Abstract
Ephemerally wet playas are conspicuous features of arid landscapes worldwide; however, they have not been well studied as habitats for microorganisms. We tracked the geochemistry and microbial community in Silver Lake playa, California, over one flooding/desiccation cycle following the unusually wet winter of 2004–2005. Over the course of the study, total dissolved solids increased by ∽10-fold and pH increased by nearly one unit. As the lake contracted and temperatures increased over the summer, a moderately dense planktonic population of ∽1 × 106 cells ml−1 of culturable heterotrophs was replaced by a dense population of more than 1 × 109 cells ml−1, which appears to be the highest concentration of culturable planktonic heterotrophs reported in any natural aquatic ecosystem. This correlated with a dramatic depletion of nitrate as well as changes in the microbial community, as assessed by small subunit ribosomal RNA gene sequencing of bacterial isolates and uncultivated clones. Isolates from the early-phase flooded playa were primarily Actinobacteria, Firmicutes, and Bacteroidetes, yet clone libraries were dominated by Betaproteobacteria and yet uncultivated Actinobacteria. Isolates from the late-flooded phase ecosystem were predominantly Proteobacteria, particularly alkalitolerant isolates of Rhodobaca, Porphyrobacter, Hydrogenophaga, Alishwenella, and relatives of Thauera; however, clone libraries were composed almost entirely of Synechococcus (Cyanobacteria). A sample taken after the playa surface was completely desiccated contained diverse culturable Actinobacteria typically isolated from soils. In total, 205 isolates and 166 clones represented 82 and 44 species-level groups, respectively, including a wide diversity of Proteobacteria, Bacteroidetes, Actinobacteria, Firmicutes, Gemmatimonadetes, Acidobacteria, and Cyanobacteria.
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References
Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
Benlloch S, Lopez-Lopez A, Casamayor EO, Ovreas L, Goddard V, Daae FL, Smerdon G, Massana R, Joint I, Thingstad F, Pedros-Alio C, Rodriguez-Valera F (2002) Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ Microbiol 4:349–360
Blum JS, Stolz JF, Oren A, Oremland RS (2001) Selenihalanaerobacter shriftii gen. nov., sp. nov., a halophilic anaerobe from Dead Sea sediments that respires selenate. Arch Microbiol 175:208–219
Boldareva EN, Briantseva IA, Tsapin A, Nelson K, Sorokin D, Turova TP, Boichenko VA, Stadnichuk IN, Gorlenko VM (2007) The new bacteriochlorophyll a-containing bacterium Roseinatronobacter monicus sp. nov. from the hypersaline soda Mono Lake (California, United States). Mikrobiologiia 76:95–106
Borsodi AK, Micsinai A, Rusznyak A, Vladar P, Kovacs G, Toth EM, Marialigeti K (2005) Diversity of alkaliphilic and alkalitolerant bacteria cultivated from decomposing reed rhizomes in a Hungarian soda lake. Microb Ecol 50:9–18
Brettar I, Christen R, Höfle MG (2004) Belliella baltica gen. nov., sp. nov., a novel marine bacterium of the Cytophaga–Flavobacterium–Bacteroides group isolated from surface water of the central Baltic Sea. Int J Syst Evol Microbiol 54:65–70
Brosius J, Palmer ML, Kennedy PJ, Noller HF (1978) Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci U S A 75:4801–4805
Bruns A, Philipp H, Cypionka H, Brinkhoff T (2003) Aeromicrobium marinum sp. nov., an abundant pelagic bacterium isolated from the German Wadden Sea. Int J Syst Evol Microbiol 53:1917–1923
Casamayor EO, Massana R, Benlloch S, Øvreas L, Diez B, Goddard VJ, Gasol JM, Joint I, Rodriguez-Valera F, Pedros-Alio C (2002) Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environ Microbiol 4:338–348
Caton TM, Witte LR, Ngyuen HD, Buchheim JA, Buchheim MA, Schneegurt MA (2004) Halotolerant aerobic heterotrophic bacteria from the Great Salt Plains of Oklahoma. Microb Ecol 48:449–462
Crowley JK, Hook SJ (1996) Mapping playa evaporite minerals and associated sediments in Death Valley, California, with multispectral thermal infrared images. J Geophys Res B: Solid Earth 101:643–660
