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Environmental Controls on Microbial Diversity in Arctic Lakes of West Greenland

Abstract

We assessed the microbial community structure of six arctic lakes in West Greenland and investigated relationships to lake physical and chemical characteristics. Lakes from the ice sheet region exhibited the highest species richness, while inland and plateau lakes had lower observed taxonomical diversity. Lake habitat differentiation during summer stratification appeared to alter within lake microbial community composition in only a subset of lakes, while lake variability across regions was a consistent driver of microbial community composition in these arctic lakes. Principal coordinate analysis revealed differentiation of communities along two axes: each reflecting differences in morphometric (lake surface area), geographic (latitude and distance from the ice sheet), physical lake variables (water clarity), and lakewater chemistry (dissolved organic carbon [DOC], dissolved oxygen [DO], total nitrogen [TN], and conductivity). Understanding these relationships between environmental variables and microbial communities is especially important as heterotrophic microorganisms are key to organic matter decomposition, nutrient cycling, and carbon flow through nutrient poor aquatic environments in the Arctic.

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Data Availability

The nucleotide sequence data reported are available in the GenBank database under the accession number SRP160381.

References

  1. 1.

    Hinzman LD, Deal CJ, McGuire AD, Mernild SH, Polyakov IV, Walsh JE (2013) Trajectory of the Arctic as an integrated system. Ecol Appl 23(8):1837–1868. https://doi.org/10.1890/11-1498.1

  2. 2.

    Mayewski PA, Sneed SB, Birkel SD, Kurbatov AV, Maasch KA (2014) Holocene warming marked by abrupt onset of longer summers and reduced storm frequency around Greenland. J Quat Sci 29(1):99–104. https://doi.org/10.1002/jqs.2684

  3. 3.

    Boberg F, Langen PL, Mottram RH, Christensen JH, Olesen M (2018) 21st-century climate change around Kangerlussuaq, West Greenland: from the ice sheet to the shores of Davis Strait. Arct Antarct Alp Res 50(1):S100006. https://doi.org/10.1080/15230430.2017.1420862

  4. 4.

    Monteith DT, Stoddard JL, Evans CD, de Wit HA, Forsius M, Hogasen T, Wilander A, Skjelkvale BL, Jeffries DS, Vuorenmaa J, Keller B, Kopacek J, Vesely J (2007) Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450(7169):537–540. https://doi.org/10.1038/nature06316

  5. 5.

    Saros JE, Osburn CL, Northington RM, Birkel SD, Auger JD, Stedmon CA, Anderson NJ (2015) Recent decrease in DOC concentrations in Arctic lakes of southwest Greenland. Geophys Res Lett 42(16):6703–6709. https://doi.org/10.1002/2015gl065075

  6. 6.

    Saros JE, Northington RM, Osburn CL, Burpee BT, Anderson NJ (2016) Thermal stratification in small arctic lakes of southwest Greenland affected by water transparency and epilimnetic temperatures. Limnol Oceanogr 61(4):1530–1542. https://doi.org/10.1002/lno.10314

  7. 7.

    Azam F, Fenchel T, Field JG, Gray JS, Meyerreil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10(3):257–263. https://doi.org/10.3354/meps010257

  8. 8.

    Bowman JS, Vick-Majors TJ, Morgan-Kiss R, Takacs-Vesbach C, Ducklow HW, Priscu JC (2016) Microbial community dynamics in two polar extremes: the lakes of the McMurdo Dry Valleys and the West Antarctic Peninsula marine ecosystem. Bioscience 66(10):829–847. https://doi.org/10.1093/biosci/biw103

  9. 9.

    Casamayor EO, Schafer H, Baneras L, Pedros-Alio C, Muyzer G (2000) Identification of and spatio-temporal differences between microbial assemblages from two neighboring sulfurous lakes: comparison by microscopy and denaturing gradient gel electrophoresis. Appl Environ Microbiol 66(2):499–508. https://doi.org/10.1128/Aem.66.2.499-508.2000

  10. 10.

