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Structure of bacterial and eukaryote communities reflect in situ controls on community assembly in a high-alpine lake

  • Eli Michael S. GendronEmail author
  • John L. Darcy
  • Katherinia Hell
  • Steven K. Schmidt
Article

Abstract

Recent work suggests that microbial community composition in high-elevation lakes is significantly influenced by microbes entering from upstream terrestrial and aquatic habitats. To test this idea, we conducted 18S and 16S rDNA surveys of microbial communities in a high-alpine lake in the Colorado Rocky Mountains. We compared the microbial community of the lake to water entering the lake and to uphill soils that drain into the lake. Utilizing hydrological and abiotic data, we identified potential factors controlling microbial diversity and community composition. Results show a diverse community entering the lake at the inlet with a strong resemblance to uphill terrestrial and aquatic communities. In contrast, the lake communities (water column and outlet) showed significantly lower diversity and were significantly different from the inlet communities. Assumptions of neutral community assembly poorly predicted community differences between the inlet and lake, whereas “variable selection” and “dispersal limitation” were predicted to dominate. Similarly, the lake communities were correlated with discharge rate, indicating that longer hydraulic residence times limit dispersal, allowing selective pressures within the lake to structure communities. Sulfate and inorganic nitrogen and phosphorus concentrations correlated with community composition, indicating “bottom up” controls on lake community assembly. Furthermore, bacterial community composition was correlated with both Zooplankton density and eukaryotic community composition, indicating biotic controls such as “top-down” interactions also contribute to community assembly in the lake. Taken together, these community analyses suggest that deterministic biotic and abiotic selection within the lake coupled with dispersal limitation structures the microbial communities in Green Lake 4.

Keywords

co-occurrence patterns landscape connectivity deterministic community assembly Hydrurus 

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Notes

Acknowledgements

We thank Robert Spencer, Sarah Power, Brian Straight, and Jessica Henley for field and laboratory assistance, and Diane McKnight and Pacifica Sommers for helpful discussions. Logistical support and meta-data were provided by the NSF supported Niwot Ridge Long-Term Ecological Research project and the University of Colorado Mountain Research Station. Funding was provided by the Niwot Ridge LTER program (NSF DEB-1637686) and grants to study global change effects on high-elevation microbial and plant communities (NSF DEB-1457827 and 1656978).

