Abstract
Lake Lucero is a gypsum-rich, hypersaline, ephemeral playa located on the southern part of the Alkali Flat at the White Sands National Monument (WSNM), New Mexico, USA. This modern playa setting provides a dynamic extreme environment that changes from a freshwater lake to a hypersaline dry desert during the year. We investigated the microbial diversity (bacteria, archaea, and microbial eukaryotes) of the Lake Lucero sediments using 16S- and 18S-based amplicon sequencing approach and explored the diversity patterns in different geochemical microenvironments. Our results indicated that similar microbial communities, in particular bacterial communities colonized, were remarkably consistent across our depth profiles. Therefore, these communities show a first-order relevance on the environmental conditions (moisture content, oxygen content, and mineral composition). We found that Proteobacteria, Actinobacteria, Bacteroidetes, Firmicutes, and Gemmatimonadetes were the major bacterial phyla, while Cyanobacteria were present in relatively low abundances and appeared only at the surface. Genus level assessment reflected that Truepera, Delftia, and Pseudomonas were the predominant bacterial genera across all samples. Euryarchaeota was the major archaeal phylum in all the samples, while Candidatus Halobonum and Candidatus Nitrososphaera were the main genera. Diatoms were the dominant eukaryotic group in surface samples and Fungi, Ciliophora, Metazoa, and Nematodes were the other major groups. As expected, metabolic inference indicated that aerobic microbial communities were near surface colonizers, with anaerobic communities dominating with increasing depth. We demonstrated that these microbial communities could be used to characterize unique geochemical microenvironments enabling us to extrapolate these results into other terrestrial and possibly extraterrestrial environments with comparable geochemical characteristics.
Similar content being viewed by others
References
Langford RP (2003) The Holocene history of the White Sands dune field and influences on eolian deflation and playa lakes. Quat Int 104:31–39
Szynkiewicz A, Ewing RC, Moore CH, Glamoclija M, Bustos D, Pratt LM (2010) Origin of terrestrial gypsum dunes—implications for Martian gypsum-rich dunes of Olympia Undae. Geomorphology 121:69–83
Glamoclija M, Fogel ML, Steele A, Kish A (2012) Microbial nitrogen and sulfur cycles at the gypsum dunes of White Sands National Monument, New Mexico. Geomicrobiol J 29:733–751
Glamoclija M, Steele A, Starke V, Zeidan M, Potochniak S, Sirisena K, Widanagamage IH (2016) Microbial signatures in sulfate-rich playas. Biosignature preservation and detection in mars analog environments (Vol. 1912). https://adsabs.harvard.edu/abs/2016LPICo1912.2051G
Grotzinger JP, Arvidson R, Bell J, Calvin W, Clark B, Fike D, Golombek M, Greeley R, Haldemann A, Herkenhoff K (2005) Stratigraphy and sedimentology of a dry to wet eolian depositional system, Burns formation, Meridiani Planum, Mars. Earth Planet Sci Lett 240:11–72
Andrews‐Hanna JC, Zuber MT, Arvidson RE, Wiseman SM (2010) Early mars hydrology: Meridiani playa deposits and the sedimentary record of Arabia Terra. J Geophys Res Planets 115(E6). https://doi.org/10.1029/2009JE003485
Malin MC, Edgett KS (2003) Evidence for persistent flow and aqueous sedimentation on early Mars. Science 302:1931–1934
Squyres S, Grotzinger J, Arvidson R, Bell J, Calvin W, Christensen P, Clark B, Crisp J, Farrand W, Herkenhoff KE (2004) In situ evidence for an ancient aqueous environment at Meridiani Planum, Mars. Science 306:1709–1714
Shields LM, Mitchell C, Drouet F (1957) Alga-and lichen-stabilized surface crusts as soil nitrogen sources. Am J Bot:489–498
