Abstract
The Salton Sea is a large, shallow, endorheic, polymictic, saline lake in Southern California sustained by runoff from local agricultural and municipal wastewater. As a closed-basin lake in an arid region with declining water supply, it is becoming increasingly saline. Due to its eutrophic status and episodic wind-driven mixing, basin-wide anoxia events are becoming more common during summer. Sequencing of 16S rRNA gene clones obtained from the water column and sediments provided the first molecular assessment of bacterial community structure in the Salton Sea. Similar to other saline habitats, the water column community was dominated by Gamma- and Alphaproteobacteria, and Bacteroidetes, although there was significant seasonal variability in diversity, richness, and the specific genera recovered. Sediments showed high diversity and richness and were dominated by sequences from cultured and uncultured phyla typical of marine sediments, especially the Deltaproteobacteria. This study has provided baseline data about the bacterial communities found in this important California water body and may serve as important indicators of change as the lake becomes increasingly saline over time or as remediation efforts are enacted.
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Altschul, S. F., T. L. Madden, A. A. Schäffer, J. Zhang, Z. Zhang, W. Miller & D. Lipman, 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389–3402.
Anton, J., R. Rossello-Mora, F. Rodriguez-Valera & R. Amann, 2000. Extremely halophilic bacteria in crystallizer ponds from solar salterns. Applied and Environmental Microbiology 66: 3052–3057.
Barlow, S. B. & P. Kugrens, 2002. Cryptomonads from the Salton Sea, California. Hydrobiologia 473: 129–137.
Benlloch, S., A. Lopez-Lopez, E. O. Casamayor, L. Ovreas, V. Goddard, F. L. Daae, G. Smerdon, R. Massana, I. Joint, F. Thingstad, C. Pedros-Alio & F. Rodriguez-Valera, 2002. Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environmental Microbiology 4: 349–360.
Britschgi, T. B. & S. J. Giovanonni, 1991. Phylogenetic analysis of a natural marine bacterioplankton pupulation by rRNA cloning and sequencing. Applied and Environmental Microbiology 57: 1707–1713.
Casamayor, E. O., R. Massana, S. Benlloch, L. Ovreas, B. Diez, V. J. Goddard, J. M. Gasol, I. Joint, F. Rodriguez-Valera & C. Pedros-Alio, 2002. Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environmental Microbiology 4: 338–348.
Caskey, L. L., R. R. Riedel, B. Costa-Pierce, J. Butler & S. H. Hurlbert, 2007. Population dynamics, distribution, and growth rate of tilapia (Oreochromis mossambicus) in the Salton Sea, California, with notes on bairdiella (Bairdiella icistia) and orangemouth corvina (Cynoscion xanthulus). Hydrobiologia 576: 185–203.
Chattopadhyay, J., P. D. N. Srinivasu & N. Bairagi, 2003. Pelicans at risk in Salton Sea—an eco-epidemiological model-II. Ecological Modelling 167: 199–211.
Corzo, A., F. Jimenez-Gomez, F. Gordillo, R. Garcia-Ruiz & F. Niell, 1999. Short communication, Synechococcus and Prochlorococcus-like populations detected by flow cytometry in a eutrophic reservoir in summer. Journal of Plankton Research 21: 1575–1581.
Crump, B. C., C. S. Hopkinson, M. L. Sogin & J. E. Hobbie, 2004. Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Applied and Environmental Microbiology 70: 1494–1505.
Dang, H., T. Li, M. Chen & G. Huang, 2008. Cross-ocean distribution of Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters. Applied and Environmental Microbiology 74: 52–60.
Demergasso, C., E. O. Casamayor, G. Chong, P. Galleguillos, L. Escudero & C. Pedros-Alio, 2004. Distribution of prokaryotic genetic diversity in athalassohaline lakes of the Atacama Desert, Northern Chile. FEMS Microbiology Ecology 48: 57–69.
Demergasso, C., L. Escudero, E. Casamayor, G. Chong, V. Balagué & C. Pedrós-Alió, 2008. Novelty and spatio–temporal heterogeneity in the bacterial diversity of hypersaline Lake Tebenquiche (Salar de Atacama). Extremophiles 12: 491–504.
