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Life at the hyperarid margin: novel bacterial diversity in arid soils of the Atacama Desert, Chile

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Abstract

Nearly half the earth’s surface is occupied by dryland ecosystems, regions susceptible to reduced states of biological productivity caused by climate fluctuations. Of these regions, arid zones located at the interface between vegetated semiarid regions and biologically unproductive hyperarid zones are considered most vulnerable. The objective of this study was to conduct a deep diversity analysis of bacterial communities in unvegetated arid soils of the Atacama Desert, to characterize community structure and infer the functional potential of these communities based on observed phylogenetic associations. A 454-pyrotag analysis was conducted of three unvegetated arid sites located at the hyperarid–arid margin. The analysis revealed communities with unique bacterial diversity marked by high abundances of novel Actinobacteria and Chloroflexi and low levels of Acidobacteria and Proteobacteria, phyla that are dominant in many biomes. A 16S rRNA gene library of one site revealed the presence of clones with phylogenetic associations to chemoautotrophic taxa able to obtain energy through oxidation of nitrite, carbon monoxide, iron, or sulfur. Thus, soils at the hyperarid margin were found to harbor a wealth of novel bacteria and to support potentially viable communities with phylogenetic associations to non-phototrophic primary producers and bacteria capable of biogeochemical cycling.

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Abbreviations

MAP:

Mean annual precipitation

MDRS:

Mars Desert Research Station

References

  • Aanderud ZT, Shuldman MI, Drenovsky RE, Richards JH (2008) Shrub-interspace dynamics alter relationships between microbial community composition and belowground ecosystem characteristics. Soil Biol Biochem 40:2206–2216

    Article  CAS  Google Scholar 

  • Arroyo MTK, Castor C, Marticorena C, Muñoz M, Cavieres L, Mathei O, Squeo F, Grosjean M, Rodríguez R (1998) The flora of Llullaillaco National Park located in the transitional winter–summer rainfall area of the northern Chilean Andes. Gayana Botánica 55:93–110

    Google Scholar 

  • Bachar A, Al-Ashhab A, Soares MIM, Sklarz MY, Angel R, Ungar ED, Gillor O (2010) Soil microbial abundance and diversity along a low precipitation gradient. Microb Ecol 60:453–461

    Article  PubMed  Google Scholar 

  • Belnap J, Budel B, Lange OL (2001) Biological soil crusts: characteristics and distribution. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function and management. Springer, Berlin, pp 3–30

    Chapter  Google Scholar 

  • Chanal A, Chapon V, Benzerara K, Barakat M, Christen R, Achouak W, Barras F, Heulin T (2006) The desert of Tataouine: an extreme environment that hosts a wide diversity of microorganisms and radiotolerant bacteria. Environ Microbiol 8:514–525

    Article  PubMed  CAS  Google Scholar 

  • Collins HP, Cavigelli MA (2003) Soil microbial community characteristics along an elevation gradient in the Laguna Mountains of Southern California. Soil Biol Biochem 35:1027–1037

    Article  CAS  Google Scholar 

  • Connon SA, Lester ED, Shafaat HS, Obenhuber DC, Ponce A (2007) Bacterial diversity in hyperarid Atacama Desert soils. J Geophys Res Biogeosci 112:GO4s17. doi:10.1029/2006JG000311

    Article  Google Scholar 

  • Costello EK, Schmidt SK (2006) Microbial diversity in alpine tundra wet meadow soil: novel Chloroflexi from a cold, water-saturated environment. Environ Microbiol 8:1471–1486

    Article  PubMed  CAS  Google Scholar 

  • Costello EK, Halloy SRP, Reed SC, Sowell P, Schmidt SK (2009) Fumarole-supported islands of biodiversity within a hyperarid, high-elevation landscape on Socompa Volcano, Puna de Atacama, Andes. Appl Environ Microbiol 75:735–747

    Article  PubMed  CAS  Google Scholar 

  • Davis KER, Sangwan P, Janssen PH (2011) Acidobacteria, Rubrobacteridae and Chloroflexi are abundant among very slow-growing and mini-colony-forming soil bacteria. Environ Microbiol 13:798–805