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References

  1. Adams, H.E., Crump, B.C., and Kling, G.W. 2014. Metacommunity dynamics of bacteria in an arctic lake: The impact of species sorting and mass effects on bacterial production and biogeography. Front. Microbiol. 5, 82.CrossRefGoogle Scholar
  2. Amaral-Zettler, L.A., McCliment, E.A., Ducklow, H.W., and Huse, S.M. 2009. A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS One 4, e6372.CrossRefGoogle Scholar
  3. Angel, A., Vila, I., and Herrera, V. 2016. Extremophiles: photosynthetic systems in a high-altitude saline basin (Altiplano, Chile). Inter. Aquat. Res. 8, 91–108.CrossRefGoogle Scholar
  4. Barnes, R.T., Williams, M.W., Parman, J.N., Hill, K., and Caine, N. 2014. Thawing glacial and permafrost features contribute to nitrogen export from Green Lakes Valley, Colorado Front Range, USA. Biogeochemistry 117, 413–430.CrossRefGoogle Scholar
  5. Bueno de Mesquita, C.P., Sartwell, S.A., Ordemann, E.V., Porazinska, D.L., Farrer, E.C., King, A.J., Spasojevic, M.J., Smith, J.G., Suding, K.N., and Schmidt, S.K. 2018. Patterns of root colonization by arbuscular mycorrhizal fungi and dark septate endophytes across a mostly-unvegetated, high-elevation landscape. Fungal Ecol. 36, 63–74.CrossRefGoogle Scholar
  6. Caine, N. 2010. Recent hydrologic change in a Colorado alpine basin: An indicator of permafrost thaw? Ann. Glaciol. 51, 130–134.CrossRefGoogle Scholar
  7. Callieri, C., Pugnetti, A., and Manca, M. 1999. Carbon partitioning in the food web of a high mountain lake: from bacteria to zoo-plankton. J. Limnol. 58, 144–151.CrossRefGoogle Scholar
  8. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336.CrossRefGoogle Scholar
  9. Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Huntley, J., Fierer, N., Owens, S.M., Betley, J., Fraser, L., Bauer, M., et al. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621–1624.CrossRefGoogle Scholar
  10. Chase, J.M., Kraft, N., Smith, K.G., and Vellend, M. 2011. Using null models to disentangle variation in community dis-similarity from variation in α-diversity. Ecosphere 2, 1–11.CrossRefGoogle Scholar
  11. Chave, J. 2004. Neutral theory and community ecology. Ecol. Lett. 7, 241–253.CrossRefGoogle Scholar
  12. Comte, J., Lovejoy, C., Crevecoeur, S., and Vincent, W.F. 2015. Cooccurrence patterns in aquatic bacterial communities across changing permafrost landscapes. Biogeosciences 13, 175–190.CrossRefGoogle Scholar
  13. Crump, B.C., Amaral-Zettler, L.A., and Kling, G.W. 2012. Microbial diversity in arctic freshwaters is structured by inoculation of microbes from soils. ISME J. 6, 1629–1639.CrossRefGoogle Scholar
  14. Darcy, J.L., King, A.J., Gendron, E.M.S., and Schmidt, S.K. 2017. Spatial autocorrelation of microbial communities atop a debris-covered glacier is evidence of a supraglacial chronosequence. FEMS Microbiol. Ecol. 93, 1–11.CrossRefGoogle Scholar
  15. Edgar, R.C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.CrossRefGoogle Scholar
  16. Faith, D.P. 1992. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10.CrossRefGoogle Scholar
  17. Farjalla, V.F., Srivastava, D.S., Marino, N.A.C., Azevedo, F.D., Dib, V., Lopes, P.M., Rosado, A.S., Bozelli, R.L., and Esteves, F.A. 2012. Ecological determinism increases with organism size. Ecology 93, 1752–1759.CrossRefGoogle Scholar