Detwiler, P. M., M. F. Coe & D. M. Dexter, 2002. The benthic invertebrates of the Salton Sea: distribution and seasonal dynamics. Hydrobiologia 473: 139–160.
Dimitriu, P. A., H. C. Pinkart, B. M. Peyton & M. R. Mormile, 2008. Spatial and temporal patterns in the microbial diversity of a Meromictic Soda Lake in Washington State. Applied and Environmental Microbiology 74: 4877–4888.
Eckburg, P. B., E. M. Bik, C. N. Bernstein, E. Purdom, L. Dethlefsen, M. Sargent, S. R. Gill, K. E. Nelson & D. A. Relman, 2005. Diversity of the human intestinal microbial flora. Science 308: 1635–1638.
Eiler, A. & S. Bertilsson, 2007. Flavobacteria blooms in four eutrophic lakes: linking population dynamics of freshwater bacterioplankton to resource availability. Applied and Environmental Microbiology 73: 3511–3518.
Foti, M., D. Sorokin, E. Zacharova, N. Pimenov, J. Kuenen & G. Muyzer, 2008. Bacterial diversity and activity along a salinity gradient in soda lakes of the Kulunda Steppe (Altai, Russia). Extremophiles 12: 133–145.
Friend, M., 2002. Avian disease at the Salton Sea. Hydrobiologia 473: 293–306.
Fuhrman, J. A., K. McCallum & A. A. Davis, 1993. Phylogenetic diversity of subsurface marine microbial communities from the Atlantic and Pacific Oceans. Applied and Environmental Microbiology 59: 1294–1302.
Giovannoni, S. J., T. B. Britschgi, C. L. Moyer & K. G. Field, 1990. Genetic diversity in Sargasso Sea bacterioplankton. Nature 345: 60–63.
Giovannoni, S. J., M. S. Rappé, K. L. Vergin & N. L. Adair, 1996. 16S rRNA genes reveal stratified open ocean bacterioplankton populations related to the green non-sulfur bacteria. Proceedings of the National Academy of Sciences, USA 93: 7979–7984.
Glockner, F. O., B. M. Fuchs & R. Amann, 1999. Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Applied and Environmental Microbiology 65: 3721–3726.
Gonzalez, M. R., C. M. Hart & J. R. Verfaillie, 1998. Salinity and fish effects on Salton Sea microecosystems: water chemistry and nutrient cycling. Hydrobiologia 381: 105–128.
Good, I. J., 1953. The population frequencies of species and the estimation of population parameters. Biometrika 40: 237–264.
Hagstrom, A., T. Pommier, F. Rohwer, K. Simu, W. Stolte, D. Svensson & U. L. Zweifel, 2002. Use of 16S ribosomal DNA for delineation of marine bacterioplankton species. Applied and Environmental Microbiology 68: 3628–3633.
Hahn, M. W., 2006. The microbial diversity of inland waters. Current Opinion in Biotechnology 17: 256–261.
Hart, C. M., M. R. Gonzalez, E. P. Simpson & H. H. T. Stuart, 1998. Salinity and fish effects on Salton Sea microecosystems: zooplankton and nekton. Hydrobiologia 381: 129–152.
Henriksen, J. R., 2004. webLIBSHUFF. http://libshuff.mib.uga.edu.
Hofle, M. G., H. Haas & K. Dominik, 1999. Seasonal dynamics of bacterioplankton community structure in a eutrophic lake as determined by 5S rRNA analysis. Applied and Environmental Microbiology 65: 3164–3174.
Holdren, G. C. & A. Montaño, 2002. Chemical and physical characteristics of the Salton Sea, California. Hydrobiologia 473: 1–21.
Hollibaugh, J. T., P. S. Wong, N. Bano, S. K. Pak, E. M. Prager & C. Orrego, 2001. Stratification of microbial assemblages in Mono Lake, California, and response to a mixing event. Hydrobiologia 466: 45–60.
Huber, T., G. Faulkner & P. Hugenholtz, 2004. Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317–2319.
Huelsenbeck, J. P. & F. Ronquist, 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.
Humayoun, S. B., N. Bano & J. T. Hollibaugh, 2003. Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Applied and Environmental Microbiology 69: 1030–1042.