Kocurek G, Carr M, Ewing R, Havholm KG, Nagar Y, Singhvi A (2007) White Sands Dune Field, New Mexico: age, dune dynamics and recent accumulations. Sediment Geol 197:313–331
Lichvar R, Brostoff W, Sprecher S (2006) Surficial features associated with ponded water on playas of the arid southwestern United States: indicators for delineating regulated areas under the Clean Water Act. Wetlands 26:385–399
Kidron GJ, Monger HC, Vonshak A, Conrod W (2012) Contrasting effects of microbiotic crusts on runoff in desert surfaces. Geomorphology 139:484–494
Navarro JB, Moser DP, Flores A, Ross C, Rosen MR, Dong H, Zhang G, Hedlund BP (2009) Bacterial succession within an ephemeral hypereutrophic Mojave Desert playa Lake. Microb Ecol 57:307–320
Rasuk MC, Kurth D, Flores MR, Contreras M, Novoa F, Poire D, Farias ME (2014) Microbial characterization of microbial ecosystems associated to evaporites domes of gypsum in Salar de Llamara in Atacama desert. Microb Ecol 68:483–494
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
Eigenbrode J, Benning LG, Maule J, Wainwright N, Steele A, Amundsen HE (2009) A field-based cleaning protocol for sampling devices used in life-detection studies. Astrobiology 9:455–465
Solorzano L (1969) Determination of ammonia in natural waters by the phenol hypochlorite method. Limnol Oceanogr 14:799–801. https://doi.org/10.4319/lo.1969.14.5.0799
DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci 89:5685–5689
Broderick NA, Raffa KF, Goodman RM, Handelsman J (2004) Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol 70:293–300
Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74:2461–2470
Teske A, Hinrichs K-U, Edgcomb V, de Vera GA, Kysela D, Sylva SP, Sogin ML, Jannasch HW (2002) Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. Appl Environ Microbiol 68:1994–2007
García-Maldonado JQ, Bebout BM, Everroad RC, López-Cortés A (2015) Evidence of novel phylogenetic lineages of methanogenic archaea from hypersaline microbial mats. Microb Ecol 69:106–117
Forget N, Murdock S, Juniper S (2010) Bacterial diversity in Fe-rich hydrothermal sediments at two South Tonga Arc submarine volcanoes. Geobiology 8:417–432
Wada H, Satoh N (1994) Details of the evolutionary history from invertebrates to vertebrates, as deduced from the sequences of 18S rDNA. Proc Natl Acad Sci 91:1801–1804
Zhao B, Chen M, Sun Y, Yang J, Chen F (2011) Genetic diversity of picoeukaryotes in eight lakes differing in trophic status. Can J Microbiol 57:115–126
Maza-Márquez P, González-Martínez A, Martínez-Toledo M, Fenice M, Lasserrot A, González-López J (2017) Biotreatment of industrial olive washing water by synergetic association of microalgal-bacterial consortia in a photobioreactor. Environ Sci Pollut Res 24:527–538
Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499
Carnegie RB, Meyer GR, Blackbourn J, Cochennec-Laureau N, Berthe FC, Bower SM (2003) Molecular detection of the oyster parasite Mikrocytos mackini, and a preliminary phylogenetic analysis. Dis Aquat Org 54:219–227
Abbott CL, Gilmore SR, Lowe G, Meyer G, Bower S (2011) Sequence homogeneity of internal transcribed spacer rDNA in Mikrocytos mackini and detection of Mikrocytos sp. in a new location. Dis Aquat Org 93:243–250
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624
Itoh H, Navarro R, Takeshita K, Tago K, Hayatsu M, Hori T, Kikuchi Y (2014) Bacterial population succession and adaptation affected by insecticide application and soil spraying history. Front Microbiol 5:457
Pylro VS, Roesch LFW, Morais DK, Clark IM, Hirsch PR, Tótola MR (2014) Data analysis for 16S microbial profiling from different benchtop sequencing platforms. J Microbiol Methods 107:30–37