    Crump BC, Kling GW, Bahr M, Hobbie JE (2003) Bacterioplankton community shifts in an Arctic lake correlate with seasonal changes in organic matter source. Appl Environ Microbiol 69(4):2253–2268. https://doi.org/10.1128/Aem.69.4.2253-2268.2003

  11. 11.

    Høj L, Olsen RA, Torsvik VL (2008) Effects of temperature on the diversity and community structure of known methanogenic groups and other archaea in high Arctic peat. Isme J 2(1):37–48. https://doi.org/10.1038/ismej.2007.84

  12. 12.

    Haukka K, Kolmonen E, Hyder R, Hietala J, Vakkilainen K, Kairesalo T, Haari H, Sivonen K (2006) Effect of nutrient loading on bacterioplankton community composition in lake mesocosms. Microb Ecol 51(2):137–146. https://doi.org/10.1007/s00248-005-0049-7

  13. 13.

    Langenheder S, Lindstrom ES, Tranvik LJ (2005) Weak coupling between community composition and functioning of aquatic bacteria. Limnol Oceanogr 50(3):957–967. https://doi.org/10.4319/lo.2005.50.3.0957

  14. 14.

    Lindström ES, Bergstrom AK (2004) Influence of inlet bacteria on bacterioplankton assemblage composition in lakes of different hydraulic retention time. Limnol Oceanogr 49(1):125–136. https://doi.org/10.4319/lo.2004.49.1.0125

  15. 15.

    Boucher D, Jardillier L, Debroas D (2006) Succession of bacterial community composition over two consecutive years in two aquatic systems: a natural lake and a lake-reservoir. FEMS Microbiol Ecol 55(1):79–97. https://doi.org/10.1111/j.1574-6941.2005.00011.x

  16. 16.

    Selig U, Hubener T, Heerkloss R, Schubert H (2004) Vertical gradient of nutrients in two dimictic lakes - influence of phototrophic sulfur bacteria on nutrient balance. Aquat Sci 66(3):247–256. https://doi.org/10.1007/s00027-004-0684-y

  17. 17.

    Shade A, Jones SE, McMahon KD (2008) The influence of habitat heterogeneity on freshwater bacterial community composition and dynamics. Environ Microbiol 10(4):1057–1067. https://doi.org/10.1111/j.1462-2920.2007.01527.x

  18. 18.

    Tammert H, Kisand V, Noges T (2005) Bacterioplankton abundance and activity in a small hypertrophic stratified lake. Hydrobiologia 547:83–90. https://doi.org/10.1007/s10750-005-4148-8

  19. 19.

    Tonno I, Ott K, Noges T (2005) Nitrogen dynamics in the steeply stratified, temperate Lake Verevi, Estonia. Hydrobiologia 547:63–71. https://doi.org/10.1007/s10750-005-4145-y

  20. 20.

    Williamson CE, Overholt EP, Pilla RM, Leach TH, Brentrup JA, Knoll LB, Mette EM, Moeller RE (2015) Ecological consequences of long-term browning in lakes. Sci Rep 5:18666. https://doi.org/10.1038/srep18666

  21. 21.

    Søndergaard M, Jensen JP, Jeppesen E (2003) Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia 506(1–3):135–145. https://doi.org/10.1023/B:HYDR.0000008611.12704.dd

  22. 22.

    Peter S, Agstam O, Sobek S (2017) Widespread release of dissolved organic carbon from anoxic boreal lake sediments. Inland Waters 7(2):151–163. https://doi.org/10.1080/20442041.2017.1300226

  23. 23.

    Cotner JB, Biddanda BA (2002) Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosyst 5(2):105–121. https://doi.org/10.1007/s10021-001-0059-3

  24. 24.

    Villar-Argaiz M, Medina-Sanchez JM, Carrillo P (2002) Microbial plankton response to contrasting climatic conditions: insights from community structure, productivity and fraction stoichiometry. Aquat Microb Ecol 29(3):253–266. https://doi.org/10.3354/ame029253

  25. 25.