Jiang, H. C., H. L. Dong, G. X. Zhang, B. S. Yu, L. R. Chapman & M. W. Fields, 2006. Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Applied and Environmental Microbiology 72: 3832–3845.
Jones, B. E., W. D. Grant, A. W. Duckworth & G. G. Owenson, 1998. Microbial diversity of soda lakes. Extremophiles 2: 191–200.
Kerkhof, L. J., M. A. Voytek, R. M. Sherrell, D. Millie & O. Schofield, 1999. Variability in bacterial community structure during upwelling in the coastal ocean. Hydrobiologia 401: 139–148.
Kirchman, D. L., 2002. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiology Ecology 39: 91.
Kirchman, D. L., A. I. Dittel, R. R. Malmstrom & M. T. Cottrell, 2005. Biogeography of major bacterial groups in the Delaware Estuary. Limnology and Oceanography 50: 1697–1706.
Kisand, V. & T. Nıges, 2004. Abiotic and biotic factors regulating dynamics of bacterioplankton in a large shallow lake. FEMS Microbiology Ecology 50: 51–62.
Koizumi, Y., H. Kojima, K. Oguri, H. Kitazato & M. Fukui, 2004. Vertical and temporal shifts in microbial communities in the water column and sediment of saline meromictic Lake Kaiike (Japan), as determined by a 16S rDNA-based analysis, and related to physicochemical gradients. Environmental Microbiology 6: 622–637.
Kroes, I., P. W. Lepp & D. A. Relman, 1999. Bacterial diversity within the human subgingival crevice. Proceedings of the National Academy of Sciences USA 96: 14547–14552.
Kuperman, B. I., V. E. Matey & S. B. Barlow, 2002a. Flagellate Cryptobia branchialis (Bodonida : Kinetoplastida), ectoparasite of tilapia from the Salton Sea. Hydrobiologia 473: 93–102.
Kuperman, B. I., V. E. Matey, D. M. Dexter & M. A. Tiffany, 2002b. Invertebrates of the Salton Sea: a scanning electron microscopy portfolio. Hydrobiologia 473: 203–216.
Lange, C. B. & M. A. Tiffany, 2002. The diatom flora of the Salton Sea, California. Hydrobiologia 473: 179–201.
Ley, R. E., J. K. Harris, J. Wilcox, J. R. Spear, S. R. Miller, B. M. Bebout, J. A. Maresca, D. A. Bryant, M. L. Sogin & N. R. Pace, 2006. Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Applied and Environmental Microbiology 72: 3685–3695.
Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Forster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. Konig, T. Liss, R. Lussmann, M. May, B. Nonhoff, B. Reichel, R. Strehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode & K. H. Schleifer, 2004. ARB: a software environment for sequence data. Nucleic Acids Research 32: 1363–1371.
Ma, Y. H., W. Z. Zhang, Y. F. Xue, P. J. Zhou, A. Ventosa & W. D. Grant, 2004. Bacterial diversity of the Inner Mongolian Baer Soda Lake as revealed by 16S rRNA gene sequence analyses. Extremophiles 8: 45–51.
Marti-Cardona, B., T. E. Steissberg, S. G. Schladow & S. J. Hook, 2008. Relating fish kills to upwellings and wind patterns in the Salton Sea. Hydrobiologia 604: 85–95.
Mendelsohn, M. B., W. I. Boarman, R. N. Fisher & S. A. Hathaway, 2007. Diversity of terrestrial avifauna in response to distance from the shoreline of the Salton Sea. Journal of Arid Environments 68: 574–587.
Mesbah, N. M., S. H. Abou-El-Ela & J. Wiegel, 2007. Novel and unexpected prokaryotic diversity in water and sediments of the alkaline, hypersaline lakes of the Wadi An Natrun, Egypt. Microbial Ecology 54: 598–617.
Moreau, M. F., J. Surico-Bennett, M. Vicario-Fisher, D. Crane, R. Gerads, R. M. Gersberg & S. H. Hurlbert, 2007. Contaminants in tilapia (Oreochromis mossambicus) from the Salton Sea, California, in relation to human health, piscivorous birds and fish meal production. Hydrobiologia 576: 127–165.
