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Contrasting Patterns of Community Assembly in the Stratified Water Column of Great Salt Lake, Utah

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Abstract

Phylogenetic examinations of communities sampled along geochemical gradients provide a framework for inferring the relative importance of niche-based ecological interactions (competition, environmental filtering) and neutral-based evolutionary interactions in structuring biodiversity. Great Salt Lake (GSL) in Utah exhibits strong spatial gradients due to both seasonal variation in freshwater input into the watershed and restricted fluid flow within North America’s largest saline terminal lake ecosystem. Here, we examine the phylogenetic structure and composition of archaeal, bacterial, and eukaryal small subunit (SSU) rRNA genes sampled along a stratified water column (DWR3) in the south arm of GSL in order to infer the underlying mechanism of community assembly. Communities sampled from the DWR3 epilimnion were phylogenetically clustered (i.e., coexistence of close relatives due to environmental filtering) whereas those sampled from the DWR3 hypolimnion were phylogenetically overdispersed (i.e., coexistence of distant relatives due to competitive interactions), with minimal evidence for a role for neutral processes in structuring any assemblage. The shift from phylogenetically clustered to overdispersed assemblages was associated with an increase in salinity and a decrease in dissolved O2 (DO) concentration. Likewise, the phylogenetic diversity and phylogenetic similarity of assemblages was strongly associated with salinity or DO gradients. Thus, salinity and/or DO appeared to influence the mechanism of community assembly as well as the phylogenetic diversity and composition of communities. It is proposed that the observed patterns in the phylogenetic composition and structure of DWR3 assemblages are attributable to the meromictic nature of GSL, which prevents significant mixing between the epilimnion and the hypolimnion. This leads to strong physicochemical gradients at the halocline, which are capable of supporting a greater diversity. However, concomitant shifts in nutrient availability (e.g., DO) at and below the halocline drive competitive interactions leading to hypolimnion assemblages with minimal niche overlap.

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References

  1. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505

    Article  Google Scholar 

  2. Wiens JJ, Graham CH (2005) Niche conservatism: Integrating evolution, ecology, and conservation biology. Annu Rev Ecol Evol Syst 36:519–539

    Article  Google Scholar 

  3. Westoby M (2006) Phylogenetic ecology at world scale, a new fusion between ecology and evolution. Ecology 87:S163–S165

    Article  PubMed  Google Scholar 

  4. Boyd ES, Hamilton TL, Spear JR, Lavin M, Peters JW (2010) [FeFe]-hydrogenase in Yellowstone National Park: evidence for dispersal limitation and phylogenetic niche conservatism. ISME J 4:1485–1495

    Article  PubMed  Google Scholar 

  5. Bryant JB, Lamanna C, Morlon H, Kerkhoff AJ, Enquist BJ, Green JL (2008) Microbes on mountainsides: Contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci USA 105:11505–11511

    Google Scholar 

  6. Hamilton TL, Boyd ES, Peters JW (2011) Environmental constraints underpin the distribution and phylogenetic diversity of nifH in the Yellowstone geothermal complex. Microb Ecol 61:860–870

    Article  PubMed  Google Scholar 

  7. Horner-Devine MC, Bohannan BJM (2006) Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87:S100–S108

    Article  PubMed  Google Scholar 

  8. Newton RJ, Jones SE, Helmus MR, McMahon KD (2007) Phylogenetic ecology of the freshwater Actinobacteria acI lineage. Appl Environ Microbiol 73:7169–7176

    Article  PubMed  CAS  Google Scholar 

  9. Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 1746–1748

  10. Wiens JJ (2004) Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution 58:193–197

    PubMed  Google Scholar 

  11. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography Princeton University Press. Princeton, New Jersey

  12. Kembel SW (2009) Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests. Ecol Lett 12:949–960

    Article  PubMed  Google Scholar 

  13. Vamosi SM, Heard SB, Vamosi JC, Webb CO (2009) Emerging patterns in the comparative analysis of phylogenetic community structure. Mol Ecol 18:572–592

    Article  PubMed  CAS  Google Scholar 

  14. Armitage DW, Gallagher KL, Youngblut ND, Buckley DH, Zinder SH (2012) Millimeter-scale patterns of phylogenetic and trait diversity in a salt marsh microbial mat. Frontiers in Microbiology 3:293