de Man JC (1975) The probability of most probable numbers. Appl Microbiol Biotechnol 1:67–78
Demergasso C, Casamayor EO, Chong G, Galleguillos P, Escudero L, Pedros-Alio C (2004) Distribution of prokaryotic genetic diversity in athalssohaline lakes of the Atacama Desert, Northern Chile. FEMS Microbiol Ecol 48:57–69
Dong H, Zhang G, Jiang H, Yu B, Chapman LR, Lucas CR, Fields MW (2006) Microbial diversity in sediments of saline Qinghai Lake, China: linking geochemical controls to microbial ecology. Microb Ecol 51:65–82
Eder W, Jahnke LL, Schmidt M, Huber R (2001) Microbial diversity of the brine–seawater interface of the Kebrit Deep, Red Sea, studied via 16S rRNA gene sequences and cultivation methods. Appl Environ Microbiol 67:3077–3085
Eder W, Ludwig W, Huber R (1999) Novel 16S rRNA gene sequences retrieved from highly saline brine sediments of Kebrit Deep, Red Sea. Arch Microbiol 172:213–218
Eiler A, Farnleitner AH, Zechmeister TC, Herzig A, Hurban C, Wesner W, Krachler R, Velimirov B, Kirschner AK (2003) Factors controlling extremely productive heterotrophic bacterial communities in shallow soda pools. Microb Ecol 46:43–54
Elevi Bardavid R, Khristo P, Oren A (2008) Interrelationships between Dunaliella and halophilic prokaryotes in saltern crystallizer ponds. Extremophiles 12:5–14
Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56:340–373
Fenchel T, King GM, Blackburn TH (1998) Bacterial biogeochemistry: The ecophysiology of mineral cycling, 2nd edn. Elsevier, San Diego
Fisher JC, Hollibaugh JT (2008) Selenate-dependent anaerobic arsenite oxidation by a bacterium from Mono Lake, California. Appl Environ Microbiol 74:2588–2594
Frund C, Cohen Y (1992) Diurnal cycles of sulfate reduction under oxic conditions in cyanobacterial mats. Appl Environ Microbiol 58:70–77
Hahn MW, Lunsdorf H, Wu Q, Schauer M, Höfle MG, Boenigk J, Stadler P (2003) Isolation of novel ultramicrobacteria classified as actinobacteria from five freshwater habitats in Europe and Asia. Appl Environ Microbiol 69:1442–1451
Heider J, Fuchs G (2005) Thauera. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology, vol. 2C. Springer, New York, pp 907–913
Hollibaugh JT, Budinoff C, Hollibaugh RA, Ransom B, Bano N (2006) Sulfide oxidation coupled to arsenate reduction by a diverse microbial community in a soda lake. Appl Environ Microbiol 72:2043–2049
Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319
Humayoun SB, Bano N, Hollibaugh JT (2003) Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Appl Environ Microbiol 69:1030–1042
Jiang H, Dong H, Zhang G, Yu B, Chapman LR, Fields MW (2006) Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Appl Environ Microbiol 72:3832–3845
Jiang S, Steward G, Jellison R, Chu W, Choi S (2004) Abundance, distribution, and diversity of viruses in alkaline, hypersaline Mono Lake, California. Microb Ecol 47:9–17
Johnson DB, Rolfe S, Hallberg KB, Iversen E (2001) Isolation and phylogenetic characterization of acidophilic microorganisms indigenous to acidic drainage waters at an abandoned Norwegian copper mine. Environ Microbiol 3:630–637
Kallas T, Coursin T, Rippka R (1985) Different organization of nif genes in nonheterocystous and heterocystous cyanobacteria. Plant Mol Biol 5:321–329
Kanagawa T (2003) Bias and artifacts in multitemplate polymerase chain reactions (PCR). J Biosci Bioeng 96:317–323
Kulp TR, Hoeft SE, Miller LG, Saltikov C, Murphy JN, Han S, Lanoil B, Oremland RS (2006) Dissimilatory arsenate and sulfate reduction in sediments of two hypersaline, arsenic-rich soda lakes: Mono and Searles Lakes, California. Appl Environ Microbiol 72:6514–6526
Ley RE, Harris JK, Wilcox J, Spear JR, Miller SR, Bebout BM, Maresca JA, Bryant DA, Sogin ML, Pace NR (2006) Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl Environ Microbiol 72:3685–3695
Liu WY, Zeng J, Wang L, Dou YT, Yang SS (2005) Halobacillus dabanensis sp. nov. and Halobacillus aidingensis sp. nov., isolated from salt lakes in Xinjiang, China. Int J Syst Evol Microbiol 55:1991–1996
