1148. CrossRefGoogle Scholar
  56. 56.
    Nemergut DR, Anderson SP, Cleveland CC, Martin AP, Miller AE, Seimon A, Schmidt SK (2007) Microbial community succession in an unvegetated, recently deglaciated soil. Microb. Ecol. 53:110–122. CrossRefPubMedGoogle Scholar
  57. 57.
    Franzetti A, Tatangelo V, Gandolfi I, Bertolini V, Bestetti G, Diolaiuti G, D’Agata C, Mihalcea C, Smiraglia C, Ambrosini R (2013) Bacterial community structure on two alpine debris-covered glaciers and biogeography of Polaromonas phylotypes. ISME J. 7:1483–1492. CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Edlund A, Soule T, Sjöling S, Jansson JK (2006) Microbial community structure in polluted Baltic Sea sediments. Environ. Microbiol. 8:223–232. CrossRefPubMedGoogle Scholar
  59. 59.
    Coci M, Odermatt N, Salcher MM, Parnthaler J, Corno G (2015) Ecology and distribution of Thaumarchaea in the deep hypolimnion of Lake Maggiore. Archaea 2015:1–11. CrossRefGoogle Scholar
  60. 60.
    Albrecht M, Pröschold T, Schumann R (2017) Identification of Cyanobacteria in a eutrophic coastal lagoon on the Southern Baltic Coast. Front. Microbiol. 8:923. CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Savichtcheva O, Debroas D, Kurmayer R, Villar C, Jenny JP, Arnaud F, Perga ME, Domaizon I (2011) Quantitative PCR enumeration of total/toxic Planktothrix rubescens and total cyanobacteria in preserved DNA isolated from lake sediments. Appl. Environ. Microbiol. 77:8744–8753. CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Vopel K, Hawes I (2006) Photosynthetic performance of benthic microbial mats in Lake Hoare, Antartica. Limnol. Oceanogr. 51:1801–1812CrossRefGoogle Scholar
  63. 63.
    Charpy L, Alliod R, Rodier M, Golubic S (2007) Benthic nitrogen fixation in the SW New Caledonia lagoon. Aquat. Microb. Ecol. 47:73–81. CrossRefGoogle Scholar
  64. 64.
    Zhang L, Jungblut AD, Hawes I, Andersen DT, Sumner DY, Mackey TJ (2015) Cyanobacterial diversity in benthic mats of the McMurdo Dry Valley lakes, Antarctica. Polar Biol. 38:1097–1110. CrossRefGoogle Scholar
  65. 65.
    Thureborn P, Franzetti A, Lundin D, Sjöling S (2016) Reconstructing ecosystem functions of the active microbial community of the Baltic Sea oxygen depleted sediments. PeerJ 4:e1593. CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Taton A, Grubisic S, Balthasart P, Hodgson DA, Laybourn-Parry J, Wilmotte A (2006) Biogeographical distribution and ecological ranges of benthic cyanobacteria in East Antarctic lakes. FEMS Microbiol. Ecol. 57:272–289. CrossRefPubMedGoogle Scholar
  67. 67.
    Spears BM, Carvalho L, Perkins R, O’Malley MB, Paterson DM (2010) The contribution of epipelon to total sediment microalgae in a shallow temperate eutrophic loch (Loch Leven, Scotland). Hydrobiologia 646:281–293. CrossRefGoogle Scholar
  68. 68.
    Cantonati M, Guella G, Komárek J, Spitale D (2014) Depth distribution of epilithic cyanobacteria and pigments in a mountain lake characterized by marked water-level fluctuations. Freshw. Sci. 33:537–547. CrossRefGoogle Scholar
  69. 69.
    Giardino JR, Shroder JF, Vitek JD (1987) Rock Glaciers. Allen and Unwin, LondonGoogle Scholar
  70. 70.
    Barsch D, Caine N (1984) The nature of mountain geomorphology. Mt. Res. Dev. 4:287–298CrossRefGoogle Scholar
  71. 71.
    Kummert M, Delaloye R (2018) Mapping and quantifying sediment transfer between the front of rapidly moving rock glaciers and torrential gullies. Geomorphology 309:60–76. CrossRefGoogle Scholar
  72. 72.
    Stanchi S, Falsone G, Bonifacio E (2015) Soil aggregation, erodibility, and erosion rates in mountain soils (NW Alps, Italy). Solid Earth 6:403–414. CrossRefGoogle Scholar
  73. 73.
    Larouche JR, Bowden WB, Giordano R, Flinn MB, Crump BC (2012) Microbial biogeography of arctic streams: exploring influences of lithology and habitat. Front. Microbiol. 3:1–9. CrossRefGoogle Scholar
  74. 74.
    Nyyssönen M, Hultman J, Ahonen L, Kukkonen I, Paulin L, Laine P, Itävaara M, Auvinen P (2014) Taxonomically and functionally diverse microbial communities in deep crystalline rocks of the Fennoscandian shield. ISME J. 8:126–138. CrossRefPubMedGoogle Scholar
  75. 75.
    Beyer A, Rzanny M, Weist A, Möller S, Burow K, Gutmann F, Neumann S, Lindner J, Müsse S, Brangsch H, Stoiber-Lipp J, Lonschinski M, Merten D, Büchel G, Kothe E (2015) Aquifer community structure in dependence of lithostratigraphy in groundwater reservoirs. Environ. Sci. Pollut. Res. 22:19342–19351. CrossRefGoogle Scholar
  76. 76.
    Ambrosini R, Musitelli F, Navarra F, Tagliaferri I, Gandolfi I, Bestetti G, Mayer C, Minora U, Azzoni RS, Diolaiuti G, Smiraglia C, Franzetti A (2017) Diversity and assembling processes of bacterial communities in cryoconite holes of a Karakoram Glacier. Microb. Ecol. 73:827–837. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Agriculture, Forest and Food Sciences (DISAFA)University of TurinGrugliascoItaly
  2. 2.Bristol Glaciology Centre, School of Geographical SciencesUniversity of BristolBristolUK
  3. 3.Department of Earth SciencesUniversity of TurinTorinoItaly
  4. 4.Department of Geography and Environmental StudiesCarleton UniversityOttawaCanada
  5. 5.Department of Environmental SciencesAarhus UniversityRoskildeDenmark

Personalised recommendations