    PubMed  Google Scholar 

  15. Webb CO (2000) Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am Nat 156:145–155

    Article  PubMed  Google Scholar 

  16. Hamilton TL, Vogl K, Bryant DA, Boyd ES, Peters JW (2012) Environmental constraints defining the distribution, composition, and evolution of chlorophototrophs in thermal features of Yellowstone National Park. Geobiol 10:236–249

    Article  CAS  Google Scholar 

  17. Hassibe WR, Keck WG (1978) The Great Salt Lake. US Geological Survey. Reston, VA

  18. Cannon JS, Cannon MA (2002) The Southern Pacific Railroad Trestle—past and present. In: Gwynn, JW (ed.) Great Salt Lake, an overview of change. Special Publication of the Utah Department of Natural Resources, Salt Lake City, Utah, pp 283–294

  19. Baxter BK, Litchfield CD, Sowers K, Griffith JD, DasSarma PA, DasSarma S (2005) In: Gunde-Cimerron N, Oren A, Plemenita A (eds) Adaptation to life in high salt concentrations in Archaea, Bacteria and Eukarya. Springer, Netherlands

  20. Naftz D., Angeroth C, Kenney T, Waddell B, Darnell N, Silva S, Perschon C, Whitehead J (2008) Anthropogenic influences on the input and biogeochemical cycling of nutrients and mercury in Great Salt Lake, Utah, USA. Appl Geochem 23:1731–1744

    Google Scholar 

  21. Stephens DW, Gillespie DM (1976) Phytoplankton production in the Great Salt Lake, Utah, and a laboratory study of algal response to enrichment. Limnol Ocean 21:74–87

    Google Scholar 

  22. Graham CH, Parra JL, Rahbek C, McGuire JA (2009) Phylogenetic structure in tropical hummingbird communities. Proc Natl Acad Sci USA 106:19673–19678

    Article  PubMed  CAS  Google Scholar 

  23. Weiss RF (1970) The solubility of nitrogen, oxygen and argon in water and seawater. Deep Sea Res Oceanogr Abstr 17:721–735

    Article  CAS  Google Scholar 

  24. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackenbrandt E, Goodfellow M (eds.) Nucleic acid techniques in bacterial systematics. John Wiley and Sons, New York, NY, pp 115–175

  25. Spear JR, Walker JJ, McCollom TM, Pace NR (2005) Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. Proc Natl Acad Sci USA 102:2555–2560

    Article  PubMed  CAS  Google Scholar 

  26. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  27. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2006) New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72:5734–5741

    Article  PubMed  CAS  Google Scholar 

  28. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2005) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71:7724–7736

    Article  PubMed  CAS  Google Scholar 

  29. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506

    Article  PubMed  CAS  Google Scholar 

  30. Jost L (2006) Entropy and diversity. Oikos 113:363–375

    Article  Google Scholar 

  31. Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552

    Article  PubMed  Google Scholar 

  32. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  33. Posada D (2006) ModelTest Server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Res 34:W700–W703

    Article  PubMed  CAS  Google Scholar 

  34. Swofford DL (2001) Paup: Phylogenetic analysis using parsimony (and other methods). Sinauer, Sunderland, MA

    Google Scholar 

  35. Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and character evolution. Bioinformatics 24:2098–2100

    Article  PubMed  CAS  Google Scholar 

  36. Boyd ES, Skidmore M, Mitchell AC, Bakermans C, Peters JW (2010) Methanogenesis in subglacial sediments. Environ Microbiol Rep 2:685–692

    Article  PubMed  CAS  Google Scholar 

  37. Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Google Scholar 

  38. Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    Article  PubMed  Google Scholar 

  39. Naiman RJ, Décamps H, Pollock M (1993) The role of riparian corridors in maintaining regional biodiversity. Ecol Appl 3:209–212

    Article  Google Scholar 

  40. Totsche KU, Rennert T, Gerzabek MH, Kögel-Knabner I, Smalla K, Spiteller M, Vogel H (2010) Biogeochemical interfaces in soil: The interdisciplinary challenge for soil science. J Plant Nutr Soil Sci 173:88–99

    Google Scholar 

  41. Curtis TP, Sloan WT (2005) Exploring microbial diversity—a vast below. Science 309:1331–1333

    Article  PubMed  CAS  Google Scholar 

  42. Harris JK, Caporaso JG, Walker JJ, Spear JR, Gold NJ, Robertson CE, Hugenholtz P, Goodrich J, McDonald D, Knights D, Marshall P, Tufo H, Knight R, Pace NR (2013) Phylogenetic stratigraphy in the Guerrero Negro hypersaline microbial mat. ISME J 7:50–60