    Vila X, Abella CA, Figueras JB, Hurley JP (1998) Vertical models of phototrophic bacterial distribution in the metalimnetic microbial communities of several freshwater North-American kettle lakes. FEMS Microbiol Ecol 25(3):287–299. https://doi.org/10.1016/S0168-6496(98)00010-5

  26. 26.

    Anderson NJ, Harriman R, Ryves DB, Patrick ST (2001) Dominant factors controlling variability in the ionic composition of West Greenland lakes. Arct Antarct Alp Res 33(4):418–425. https://doi.org/10.2307/1552551

  27. 27.

    Northington RM, Saros JE (2016) Factors controlling methane in Arctic lakes of Southwest Greenland. PLoS One 11(7):e0159642. https://doi.org/10.1371/journal.pone.0159642

  28. 28.

    Yuan SQ, Cohen DB, Ravel J, Abdo Z, Forney LJ (2012) Evaluation of methods for the extraction and purification of DNA from the human microbiome. PLoS One 7(3):e33865. https://doi.org/10.1371/journal.pone.0033865

  29. 29.

    Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glockner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41(1):e1. https://doi.org/10.1093/nar/gks808

  30. 30.

    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. https://doi.org/10.1093/bioinformatics/btq461

  31. 31.

    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303

  32. 32.

    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267. https://doi.org/10.1128/Aem.00062-07

  33. 33.

    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381

  34. 34.

    Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26(2):266–267. https://doi.org/10.1093/bioinformatics/btp636

  35. 35.

    Cole JR, Wang Q, Fish JA, Chai BL, McGarrell DM, Sun YN, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42(D1):D633–D642. https://doi.org/10.1093/nar/gkt1244

  36. 36.

    DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072. https://doi.org/10.1128/Aem.03006-05

  37. 37.

    Rohwer RR, Hamilton JJ, Newton RJ, McMahon KD (2018) TaxAss: leveraging a custom freshwater database achieves fine-scale taxonomic resolution. mSphere 3(5). https://doi.org/10.1128/mSphere.00327-18

  38. 38.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

  39. 39.

    Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71(12):8228–8235. https://doi.org/10.1128/Aem.71.12.8228-8235.2005

  40. 40.

    McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10(4):e1003531. https://doi.org/10.1371/journal.pcbi.1003531

  41. 41.

    Vazquez-Baeza Y, Pirrung M, Gonzalez A, Knight R (2013) EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience 2:16. https://doi.org/10.1186/2047-217x-2-16

  42. 42.

    Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) Vegan: community ecology package. R package version 2.5–4. https://CRANR-project.org/package=vegan

  43. 43.

    Dollhopf SL, Hashsham SA, Tiedje JM (2001) Interpreting 16S rDNA T-RFLP data: application of self-organizing maps and principal component analysis to describe community dynamics and convergence. Microb Ecol 42(4):495–505. https://doi.org/10.1007/s00248-001-0027-7

  44. 44.

    Buttigieg PL, Ramette A (2014) A guide to statistical analysis in microbial ecology: a community-focused, living review of multivariate data analyses. FEMS Microbiol Ecol 90(3):543–550. https://doi.org/10.1111/1574-6941.12437

  45. 45.

    Jombart T (2016) Introduction to genetic data analysis using R. http://adegenet.r-forge.r-project.org/files/PRstats/practical-MVAintro.1.0.pdf

  46. 46.

    Harris JK, Kelley ST, Pace NR (2004) New perspective on uncultured bacterial phylogenetic division OP11. Appl Environ Microbiol 70(2):845–849. https://doi.org/10.1128/AEM.70.2.845-849.2004

  47. 47.