  18. Flanagan, C.M., McKnight, D.M., Liptzin, D., Williams, M.W., and Miller, M.P. 2009. Response of the phytoplankton community in an Alpine Lake to drought conditions: Colorado Rocky Mountain Front Range, USA. Arct. Antarct. Alp. Res. 41, 191–203.CrossRefGoogle Scholar
  19. Fodelianakis, S., Lorz, A., Valenzuela-Cuevas, A., Barozzi, A., Booth, J.M., and Daffonchio, D. 2019. Dispersal homogenizes communities via immigration even at low rates in a simplified synthetic bacterial metacommunity. Nat. Commun. 10, 1314.CrossRefGoogle Scholar
  20. Foley, B., Jones, I.D., Maberly, S.C., and Rippey, B. 2012. Long-term changes in oxygen depletion in a small temperate lake: Effects of climate change and eutrophication. Freshwater Biol. 57, 278–289.CrossRefGoogle Scholar
  21. Freeman, K.R., Pescador, M.Y., Reed, S.C., Costello, E.K., Robeson, M.S., and Schmidt, S.K. 2009. Soil CO2 flux and photoautotrophic community composition in high-elevation, ‘barren’ soil. Environ. Microbiol. 11, 674–686.CrossRefGoogle Scholar
  22. Gardner, E.M., McKnight, D.M., Lewis, W.M., and Miller, M.P. 2008. Effects of nutrient enrichment on phytoplankton in an alpine lake, Colorado, USA. Arct. Antarct. Alp. Res. 40, 55–64.CrossRefGoogle Scholar
  23. Grossart, H.P., Jezbera, J., Horňák, K., Hutalle, K.M.L., Buck, U., and Šimek, K. 2008. Top-down and bottom-up induced shifts in bacterial abundance, production and community composition in an experimentally divided humic lake. Environ. Microbiol. 10, 635–652.CrossRefGoogle Scholar
  24. Hinder, B., Baur, I., Hanselmann, K., and Schanz, F. 1999. Microbial food web in an oligotrophic high mountain lake (Jöri Lake III, Switzerland). J. Limnol. 58, 162–168.CrossRefGoogle Scholar
  25. Hu, Y., Cai, J., Bai, C., Shao, K., Tang, X., and Gao, G. 2018. Contrasting patterns of the bacterial and archaeal communities in a high-elevation river in northwestern China. J. Microbiol. 56, 104–112.CrossRefGoogle Scholar
  26. Hubbell, S.P. 2001. The unified neutral theory of biodiversity and biogeography, p. 29. Princeton University Press, Princeton, NJ, USA.Google Scholar
  27. Kammerlander, B., Breiner, H., Filker, S., Sommaruga, R., Sonntag, B., and Stoeck, T. 2015. High diversity of protistan plankton communities in remote high mountain lakes in the European Alps and the Himalayan Mountains. FEMS Microbiol. Ecol. 91, 1–10.CrossRefGoogle Scholar
  28. Kembel, S.W., Cowan, P.D., Helmus, M.R., Cornwell, W.K., Morlon, H., Ackerly, D.D., Blomberg, S.P., and Webb, C.O. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464.CrossRefGoogle Scholar
  29. King, A.J., Farrer, E.C., Suding, K.N., and Schmidt, S.K. 2012. Cooccurrence patterns of plants and soil bacteria in the high-alpine subnival zone track environmental harshness. Front. Microbiol. 3, 347.CrossRefGoogle Scholar
  30. King, A.J., Freeman, K.R., McCormick, K.F., Lynch, R.C., Lozupone, C., Knight, R., and Schmidt, S.K. 2010. Biogeography and habitat modelling of high-alpine bacteria. Nat. Commun. 1, 53.CrossRefGoogle Scholar
  31. Langenheder, S. and Ragnarsson, H. 2007. The role of environmental and spatial factors for the composition of aquatic bacterial communities. Ecology 88, 2154–2161.CrossRefGoogle Scholar
  32. Lefèvre, E., Roussel, B., Amblard, C., and Sime-Ngando, T. 2008. The molecular diversity of freshwater picoeukaryotes reveals high occurrence of putative parasitoids in the plankton. PLoS One 3, e2324.CrossRefGoogle Scholar
  33. Legendre, P. 2014. Package ‘lmodel2.’ Model II Regression. R package version 1.7-2.Google Scholar
