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.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
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.
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.
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.
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.
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.
Caine, N. 2010. Recent hydrologic change in a Colorado alpine basin: An indicator of permafrost thaw? Ann. Glaciol. 51, 130–134.
Callieri, C., Pugnetti, A., and Manca, M. 1999. Carbon partitioning in the food web of a high mountain lake: from bacteria to zooplankton. J. Limnol. 58, 144–151.
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.
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.
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.
Chave, J. 2004. Neutral theory and community ecology. Ecol. Lett. 7, 241–253.
Comte, J., Lovejoy, C., Crevecoeur, S., and Vincent, W.F. 2015. Co-occurrence patterns in aquatic bacterial communities across changing permafrost landscapes. Biogeosciences 13, 175–190.
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.
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.
Edgar, R.C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.
Faith, D.P. 1992. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Hubbell, S.P. 2001. The unified neutral theory of biodiversity and biogeography, p. 29. Princeton University Press, Princeton, NJ, USA.
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.
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.
King, A.J., Farrer, E.C., Suding, K.N., and Schmidt, S.K. 2012. Co-occurrence patterns of plants and soil bacteria in the high-alpine subnival zone track environmental harshness. Front. Microbiol. 3, 347.
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.
Langenheder, S. and Ragnarsson, H. 2007. The role of environmental and spatial factors for the composition of aquatic bacterial communities. Ecology 88, 2154–2161.
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.
Legendre, P. 2014. Package ‘lmodel2.’ Model II Regression. R package version 1.7–2.
Legendre, P. and Anderson, M.J. 1999. Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol. Monogr. 69, 1–24.
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.
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.
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.
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.
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.
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.
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.
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).
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.
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
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Pommier, T., Douzery, E.J.P., and Mouillot, D. 2012. Environment drives high phylogenetic turnover among oceanic bacterial communities. Biol. Lett. 8, 562–566.
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.
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.
Price, M.N., Dehal, P.S., and Arkin, A.P. 2010. FastTree 2 — approximately maximum-likelihood trees for large alignments. PLoS One 5, e9490.
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).
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.
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.
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.
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.
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.
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.
Schmidt, K. and Jónasdóttir, S.H. 1997. Nutritional quality of two cyanobacteria: How rich is ‘poor’ food? Mar. Ecol. Prog. Ser. 151, 1–10.
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.
Ŝlapeta, 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.
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.
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.
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.
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.
Tang, K.W., Turk, V., and Grossart, H.P. 2010. Linkage between crustacean zooplankton and aquatic bacteria. Aquat. Microb. Ecol. 61, 261–277.
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.
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.
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.
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.
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.
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.
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.
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/
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.
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.
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.
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.
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.
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.
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.
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.
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.
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).
Supplemental material for this article may be found at http://www.springerlink.com/content/120956.
About this article
Cite this article
Gendron, E.M.S., Darcy, J.L., Hell, K. et al. Structure of bacterial and eukaryote communities reflect in situ controls on community assembly in a high-alpine lake. J Microbiol. 57, 852–864 (2019). https://doi.org/10.1007/s12275-019-8668-8
- co-occurrence patterns
- landscape connectivity
- deterministic community assembly