Wu L, Wen C, Qin Y, Yin H, Tu Q, Van Nostrand JD, Yuan T, Yuan M, Deng Y, Zhou J (2015) Phasing amplicon sequencing on Illumina Miseq for robust environmental microbial community analysis. BMC Microbiol 15:125
Auld RR, Mykytczuk NC, Leduc LG, Merritt TJ (2016) Seasonal variation in an acid mine drainage microbial community. Can J Microbiol 63:137–152. https://doi.org/10.1139/cjm-2016-0215
Weekers P, Gast RJ, Fuerst PA, Byers TJ (1994) Sequence variations in small-subunit ribosomal RNAs of Hartmannella Vermiformis and their phylogenetic implications. Mol Biol Evol 11:684–690
Garcia-Mazcorro JF, Mills D, Noratto G (2016) Molecular exploration of fecal microbiome in quinoa-supplemented obese mice. FEMS Microbiol Ecol 92:fiw089
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200
Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-Ε, Plymouth
Arndt D, Xia J, Liu Y, Zhou Y, Guo AC, Cruz JA, Sinelnikov I, Budwill K, Nesbø CL, Wishart DS (2012) METAGENassist: a comprehensive web server for comparative metagenomics. Nucleic Acids Res 40:W88–W95
Hollister EB, Engledow AS, Hammett AJM, Provin TL, Wilkinson HH, Gentry TJ (2010) Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments. ISME J 4:829–838
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
Farías M, Contreras M, Rasuk M, Kurth D, Flores M, Poire D, Novoa F, Visscher P (2014) Characterization of bacterial diversity associated with microbial mats, gypsum evaporites and carbonate microbialites in thalassic wetlands: Tebenquiche and La Brava, Salar de Atacama, Chile. Extremophiles 18:311–329
Schneider D, Arp G, Reimer A, Reitner J, Daniel R (2013) Phylogenetic analysis of a microbialite-forming microbial mat from a hypersaline lake of the Kiritimati Atoll, Central Pacific. PLoS One 8:e66662
Ochsenreiter T, Pfeifer F, Schleper C (2002) Diversity of Archaea in hypersaline environments characterized by molecular-phylogenetic and cultivation studies. Extremophiles 6:267–274
Ara I, Daram D, Baljinova T, Yamamura H, Hozzein W, Bakir M, Suto M (2013) Isolation, classification, phylogenetic analysis and scanning electron microscopy of halophilic, halotolerant and alkaliphilic actinomycetes isolated from hypersaline soil. Afr J Microbiol Res 7:298–308
Stivaletta N, Barbieri R, Cevenini F, Lopez-Garcia P (2011) Physicochemical conditions and microbial diversity associated with the evaporite deposits in the Laguna de la Piedra (Salar de Atacama, Chile). Geomicrobiol J 28:83–95
Sahl JW, Pace NR, Spear JR (2008) Comparative molecular analysis of endoevaporitic microbial communities. Appl Environ Microbiol 74:6444–6446
Pikuta EV, Detkova EN, Bej AK, Marsic D, Hoover RB (2003) Anaerobic halo-alkaliphilic bacterial community of athalassic, hypersaline Mono Lake and Owens Lake in California. Astronomical Telescopes and Instrumentation. International Society for Optics and Photo-Dermatology, pp. 130–144
Cockell C, Osinski G, Banerjee N, Howard K, Gilmour I, Watson J (2010) The microbe–mineral environment and gypsum neogenesis in a weathered polar evaporite. Geobiology 8:293–308
Swan BK, Ehrhardt CJ, Reifel KM, Moreno LI, Valentine DL (2010) Archaeal and bacterial communities respond differently to environmental gradients in anoxic sediments of a California hypersaline lake, the Salton Sea. Appl Environ Microbiol 76:757–768
Kim JS, Makama M, Petito J, Park NH, Cohan FM, Dungan RS (2012) Diversity of bacteria and archaea in hypersaline sediment from Death Valley National Park, California. Microbiol Open 1:135–148
Spring S, Brinkmann N, Murrja M, Spröer C, Reitner J, Klenk H-P (2015) High diversity of culturable prokaryotes in a lithifying hypersaline microbial mat. Geomicrobiol J 32:332–346