  34. Legendre, P. and Anderson, M.J. 1999. Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol. Monogr. 69, 1–24.CrossRefGoogle Scholar
  35. Ley, R.E., Lipson, D.A., and Schmidt, S.K. 2001. Microbial biomass levels in barren and vegetated high-altitude talus soils. Soil Sci. Soc. Am. J. 65, 111–117.CrossRefGoogle Scholar
  36. Ley, R.E., Williams, M.W., and Schmidt, S.K. 2004. Microbial population dynamics in an extreme environment: controlling factors in talus soils at 3750 m in the Colorado Rocky Mountains. Biogeochemistry 68, 297–311.CrossRefGoogle Scholar
  37. Lindström, E.S., Feng, X.M., Granéli, W., and Kritzberg, E.S. 2010. The interplay between bacterial community composition and the environment determining function of inland water bacteria. Limnol. Oceanogr. 55, 2052–2060.CrossRefGoogle Scholar
  38. Liu, F., Williams, M.W., and Caine, N. 2004. Source waters and flow paths in an alpine catchment, Colorado Front Range, United States. Water Resour. Res. 40, 1–16.Google Scholar
  39. Liu, Y., Yao, T., Jiao, N., Liu, X., Kang, S., and Luo, T. 2013. Seasonal dynamics of the bacterial community in Lake Namco, the largest Tibetan lake. Geomicrobiol. J. 30, 17–28.CrossRefGoogle Scholar
  40. Löder, M.G.J., Boersma, M., Kraberg, A.C., Aberle, N., and Wiltshire, K.H. 2014. Microbial predators promote their competitors: commensalism within an intra-guild predation system in microzooplankton. Ecosphere 5, 1–23.CrossRefGoogle Scholar
  41. Logue, J.B., Langenheder, S., Andersson, A.F., Bertilsson, S., Drakare, S., Lanzén, A., and Lindström, E.S. 2012. Freshwater bacterioplankton richness in oligotrophic lakes depends on nutrient availability rather than on species-area relationships. ISME J. 6, 1127–1136.CrossRefGoogle Scholar
  42. Loria, K. 2019. Stream and lake water chemistry data for Green Lakes Valley, 1998-ongoing. Environmental Data Initiative. https://doi.org/10.6073/pasta/974f109b0e0e658ebb77da1c62c8f4bc (Accessed 27 March 2019).
  43. Lozupone, C., Lladser, M.E., Knights, D., Stombaugh, J., and Knight, R. 2011. UniFrac: an effective distance metric for microbial community comparison. ISME J. 5, 169–172.CrossRefGoogle Scholar
  44. McKnight, D.M. 2016. Stream and lake water chemistry data for Green Lake 1 Green Lake 3 Green Lake 4 Green Lake 5 from 1998-ongoing, weekly. http://niwot.colorado.edu
  45. Medina-Sánchez, J.M., Villar-Argaiz, M., and Carrillo, P. 2004. Neither with nor without you: A complex algal control on bacterioplankton in a high mountain lake. Limnol. Oceanogr. 49, 1722–1733.CrossRefGoogle Scholar
  46. Miller, M.P. and McKnight, D.M. 2010. Comparison of seasonal changes in fluorescent dissolved organic matter among aquatic lake and stream sites in the Green Lakes Valley. J. Geophys. Res. Biogeosci. 115, G00F12.CrossRefGoogle Scholar
  47. Miller, M.P. and McKnight, D.M. 2015. Limnology of the Green Lakes Valley: Phytoplankton ecology and dissolved organic matter biogeochemistry at a long-term ecological research site. Plant Ecol. Divers. 8, 689–702.CrossRefGoogle Scholar
  48. Miller, M.P., McKnight, D.M., Cory, R.M., Williams, M.W., and Runkel, R.L. 2006. Hyporheic exchange and fulvic acid redox reactions in an alpine stream/wetland ecosystem, Colorado Front Range. Environ. Sci. Technol. 40, 5943–5949.CrossRefGoogle Scholar