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar A, Buchner A, Lai T, Steppi S, Jacob G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüßbmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371
Maidak BL, Cole JR, Lilburn TG, Parker CT Jr., Saxman PR, Farris RJ, Garrity GM, Olsen GJ, Schmidt TM, Tiedje JM (2001) The RDP-II (Ribosomal Database Project). Nucleic Acids Res 29:173–174
Mesbah NM, Abou-El-Ela SH, Wiegel J (2007) Novel and unexpected prokaryotic diversity in water and sediments of the alkaline, hypersaline lakes of the Wadi An Natrun, Egypt. Microb Ecol 54:598–617
Milford AD, Achenbach LA, Jung DO, Madigan MT (2000) Rhodobaca bogoriensis gen. nov. and sp. nov., an alkaliphilic purple nonsulfur bacterium from African Rift Valley soda lakes. Arch Microbiol 174:18–27
Minz D, Fishbain S, Green SJ, Muyzer G, Cohen Y, Rittmann BE, Stahl DA (1999) Unexpected population distribution in a microbial mat community: sulfate-reducing bacteria localized to the highly oxic chemocline in contrast to a eukaryotic preference for anoxia. Appl Environ Microbiol 65:4659–4665
Nakatsu CH, Hristova K, Hanada S, Meng XY, Hanson JR, Scow KM, Kamagata Y (2006) Methylibium petroleiphilum gen. nov., sp. nov., a novel methyl tert-butyl ether-degrading methylotroph of the Betaproteobacteria. Int J Syst Evol Microbiol 56:983–989
Neal JT (1975) Introduction. In: Neal JT (ed) Playas and dry lakes, Stroudsburg, Dowden, Hutchinson, and Ross, Inc. Benchmark Papers in Geology, pp 1–5
Nubel U, Bateson MM, Madigan MT, Kuhl M, Ward DM (2001) Diversity and distribution in hypersaline microbial mats of bacteria related to Chloroflexus spp. Appl Environ Microbiol 67:4365–4371
Nubel U, Garcia-Pichel F, Kuhl M, Muyzer G (1999) Quantifying microbial diversity: morphotypes, 16S rRNA genes, and carotenoids of oxygenic phototrophs in microbial mats. Appl Environ Microbiol 65:422–430
Oremland RS, Kulp TR, Blum JS, Hoeft SE, Baesman S, Miller LG, Stolz JF (2005) A microbial arsenic cycle in a salt-saturated, extreme environment. Science 308:1305–1308
Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348
Oren A (2000) The order halobacteriales. In: Dworkin M (ed) The prokaryotes: an evolving electronic resource for the microbobiological community, 3, release 3.7 edn, Springer-Verlag, New York
Parkhurst DL, Thorstenson DC, Plummer LN (1980) PHREEQE—a computer program for geochemical calculations: U.S. Geological Survey Water-Resources Investigations Report 80–96
Pedros-Alio C, Calderon-Paz JI, MacLean MH, Medina G, Marrase C, Gasol JM, Guixa-Boixereu N (2000) The microbial food web along salinity gradients. FEMS Microbiol Ecol 32:143–155
Ramsing NB, Kuhl M, Jorgensen BB (1993) Distribution of sulfate-reducing bacteria, O2, and H2S in photosynthetic biofilms determined by oligonucleotide probes and microelectrodes. Appl Environ Microbiol 59:3840–3849
Rappé M, Gordon DA, Vergin KL, Giovannoni SJ (1999) Phylogeny of Actinobacteria small subunit (SSU) rRNA gene clones recovered from marine bacterioplankton. Syst Appl Microbiol 22:4522–4529
Reinhold-Hurek BZT, Hurek T (2005) Azoarcus. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology, vol 2C. Springer, New York, pp 890–902
Rosen MR (1994) Paleoclimate and basin evolution of playa systems. In: Rosen MR (ed) Geological Society of America Special Paper 289. Geological Society of America, Boulder, pp 1–18
Schlesner H, Lawson PA, Collins MD, Weiss N, Wehmeyer U, Volker H, Thomm M (2001) Filobacillus milensis gen. nov., sp. nov., a new halophilic spore-forming bacterium with Orn-D-Glu-type peptidoglycan. Int J Syst Evol Microbiol 51:425–431
Sekar R, Pernthaler A, Pernthaler J, Warnecke F, Posch T, Amann R (2003) An improved protocol for quantification of freshwater Actinobacteria by fluorescence in situ hybridization. Appl Environ Microbiol 69:2928–2935
Singleton DR, Furlong MA, Rathbun SL, Whitman WB (2001) Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67:4374–4376