    Amato P, Hennebelle R, Magand O, Sancelme M, Delort AM, Barbante C, Boutron C, Ferrari C (2007) Bacterial characterization of the snow cover at Spitzberg, Svalbard. FEMS Microbiol Ecol 59(2):255–264. https://doi.org/10.1111/j.1574-6941.2006.00198.x

  48. 48.

    Harding T, Jungblut AD, Lovejoy C, Vincent WF (2011) Microbes in high arctic snow and implications for the cold biosphere. Appl Environ Microbiol 77(10):3234–3243. https://doi.org/10.1128/AEM.02611-10

  49. 49.

    Humbert JF, Dorigo U, Cecchi P, Le Berre B, Debroas D, Bouvy M (2009) Comparison of the structure and composition of bacterial communities from temperate and tropical freshwater ecosystems. Environ Microbiol 11(9):2339–2350. https://doi.org/10.1111/j.1462-2920.2009.01960.x

  50. 50.

    Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microbiol 71(1):227–239. https://doi.org/10.1128/AEM.71.1.227-239.2005

  51. 51.

    Lindström ES, Vrede K, Leskinen E (2004) Response of a member of the Verrucomicrobia, among the dominating bacteria in a hypolimnion, to increased phosphorus availability. J Plankton Res 26(2):241–246. https://doi.org/10.1093/plankt/fbh010

  52. 52.

    Schmidt ML, White JD, Denef VJ (2016) Phylogenetic conservation of freshwater lake habitat preference varies between abundant bacterioplankton phyla. Environ Microbiol 18(4):1212–1226. https://doi.org/10.1111/1462-2920.13143

  53. 53.

    Paver SF, Hayek KR, Gano KA, Fagen JR, Brown CT, Davis-Richardson AG, Crabb DB, Rosario-Passapera R, Giongo A, Triplett EW, Kent AD (2013) Interactions between specific phytoplankton and bacteria affect lake bacterial community succession. Environ Microbiol 15(9):2489–2504. https://doi.org/10.1111/1462-2920.12131

  54. 54.

    Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75(1):14–49. https://doi.org/10.1128/MMBR.00028-10

  55. 55.

    Lliros M, Inceoglu O, Garcia-Armisen T, Anzil A, Leporcq B, Pigneur LM, Viroux L, Darchambeau F, Descy JP, Servais P (2014) Bacterial community composition in three freshwater reservoirs of different alkalinity and trophic status. Plos One 9(12):e116145. https://doi.org/10.1371/journal.pone.0116145

  56. 56.

    Dunfield PF, Yuryev A, Senin P, Smirnova AV, Stott MB, Hou SB, Ly B, Saw JH, Zhou ZM, Ren Y, Wang JM, Mountain BW, Crowe MA, Weatherby TM, Bodelier PLE, Liesack W, Feng L, Wang L, Alam M (2007) Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450(7171):879–U818. https://doi.org/10.1038/nature06411

  57. 57.

    Hanson PC, Hamilton DP, Stanley EH, Preston N, Langman OC, Kara EL (2011) Fate of allochthonous dissolved organic carbon in lakes: a quantitative approach. PLoS One 6(7):e21884. https://doi.org/10.1371/journal.pone.0021884

  58. 58.

    He S, Stevens SLR, Chan LK, Bertilsson S, Glavina Del Rio T, Tringe SG, Malmstrom RR, McMahon KD (2017) Ecophysiology of freshwater verrucomicrobia inferred from metagenome-assembled genomes. mSphere 2(5). https://doi.org/10.1128/mSphere.00277-17

  59. 59.

    Tranvik LJ, Downing JA, Cotner JB, Loiselle SA, Striegl RG, Ballatore TJ, Dillon P, Finlay K, Fortino K, Knoll LB, Kortelainen PL, Kutser T, Larsen S, Laurion I, Leech DM, McCallister SL, McKnight DM, Melack JM, Overholt E, Porter JA, Prairie Y, Renwick WH, Roland F, Sherman BS, Schindler DW, Sobek S, Tremblay A, Vanni MJ, Verschoor AM, von Wachenfeldt E, Weyhenmeyer GA (2009) Lakes and reservoirs as regulators of carbon cycling and climate. Limnol Oceanogr 54(6):2298–2314. https://doi.org/10.4319/lo.2009.54.6_part_2.2298

  60. 60.