  49. Mladenov, N., Williams, M.W., Schmidt, S.K., and Cawley, K. 2012. Atmospheric deposition as a source of carbon and nutrients to an alpine catchment of the Colorado Rocky Mountains. Biogeosciences 9, 3337–3355.CrossRefGoogle Scholar
  50. Molotch, N.P., Meixner, T., and Williams, M.W. 2008. Estimating stream chemistry during the snowmelt pulse using a spatially distributed, coupled snowmelt and hydrochemical modeling approach. Water Resour. Res. 44, 1–14.CrossRefGoogle Scholar
  51. Naff, C.S., Darcy, J.L., and Schmidt, S.K. 2013. Phylogeny and biogeography of an uncultured clade of snow chytrids. Environ. Microbiol. 15, 2672–2680.Google Scholar
  52. Nelson, C.E., Sadro, S., and Melack, J.M. 2009. Contrasting the influences of stream inputs and landscape position on bacterioplankton community structure and dissolved organic matter composition in high-elevation lake chains. Limnol. Oceanogr. 54, 1292–1305.CrossRefGoogle Scholar
  53. Nemergut, D.R., Schmidt, S.K., Fukami, T., O’Neill, S.P., Bilinski, T.M., Stanish, L.F., Knelman, J.E., Darcy, J.L., Lynch, R.C., Wickey, P., et al. 2013. Patterns and processes of microbial community assembly. Microbiol. Mol. Biol. Rev. 77, 342–356.CrossRefGoogle Scholar
  54. Newton, R.J., Jones, S.E., Eiler, A., McMahon, K.D., and Bertilsson, S. 2011. A guide to the natural history of freshwater lake bacteria. Microbiol. Mol. Biol. Rev. 75, 14–49.CrossRefGoogle Scholar
  55. Peura, S., Eiler, A., Hiltunen, M., Nykanen, H., Tiirola, M., and Jones, R.I. 2012. Bacterial and phytoplankton responses to nutrient amendments in a Boreal lake differ according to season and to taxonomic resolution. PLoS One 7, e38552.CrossRefGoogle Scholar
  56. Pommier, T., Douzery, E.J.P., and Mouillot, D. 2012. Environment drives high phylogenetic turnover among oceanic bacterial communities. Biol. Lett. 8, 562–566.CrossRefGoogle Scholar
  57. Porazinska, D.L., Farrer, E.C., Spasojevic, M.J., Bueno de Mesquita, C.P., Sartwell, S.A., Smith, J.G., White, C.T., King, A.J., Suding, K.N., and Schmidt, S.K. 2018. Plant diversity and density predict belowground diversity and function in an early successional alpine ecosystem. Ecology 99, 1942–1952.CrossRefGoogle Scholar
  58. Preston, D.L., Caine, N., McKnight, D.M., Williams, M.W., Hell, K., Miller, M.P., Hart, S.J., and Johnson, P.T.J. 2016. Climate regulates alpine lake ice cover phenology and aquatic ecosystem structure. Geophys. Res. Lett. 43, 5353–5360.CrossRefGoogle Scholar
  59. Price, M.N., Dehal, P.S., and Arkin, A.P. 2010. FastTree 2 — approximately maximum-likelihood trees for large alignments. PLoS One 5, e9490.CrossRefGoogle Scholar
  60. R Core Team. 2016. R: A language and environment for statistical computing. Vienna, Austria: R foundation for statistical computing. http://www.R-project.org/ (Accessed 22 November 2018).
  61. Remias, D., Jost, S., Boenigk, J., Wastian, J., and Lütz, C. 2013. Hydrurus-related golden algae (Chrysophyceae) cause yellow snow in polar summer snowfields. Phycol. Res. 61, 277–285.CrossRefGoogle Scholar
  62. Riemann, L. and Winding, A. 2001. Community dynamics of free-living and particle-associated bacterial assemblages during a freshwater phytoplankton bloom. Microb. Ecol. 42, 274–285.CrossRefGoogle Scholar
  63. Rott, E., Cantonati, M., Füreder, L., and Pfister, P. 2006. Benthic algae in high altitude streams of the Alps — a neglected component of the aquatic biota. Hydrobiologia 562, 195–216.CrossRefGoogle Scholar