Sorokin D, Turova TP, Kuznetsov BB, Briantseva IA, Gorlenko VM (2000) Roseinatronobacter thiooxidans gen. nov., sp. nov., a new alkaliphilic aerobic bacteriochlorophyll-alpha-containing bacteria from a soda lake. Mikrobiologiia 69:89–97
Sorokin DY, Foti M, Pinkart HC, Muyzer G (2007) Sulfur-oxidizing bacteria in Soap Lake (Washington State), a meromictic, haloalkaline lake with an unprecedented high sulfide content. Appl Environ Microbiol 73:451–455
Staley JT, Konopka A (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346
Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the bioshere. Princeton, Princeton, NJ
Steunou AS, Bhaya D, Bateson MM, Melendrez MC, Ward DM, Brecht E, Peters JW, Kuhl M, Grossman AR (2006) In situ analysis of nitrogen fixation and metabolic switching in unicellular thermophilic cyanobacteria inhabiting hot spring microbial mats. Proc Natl Acad Sci U S A 103:2398–2403
Stevens H, Brinkhoff T, Rink B, Vollmers J, Simon M (2007) Diversity and abundance of Gram positive bacteria in a tidal flat ecosystem. Environ Microbiol 9:1810–1822
Tindall BJ, Ross HNM, Grant WD (1984) Natronobacterium gen. nov., and Natronococcus gen. nov., two genera of haloalkalophilic archaebacterium. Syst Appl Microbiol 5:41–57
von Wintzingerode F, Gobel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:213–229
Walsh DA, Papke RT, Doolittle WF (2005) Archaeal diversity along a soil salinity gradient prone to disturbance. Environ Microbiol 7:1655–1666
Warnecke F, Amann R, Pernthaler J (2004) Actinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages. Environ Microbiol 6:242–253
Wells SG, Brown WJ, Enzel Y, Anderson RY, McFadden LD (2003) Late Quaternary geology and paleohydrology of pluvial Lake Mojave, southern California. In: Enzel Y, Wells SG, Lancaster N (ed) Paleoenvironments and paleohydrology of the Mojave and southern Great Basin deserts. Geological Society of America Special Paper 368, pp 79–114
Yoon JH, Kang KH, Oh TK, Park YH (2004) Halobacillus locisalis sp. nov., a halophilic bacterium isolated from a marine solar saltern of the Yellow Sea in Korea. Extremophiles 8:23–28
Yoon JH, Kang SJ, Lee CH, Oh HW, Oh TK (2005) Halobacillus yeomjeoni sp. nov., isolated from a marine solar saltern in Korea. Int J Syst Evol Microbiol 55:2413–2417
Yoon JH, Kim IG, Schumann P, Oh TK, Park YH (2004) Marinibacillus campisalis sp. nov., a moderate halophile isolated from a marine solar saltern in Korea, with emended description of the genus Marinibacillus. Int J Syst Evol Microbiol 54:1317–1321
Acknowledgments
We are grateful to Carrie Laughead, Joy Hallmark, Journet Wallace, Peter Starkweather, Natasha Zolotova, Everett Shock, and Bilal Zaatiti for assistance in the field and laboratory. Kyle Costa helped with both field work and with changes to the figures in advanced versions of the manuscript. We also thank Frank van Breukelen for the use of equipment. We thank the following individuals for reviewing the manuscript: Ron Oremland, Eduardo Robleto, Kyle Costa, Ralph Seiler, Michael Lico, Jeremy Dodsworth, and four anonymous reviewers.
This work was supported by NSF Grant Numbers EPS-9977809, MCB-0546865, start-up funds from UNLV to BPH and from DRI to DPM, and a Las Vegas Centennial Grant to BPH. AF was supported by the TRIO McNair Summer Scholar Research Institute and JBN was supported by a fellowship through NIH Grant Number_P20 RR016464_. This publication was also made possible by support to the Nevada Genomics Center through Grant Number _P20 RR016464_ from the National Center for Research Resources (NCRR), a component of the National Institutes of Health (NIH).
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Navarro, J.B., Moser, D.P., Flores, A. et al. Bacterial Succession within an Ephemeral Hypereutrophic Mojave Desert Playa Lake. Microb Ecol 57, 307–320 (2009). https://doi.org/10.1007/s00248-008-9426-3
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DOI: https://doi.org/10.1007/s00248-008-9426-3