Muylaert, K., K. Van der Gucht, N. Vloemans, L. D. Meester, M. Gillis & W. Vyverman, 2002. Relationship between bacterial community composition and bottom-up versus top-down variables in four eutrophic shallow lakes. Applied and Environmental Microbiology 68: 4740–4750.
Muyzer, G., A. Teske, C. O. Wirsen & H. W. Jannasch, 1995. Phylogenetic-relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel-electrophoresis of 16s rDNA fragments. Archives of Microbiology 164: 165–172.
Oglesby, L. C., 2005. The Salton Sea geology, history, potential problems, politics and possible futures of an unnatural desert salt lake. Southern California Academy of Sciences, Claremont, CA.
Olsen, A. B., J. Mikalsen, M. Rode, A. Alfjorden, E. Hoel, K. Straum-Lie, R. Haldorsen & D. J. Colquhoun, 2006. A novel systemic granulomatous inflammatory disease in farmed Atlantic cod, Gadus morhua L., associated with a bacterium belonging to the genus Francisella. Journal of Fish Diseases 29: 307–311.
Phillips, B. M., B. S. Anderson, J. W. Hunt, R. S. Tjeerdema, M. Carpio-Obeso & V. Connor, 2007. Causes of water toxicity to Hyalella azteca in the New River, California, USA. Environmental Toxicology and Chemistry 26: 1074–1079.
Posada, D. & K. A. Crandall, 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817–818.
Rappé, M. S., P. F. Kemp & S. J. Giovannoni, 1997. Phylogenetic diversity of marine coastal picoplankton 16S rRNA genes cloned from the continental shelf off Cape Hatteras, North Carolina. Limnology and Oceanography 42: 811–826.
Rappé, M. S., K. Vergin & S. J. Giovannoni, 2000. Phylogenetic comparisons of a coastal bacterioplankton community with its counterparts in open ocean and freshwater systems. FEMS Microbiology Ecology 33: 219–232.
Rees, H. C., W. D. Grant, B. E. Jones & S. Heaphy, 2004. Diversity of Kenyan soda lake alkaliphiles assessed by molecular methods. Extremophiles 8: 63–71.
Reifel, K. M., M. P. McCoy, M. A. Tiffany, T. E. Rocke, C. C. Trees, S. B. Barlow, D. J. Faulkner & S. H. Hurlbert, 2001. Pleurochrysis pseudoroscoffensis (Prymnesiophyceae) blooms on the surface of the Salton Sea, California. Hydrobiologia 466: 177–185.
Reifel, K. M., M. P. McCoy, T. E. Rocke, M. A. Tiffany, S. H. Hurlbert & D. J. Faulkner, 2002. Possible importance of algal toxins in the Salton Sea, California. Hydrobiologia 473: 275–292.
Riedel, R., L. Caskey & B. A. Costa-Pierce, 2002. Fish biology and fisheries ecology of the Salton Sea, California. Hydrobiologia 473: 229–244.
Robertson, D. M., S. G. Schladow & G. C. Holdren, 2008. Long-term changes in the phosphorus loading to and trophic state of the Salton Sea, California. Hydrobiologia 604: 21–36.
Rogerson, A. & G. Hauer, 2002. Naked amoebae (Protozoa) of the Salton Sea, California. Hydrobiologia 473: 161–177.
Sapozhnikova, Y., O. Bawardi & D. Schlenk, 2004. Pesticides and PCBs in sediments and fish from the Salton Sea, California, USA. Chemosphere 55: 797–809.
Schloss, P. D. & J. Handelsman, 2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied and Environmental Microbiology 71: 1501–1506.
Schroeder, R. A., W. H. Orem & Y. K. Kharaka, 2002. Chemical evolution of the Salton Sea, California: nutrient and selenium dynamics. Hydrobiologia 473: 23–45.
Shuford, W. D., N. Warnock, K. C. Molina & K. K. Sturm, 2002. The Salton Sea as critical habitat to migratory and resident waterbirds. Hydrobiologia 473: 255–274.
Simpson, E. P., M. R. Gonzalez, C. M. Hart & S. H. Hurlbert, 1998. Salinity and fish effects on Salton Sea microecosystems: benthos. Hydrobiologia 381: 153–177.