  64. Ruiz-Gonzalez, C., Nino-Garcia, J.P., and Giorgio, P.A. 2015. Terrestrial origin of bacterial communities in complex boreal freshwater networks. Ecol. Lett. 18, 1198–1206.CrossRefGoogle Scholar
  65. Schadt, C., Martin, A.P., Lipson, D.A., and Schmidt, S.K. 2003. Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301, 1359–1361.CrossRefGoogle Scholar
  66. Schmidt, S.K., Costello, E.K., Nemergut, D.R., Cleveland, C.C., Reed, S.C., Weintraub, M.N., Meyer, A.F., and Martin, A.M. 2007. Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. Ecology 88, 1379–1385.CrossRefGoogle Scholar
  67. Schmidt, K. and Jónasdóttir, S.H. 1997. Nutritional quality of two cyanobacteria: How rich is ‘poor’ food? Mar. Ecol. Prog. Ser. 151, 1–10.CrossRefGoogle Scholar
  68. Seastedt, T.R., Bowman, W.D., Caine, N., McKnight, D.M., Townsend, A., and Williams, M.W. 2004. The landscape continuum: a model for high-elevation ecosystems. BioScience 54, 111–121.CrossRefGoogle Scholar
  69. Šlapeta, J., Moreira, D., and López-García, P. 2005. The extent of protist diversity: insights from molecular ecology of freshwater eukaryotes. Proc. Roy. Soc. B 272, 2073–2081.CrossRefGoogle Scholar
  70. Sloan, W.T., Lunn, M., Woodcock, S., Head, I.M., Nee, S., and Curtis, T.P. 2006. Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ. Microbiol. 8, 732–740.CrossRefGoogle Scholar
  71. Stanish, L.F., O’Neill, S.P., Gonzalez, A., Legg, T.M., Knelman, J., McKnight, D.M., Spaulding, S., and Nemergut, D.R. 2013. Bacteria and diatom co-occurrence patterns in microbial mats from polar desert streams. Environ. Microbiol. 15, 1115–1131.CrossRefGoogle Scholar
  72. Stegen, J.C., Lin, X., Fredrickson, J.K., Chen, X., Kennedy, D.W., Murray, C.J., Rockhold, M.L., and Konopka A. 2013. Quantifying community assembly processes and identifying features that impose them. ISME J. 7, 2069–2079.CrossRefGoogle Scholar
  73. Stegen, J.C., Lin, X., Fredrickson, J.K., and Konopka, A.E. 2015. Estimating and mapping ecological processes influencing microbial community assembly. Front. Microbiol. 6, 1–15.CrossRefGoogle Scholar
  74. Tang, K.W., Turk, V., and Grossart, H.P. 2010. Linkage between crustacean zooplankton and aquatic bacteria. Aquat. Microb. Ecol. 61, 261–277.CrossRefGoogle Scholar
  75. Triadó-Margarit, X. and Casamayor, E.O. 2012. Genetic diversity of planktonic eukaryotes in high mountain lakes (Central Pyrenees, Spain). Environ. Microbiol. 14, 2445–2456.CrossRefGoogle Scholar
  76. Venkataraman, A., Bassis, C.M., Beck, J.M., Young, V.B., Curtis, J.L., Huffnagle, G.B., and Schmidt, T.M. 2015. Application of a neutral community model to assess structuring of the human lung microbiome. mBio 6, 1–9.CrossRefGoogle Scholar
  77. Vestheim, H. and Jarman, S.N. 2008. Blocking primers to enhance PCR amplification of rare sequences in mixed samples — a case study on prey DNA in Antarctic krill stomachs. Front. Zool. 5, 1.CrossRefGoogle Scholar
  78. Vila-Costa, M., Barberan, A., Auguet, J.C., Sharma, S., Moran, M.A., and Casamayor, E.O. 2013. Bacterial and archaeal community structure in the surface microlayer of high mountain lakes examined under two atmospheric aerosol loading scenarios. FEMS Microbiol. Ecol. 84, 387–397.CrossRefGoogle Scholar
  79. Walters, W., Hyde, E.R., Berg-Lyons, D., Ackermann, G., Humphrey, G., Parada, A., Gilbert, J.A., Jansson, J.K., Caporaso, J.G., Fuhrman, J.A., et al. 2016. Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 1, e00009–15.CrossRefGoogle Scholar