    Google Scholar 

  43. Parnell JJ, Rompato G, Latta LCIV, Pfrender ME, Van Nostrand JD, He Z, Zhou J, Andersen G, Champine P, Ganesan B, Weimer BC (2010) Functional biogeography as evidence of gene transfer in hypersaline microbial communities. PLoS One 5:e12919

    Article  PubMed  Google Scholar 

  44. Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci USA 104:11436–11440

    Article  PubMed  CAS  Google Scholar 

  45. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2010) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108:4516–4522

    Google Scholar 

  46. Gogarten JP, Townsend JP (2005) Horizontal gene transfer, genome innovation and evolution. Nat Rev Micro 3:679–687

    Article  CAS  Google Scholar 

  47. Márquez MC, Carrasco IJ, Xue Y, Ma Y, Cowan DA, Jones BE, Grant WD, Ventosa A (2007) Aquisalimonas asiatica gen. nov., sp. nov., a moderately halophilic bacterium isolated from an alkaline, saline lake in Inner Mongolia, China. Int J Syst Evol Microbiol 57:1137–1142

    Article  PubMed  Google Scholar 

  48. Garrity GM, Brenner DJ, Krieg NR, Staley JT (eds.) (2005) Bergey’s manual of systematic bacteriology, vol. 2: The proteobacteria, Part C: The Alpha-, Beta-, Delta- and Epsilonproteobacteria. Springer, New York, NY

  49. Holmes DE, Nevin KP, Woodard TL, Peacock AD, Lovley DR (2007) Prolixibacter bellariivorans gen. nov., sp. nov., a sugar-fermenting, psychrotolerant anaerobe of the phylum Bacteroidetes, isolated from a marine-sediment fuel cell. Int J Syst Evol Microbiol 57:701–707

    Article  PubMed  CAS  Google Scholar 

  50. Lupton FS, Phelps TJ, Zeikus JG (1984) Methanogenesis, sulphate reduction and hydrogen metabolism in hypersaline anoxic sediments of the Great Salt Lake, Utah. In: Editor (ed.)^(eds.) Book Methanogenesis, sulphate reduction and hydrogen metabolism in hypersaline anoxic sediments of the Great Salt Lake, Utah., vol. Bureau of Mineral Resources, City, pp. 42–48

  51. Phelps T, Zeikus JG (1980) Microbial ecology of anaerobic decomposition in Great Salt Lake. Abstract 14, pp 89, 80th Annual Meeting of the American Society for Microbiology, American Society for Microbiology, Washington, D.C.

  52. Zeikus JG (1983) Metabolic communication between biodegradative populations in nature. In: Slater, JH, Whittenbury E, and Wimpenny JWT (eds.) Microbes in their natural environments, Society for General Microbiology, Symposium 34, Cambridge University Press, Cambridge, MA

  53. Rushforth S, Felix E (1982) Biotic adjustments to changing salinities in the Great Salt Lake, Utah, USA. Microb Ecol 8:157–161

    Article  Google Scholar 

  54. Boyd ES, Spear JR, Peters JW (2009) [FeFe]-hydrogenase genetic diversity provides insight into molecular adaptation in a saline microbial mat community. Appl Environ Microbiol 75:4620–4623

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors express their sincere gratitude to John Luft and colleagues at the Utah Division of Wildlife Resources, Great Salt Lake Ecosystem Project, for boat access, sampling help, and GIS expertise. The authors of this work gratefully acknowledge the United States Air Force Office of Scientific Research under grant FA9550-05-1-0365 and FA9550-11-1-0211 (to JEM, JWP, MCP, and ESB) and R-8196-G1 to JRS. We would also like to acknowledge the technical assistance of Devin Karns and Alex Trujillo as well as Shannon Ulrich and Dave Vuono for their careful review of a previous version of this manuscript.

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Correspondence to Eric S. Boyd.

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Meuser, J.E., Baxter, B.K., Spear, J.R. et al. Contrasting Patterns of Community Assembly in the Stratified Water Column of Great Salt Lake, Utah. Microb Ecol 66, 268–280 (2013). https://doi.org/10.1007/s00248-013-0180-9

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