Sixt BS, Siegl A, Müller C, Watzka M, Wultsch A, Tziotis D, Montanaro J, Richter A, Schmitt-Kopplin P, Horn M (2013) Metabolic features of Protochlamydia amoebophila elementary bodies—a link between activity and infectivity in Chlamydiae. PLoS Pathog 9:e1003553
Cho JC, Janssen PH, Costa KC, Hedlund BP (2011) Opitutae. Bergey's manual of systematics of archaea and bacteria.https://doi.org/10.1002/9781118960608.cbm00052
Rasuk MC, Fernández AB, Kurth D, Contreras M, Novoa F, Poiré D, Farías ME (2016) Bacterial diversity in microbial mats and sediments from the Atacama Desert. Microb Ecol 71:44–56
Farías ME, Rascovan N, Toneatti DM, Albarracín VH, Flores MR, Poiré DG, Collavino MM, Aguilar OM, Vazquez MP, Polerecky L (2013) The discovery of stromatolites developing at 3570 m above sea level in a high-altitude volcanic lake Socompa, Argentinean Andes. PLoS One 8:e53497
Volkmann M, Gorbushina AA, Kedar L, Oren A (2006) Structure of euhalothece-362, a novel red-shifted mycosporine-like amino acid, from a halophilic cyanobacterium (Euhalothece sp.). FEMS Microbiol Lett 258:50–54
Kedar L, Kashman Y, Oren A (2002) Mycosporine-2-glycine is the major mycosporine-like amino acid in a unicellular cyanobacterium (Euhalothece sp.) isolated from a gypsum crust in a hypersaline saltern pond. FEMS Microbiol Lett 208:233–237
Samylina O, Gerasimenko L (2011) Fossilization of the cells of natronophilic endoevaporite cyanobacterium ‘Euhalothece natronophila’ in a modelling system. Microbiology 80:525–534
Mikhodyuk O, Gerasimenko L, Akimov V, Ivanovsky R, Zavarzin G (2008) Ecophysiology and polymorphism of the unicellular extremely natronophilic cyanobacterium Euhalothece sp. Z-M001 from Lake Magadi. Microbiology 77:717–725
Cockell CS, Schuerger AC, Billi D, Friedmann EI, Panitz C (2005) Effects of a simulated martian UV flux on the cyanobacterium, Chroococcidiopsis sp. 029. Astrobiology 5:127–140
Billi D, Friedmann EI, Hofer KG, Caiola MG, Ocampo-Friedmann R (2000) Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol 66:1489–1492
Chastain RA, Stewart JG (1985) Studies on Berkeleya hyalina (Round & Brooks) Cox, a marine tube-forming diatom. Phycologia 24:83–92
Lobban CS (1985) Marine tube-dwelling diatoms of the Pacific coast of North America. I. Berkeleya, Haslea, Nitzschia, and Navicula sect. Microstigmaticae. Can J Bot 63:1779–1784
Swingley WD, Chen M, Cheung PC, Conrad AL, Dejesa LC, Hao J, Honchak BM, Karbach LE, Kurdoglu A, Lahiri S (2008) Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina. Proc Natl Acad Sci 105:2005–2010
Nübel U, Garcia-Pichel F, Muyzer G (2000) The halotolerance and phylogeny of cyanobacteria with tightly coiled trichomes (Spirulina Turpin) and the description of Halospirulina tapeticola gen. nov., sp. nov. Int J Syst Evol Microbiol 50:1265–1277
Ferris F, Fratton C, Gerits J, Schultze-Lam S, Lollar BS (1995) Microbial precipitation of a strontium calcite phase at a groundwater discharge zone near Rock Creek, British Columbia, Canada. Geomicrobiol J 13:57–67
Abdallah MB, Karray F, Mhiri N, Mei N, Quéméneur M, Cayol J-L, Erauso G, Tholozan J-L, Alazard D, Sayadi S (2016) Prokaryotic diversity in a Tunisian hypersaline lake, Chott El Jerid. Extremophiles 20:125–138
Bowman JP, McCammon SA, Rea SM, McMeekin TA (2000) The microbial composition of three limnologically disparate hypersaline Antarctic lakes. FEMS Microbiol Lett 183:81–88
Ugalde JA, Narasingarao P, Kuo S, Podell S, Allen EE (2013) Draft genome sequence of “Candidatus Halobonum tyrrellensis” strain G22, isolated from the hypersaline waters of Lake Tyrrell, Australia. Genome Announc 1:e01001–e01013
Spang A, Poehlein A, Offre P, Zumbrägel S, Haider S, Rychlik N, Nowka B, Schmeisser C, Lebedeva EV, Rattei T (2012) The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ Microbiol 14:3122–3145