  80. Wang, J., Wang, F., Chu, L., Wang, H., Zhong, Z., Liu, Z., Gao, J., and Duan, H. 2014. High genetic diversity and novelty in eukaryotic plankton assemblages inhabiting saline lakes in the Qaidam Basin. PLoS One 9, e112812.CrossRefGoogle Scholar
  81. Waters, S.B. 1999. Master’s thesis. Responses of algal communities to environmental change in an alpine lake, Green Lakes Valley, Colorado. University of Colorado, Boulder, USA.Google Scholar
  82. Webb, C.O., Ackerly, D.D., and Kembel, S.W. 2008. Phylocom: software for the analysis of phy-logenetic community structure and trait evolution. Version 4.0.1. http://www.phylodiversity.net/phylocom/
  83. Whitman, T., Neurath, R., Perera, A., Chu-Jacoby, I., Ning, D., Zhou, J., Nico, P., Pett-Ridge, J., and Firestone, M. 2018. Microbial community assembly differs across minerals in a rhizosphere microcosm. Environ. Microbiol. 20, 4444–4460.CrossRefGoogle Scholar
  84. Williams, M.W., Hood, E., Molotch, N., Caine, N., Cowie, R., and Liu, F. 2015. The ‘teflon basin’ myth: hydrology and hydrochemistry of a seasonally snow-covered catchment. Plant Ecol. Divers. 8, 639–661.CrossRefGoogle Scholar
  85. Williams, M.W., Losleben, M., Caine, N., and Greenland, D. 1996. Changes in climate and hydro-chemical responses in a high-elevation catchment in the Rocky Mountains, USA. Limnol. Oceanogr. 41, 939–946.CrossRefGoogle Scholar
  86. Williams, T.J., Wilkins, D., Long, E., Evans, F., Demaere, M.Z., Raftery, M.J., and Cavicchioli, R. 2013. The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. Environ. Microbiol. 15, 1302–1317.CrossRefGoogle Scholar
  87. Wu, Q.L. and Hahn, M.W. 2006. High predictability of the seasonal dynamics of a species-like Polynucleobacter population in a freshwater lake. Environ. Microbiol. 8, 1660–1666.CrossRefGoogle Scholar
  88. Wu, W., Lu, H.P., Sastri, A., Yeh, Y.C., Gong, G.C., Chou, W.C., and Hsieh, C.H. 2017. Contrasting the relative importance of species sorting and dispersal limitation in shaping marine bacterial versus protist communities. ISME J. 12, 485–494.CrossRefGoogle Scholar
  89. Wu, Q.L., Zwart, G., Schauer, M., Kamst-van Agterveld, M.P., and Hahn, M.W. 2006. Bacterioplankton community composition along a salinity gradient of sixteen High-Mountain Lakes located on the Tibetan Plateau, China. Appl. Environ. Microbiol. 72, 5478–5485.CrossRefGoogle Scholar
  90. Zapala, M.A. and Schork, N.J. 2006. Multivariate regression analysis of distance matrices for testing associations between gene expression patterns and related variables. Proc. Natl. Acad. Sci. USA 103, 19430–19435.CrossRefGoogle Scholar
  91. Zhong, Z.P., Liu, Y., Miao, L.L., Wang, F., Chu, L.M., Wang, J.L., and Liu, Z.P. 2016. Prokaryotic community structure driven by salinity and ionic concentrations in plateau lakes of the Tibetan Plateau. Appl. Environ. Microbiol. 82, 1846–1858.CrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea 2019

Authors and Affiliations

  • Eli Michael S. Gendron
    • 1
    • 2
    Email author
  • John L. Darcy
    • 3
  • Katherinia Hell
    • 4
  • Steven K. Schmidt
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  2. 2.Department of Molecular, Cellular, and Developmental BiologyUniversity of ColoradoBoulderUSA
  3. 3.Computational Bioscience ProgramUniversity of Colorado, Anschutz Medical CampusAuroraUSA
  4. 4.Insitute of Arctic and Alpine ResearchUniversity of ColoradoBoulderUSA

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