Singleton, D. R., M. A. Furlong, S. L. Rathbun & W. B. Whitman, 2001. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Applied and Environmental Microbiology 67: 4374–4376.
Suzuki, M. T., O. Beja, L. T. Taylor & E. F. DeLong, 2001. Phylogenetic analysis of ribosomal RNA operons from uncultivated coastal marine bacterioplankton. Environmental Microbiology 3: 323–331.
Swan, B. K., J. M. Watts, K. M. Reifel & S. H. Hurlbert, 2007. Role of the polychaete Neanthes succinea in phosphorus regeneration from sediments in the Salton Sea, California. Hydrobiologia 576: 111–125.
Swofford, D. L., 1998. PAUP*: Phylogenetic analysis using parsimony (and other methods), V. 4.0, Beta 8. Sinauer Associates, Champaign, IL.
Tiffany, M. A., S. B. Barlow, V. E. Matey & S. H. Hurlbert, 2001. Chattonella marina (Raphidophyceae), a potentially toxic alga in the Salton Sea, California. Hydrobiologia 466: 187–194.
Walker, B., R. Whitney & G. Barlow, 1961. The fishes of the Salton Sea. In Walker, B. (ed.), The Ecology of the Salton Sea, California, in Relation to the Sportfishery. Department of Fish and Game, State of California: 77–92.
Ward, B. B., D. P. Martino, M. C. Diaz & S. B. Joye, 2000. Analysis of ammonia-oxidizing bacteria from hypersaline Mono Lake, California, on the basis of 16S rRNA sequences. Applied and Environmental Microbiology 66: 2873–2881.
Watts, J. M., B. K. Swan, M. A. Tiffany & S. H. Hurlbert, 2001. Thermal, mixing, and oxygen regimes of the Salton Sea, California, 1997–1999. Hydrobiologia 466: 159–176.
Wolny, J., K. Steidinger, M. A. Tiffany & M. Garrett, 2006. Dramatic blooms of a bioluminescent dinoflagellate and a potentially toxic prymnesiophyte in the Salton Sea, California. Journal of Phycology 42: 32–33.
Wood, A. M., S. R. Miller, W. K. W. Li & R. W. Castenholz, 2002. Preliminary studies of cyanobacteria, picoplankton, and virioplankton in the Salton Sea with special attention to phylogenetic diversity among eight strains of filamentous cyanobacteria. Hydrobiologia 473: 77–92.
Wu, Q. L., G. Zwart, M. Schauer, M. P. Kamst-van Agterveld & M. W. Hahn, 2006. Bacterioplankton community composition along a salinity gradient of sixteen high-mountain lakes located on the Tibetan Plateau, China. Applied and Environmental Microbiology 72: 5478–5485.
Yu, Y., Q. Yan & W. Feng, 2008. Spatiotemporal heterogeneity of plankton communities in Lake Donghu, China, as revealed by PCR-denaturing gradient gel electrophoresis and its relation to biotic and abiotic factors. FEMS Microbiology Ecology 63: 328–337.
Zhou, J., M. Bruns & J. Tiedje, 1996. DNA recovery from soils of diverse composition. Applied and Environmental Microbiology 62:316–322.
Acknowledgments
This work was supported by California State University, Long Beach, start-up funds and SCAC support as well as CSU Program in Education and Research in Biotechnology (CSUPERB) funding to J.G.D and Howard Hughes Medical Institute student thesis fellowship funding to L.M.M. We would like to thank the Salton Sea Authority for the use of their boat and personnel assistance and Dr. Stuart Hurlbert for introducing us to the Salton Sea during his Limnology class field trip in Fall 2004. We thank Dr. Simon Malcomber for fruitful discussions of these data and assistance with Bayesian phylogenetic analyses run on the computer-processing cluster at the University of Missouri, St. Louis. We thank Brandon Swan and Thuy Vo for assistance in sample collection in the field. We acknowledge the helpful suggestions for improvement of the manuscript by the editor and two anonymous reviewers.
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Dillon, J.G., McMath, L.M. & Trout, A.L. Seasonal changes in bacterial diversity in the Salton Sea. Hydrobiologia 632, 49–64 (2009). https://doi.org/10.1007/s10750-009-9827-4
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DOI: https://doi.org/10.1007/s10750-009-9827-4