Jiang H, Huang Q, Dong H, Wang P, Wang F, Li W, Zhang C (2010) RNA-based investigation of ammonia-oxidizing archaea in hot springs of Yunnan Province, China. Appl Environ Microbiol 76:4538–4541
Cui H-L, Li X-Y, Gao X, X-W X, Zhou Y-G, Liu H-C, Oren A, Zhou P-J (2010) Halopelagius inordinatus gen. nov., sp. nov., a new member of the family Halobacteriaceae isolated from a marine solar saltern. Int J Syst Evol Microbiol 60:2089–2093
Hezayen FF, Gutiérrez M, Steinbüchel A, Tindall BJ, Rehm BH (2010) Halopiger aswanensis sp. nov., a polymer-producing and extremely halophilic archaeon isolated from hypersaline soil. Int J Syst Evol Microbiol 60:633–637
Makhdoumi-Kakhki A, Amoozegar MA, Ventosa A (2012) Halovenus aranensis gen. nov., sp. nov., an extremely halophilic archaeon from Aran-Bidgol salt lake. Int J Syst Evol Microbiol 62:1331–1336
Roh SW, Nam Y-D, Nam S-H, Choi S-H, Park H-S, Bae J-W (2010) Complete genome sequence of Halalkalicoccus jeotgali B3T, an extremely halophilic archaeon. J Bacteriol 192:4528–4529
Buchalo AS, Nevo E, Wasser SP, Oren A, Molitoris HP (1998) Fungal life in the extremely hypersaline water of the Dead Sea: first records. Proc R Soc Lond B Biol Sci 265:1461–1465
Jones E, Sakayaroj J, Suetrong S, Somrithipol S, Pang K (2009) Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Divers 35:187
Liu K, Ding X, Wang H-F, Zhang X, Hozzein WN, Wadaan MA, Lan A, Zhang B, Li W (2014) Eukaryotic microbial communities in hypersaline soils and sediments from the alkaline hypersaline Huama Lake as revealed by 454 pyrosequencing. Antonie Van Leeuwenhoek 105:871–880
Takai K, Moser DP, Onstott TC, Spoelstra N, Pfiffner SM, Dohnalkova A, Fredrickson JK (2001) Alkaliphilus transvaalensis gen. nov., sp. nov., an extremely alkaliphilic bacterium isolated from a deep South African gold mine. Int J Syst Evol Microbiol 51:1245–1256
Takai K (2011) Limits of life and the biosphere: lessons from the detection of microorganisms in the deep sea and deep subsurface of the Earth. Origins and evolution of life: an astrobiological perspective, Cambridge Univeristy Press, Cambridge, pp 469–486
Zhilina T, Zavarzina D, Kolganova T, Lysenko A, Tourova T (2009) Alkaliphilus peptidofermentans sp. nov., a new alkaliphilic bacterial soda lake isolate capable of peptide fermentation and Fe (III) reduction. Microbiology 78:445–454
Moune S, Eatock C, Matheron R, Willison JC, Hirschler A, Herbert R, Caumette P (2000) Orenia salinaria sp. nov., a fermentative bacterium isolated from anaerobic sediments of Mediterranean salterns. Int J Syst Evol Microbiol 50:721–729
Vanparys B, Heylen K, Lebbe L, De Vos P (2005) Devosia limi sp. nov., isolated from a nitrifying inoculum. Int J Syst Evol Microbiol 55:1997–2000
Rivas R, Willems A, Subba-Rao NS, Mateos PF, Dazzo FB, Kroppenstedt RM, Martínez-Molina E, Gillis M, Velázquez E (2003) Description of Devosia neptuniae sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India. Syst Appl Microbiol 26:47–53
Acknowledgements
We would like to thank Kimberly Wirtz and David Bustos (NPS White Sands) and Verena Starke (Geophysical Laboratory, Carnegie Institution of Washington) for their invaluable help during the field season.
Funding
This work was supported by NASA-ASTEP NNX14AT28G grant to M.G.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that there are no conflicts of interests.
Electronic Supplementary Material
ESM 1
(DOCX 253 kb)
Rights and permissions
About this article
Cite this article
Sirisena, K.A., Ramirez, S., Steele, A. et al. Microbial Diversity of Hypersaline Sediments from Lake Lucero Playa in White Sands National Monument, New Mexico, USA. Microb Ecol 76, 404–418 (2018). https://doi.org/10.1007/s00248-018-1142-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-018-1142-z