    Vincent WF (2010) Microbial ecosystem responses to rapid climate change in the Arctic. Isme J 4(9):1089–1090. https://doi.org/10.1038/ismej.2010.108

  61. 61.

    Wik M, Thornton BF, Bastviken D, Uhlback J, Crill PM (2016) Biased sampling of methane release from northern lakes: a problem for extrapolation. Geophys Res Lett 43(3):1256–1262. https://doi.org/10.1002/2015gl066501

  62. 62.

    Cardman Z, Arnosti C, Durbin A, Ziervogel K, Cox C, Steen AD, Teske A (2014) Verrucomicrobia are candidates for polysaccharide-degrading bacterioplankton in an arctic fjord of Svalbard. Appl Environ Microbiol 80(12):3749–3756. https://doi.org/10.1128/AEM.00899-14

  63. 63.

    Tran P, Ramachandran A, Khawasik O, Beisner BE, Rautio M, Huot Y, Walsh DA (2018) Microbial life under ice: Metagenome diversity and in situ activity of Verrucomicrobia in seasonally ice-covered lakes. Environ Microbiol 20(7):2568–2584. https://doi.org/10.1111/1462-2920.14283

  64. 64.

    Wik M, Varner RK, Anthony KW, MacIntyre S, Bastviken D (2016) Climate-sensitive northern lakes and ponds are critical components of methane release. Nat Geosci 9(2):99–105. https://doi.org/10.1038/Ngeo2578

  65. 65.

    Bowman JP (2015) Methylococcales Ord. Nov. In: Bowman DJ (ed) Bergey’s manual of systematics of archaea and bacteria. Wiley, Hoboken

  66. 66.

    Smith GJ, Angle JC, Solden LM, Borton MA, Morin TH, Daly RA, Johnston MD, Stefanik KC, Wolfe R, Gil B, Wrighton KC (2018) Members of the genus Methylobacter are inferred to account for the majority of aerobic methane oxidation in oxic soils from a freshwater wetland. Mbio 9(6):e00815-18. https://doi.org/10.1128/mBio.00815-18

  67. 67.

    Lin X, Green S, Tfaily MM, Prakash O, Konstantinidis KT, Corbett JE, Chanton JP, Cooper WT, Kostka JE (2012) Microbial community structure and activity linked to contrasting biogeochemical gradients in bog and fen environments of the Glacial Lake Agassiz Peatland. Appl Environ Microbiol 78(19):7023–7031. https://doi.org/10.1128/AEM.01750-12

  68. 68.

    Saros JE, Anderson NJ (2015) The ecology of the planktonic diatom Cyclotella and its implications for global environmental change studies. Biol Rev 90(2):522–541. https://doi.org/10.1111/brv.12120

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Acknowledgments

The authors thank the University of Wisconsin Biotechnology Center DNA Sequencing Facility for providing 16S metagenomic sequencing facilities and services. We are sincerely grateful to Max Egener, Helen Schlimm, Benjamin Burpee, and Robert Northington for their field assistance.

Funding

This research was funded by the Arctic System Science program of the US National Science Foundation (grant #1203434 to Jasmine Saros), the Churchill Discretionary Fund, the Center for Sustainability Education at Dickinson College, and Dickinson College Research and Development.

Author information

Correspondence to Dana J. Somers or Kristin E. Strock.

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Somers, D.J., Strock, K.E. & Saros, J.E. Environmental Controls on Microbial Diversity in Arctic Lakes of West Greenland. Microb Ecol (2019). https://doi.org/10.1007/s00248-019-01474-9

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Keywords

  • Bacterial communities
  • Lake microbiome
  • Arctic lakes
  • Greenland
  • Limnology