    Article  PubMed  Google Scholar 

  • de la Torre JR, Goebel BM, Friedmann EI, Pace NR (2003) Microbial diversity of cryptoendolithic communities from the McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 69:3858–3867

    Article  PubMed  Google Scholar 

  • Direito SOL, Ehrenfreund P, Marees A, Staats M, Foing B, Roling WFM (2011) A wide variety of putative extremophiles and large beta-diversity at the Mars Desert Research Station (Utah). Int J Astrobiol 10:191–207

    Article  Google Scholar 

  • Dixon JC, McLaren SJ (2009) Duricrust. In: Parsons AJ, Abrahams AD (eds) Geomorphology of desert environments, 2nd edn. Springer, Berlin

    Google Scholar 

  • Dong HL, Rech JA, Jiang HC, Sun H, Buck BJ (2007) Endolithic cyanobacteria in soil gypsum: occurrences in Atacama (Chile), Mojave (United States), and Al-Jafr Basin (Jordan) deserts. J Geophys Res Biogeosci 112:GO2030. doi:10.1029/2006JG000385

    Google Scholar 

  • Drees KP, Neilson JW, Betancourt JL, Quade J, Henderson DA, Pryor BM, Maier RM (2006) Bacterial community structure in the hyperarid core of the Atacama Desert, Chile. Appl Environ Microbiol 72:7902–7908

    Article  PubMed  CAS  Google Scholar 

  • Dunai TJ, Lopez GAG, Juez-Larre J (2005) Oligocene–Miocene age of aridity in the Atacama Desert revealed by exposure dating of erosion-sensitive landforms. Geology 33:321–324

    Article  Google Scholar 

  • Ewing SA, Michalski G, Thiemens M, Quinn RC, Macalady JL, Kohl S, Wankel SD, Kendall C, Mckay CP, Amundson R (2007) Rainfall limit of the N cycle on Earth. Glob Biogeochem Cycles 21:GB3009. doi:3010.1029/2006GB2838

    Article  Google Scholar 

  • Ewing SA, Macalady JL, Warren-Rhodes K, McKay CP, Amundson R (2008) Changes in the soil C cycle at the arid–hyperarid transition in the Atacama Desert. J Geophys Res Biogeosci 113:GO2S90. doi:10.1029/2007JG000495

    Article  Google Scholar 

  • Ezcurra E (2006) Global deserts outlook. Division of Early Warning and Assessment, United Nations Environment Programme, Nairobi, Kenya

  • Field EK, D’Imperio S, Miller AR, VanEngelen MR, Gerlach R, Lee BD, Apel WA, Peyton BM (2010) Application of molecular techniques to elucidate the influence of cellulosic waste on the bacterial community structure at a simulated low-level-radioactive-waste site. Appl Environ Microbiol 76:3106–3115

    Article  PubMed  CAS  Google Scholar 

  • Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249

    Article  PubMed  Google Scholar 

  • Holmes AJ, Bowyer J, Holley MP, O’Donoghue M, Montgomery M, Gillings MR (2000) Diverse, yet-to-be-cultured members of the Rubrobacter subdivision of the Actinobacteria are widespread in Australian arid soils. FEMS Microbiol Ecol 33:111–120

    Article  PubMed  CAS  Google Scholar 

  • Houston J, Hartley AJ (2003) The central Andean west-slope rain-shadow and its potential contribution to the origin of hyperaridity in the Atacama Desert. Int J Climatol 23:1453–1464

    Article  Google Scholar 

  • Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728

    Article  PubMed  CAS  Google Scholar 

  • Johnson DB, Bacelar-Nicolau P, Okibe N, Thomas A, Hallberg KB (2009) Ferrimicrobium acidiphilum gen. nov., sp. nov. and Ferrithrix thermotolerans gen. nov., sp. nov.: heterotrophic, iron-oxidizing, extremely acidophilic actinobacteria. Int J Syst Evol Microbiol 59:1082–1089

    Article  PubMed  CAS  Google Scholar 

  • Keijser BJ, Zaura E, Huse SM, van der Vossen JM, Schuren FH, Montijn RC, ten Cate JM, Crielaard W (2008) Pyrosequencing analysis of the oral microflora of healthy adults. J Dent Res 87:1016–1020

    Article  PubMed  CAS  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    Article  PubMed  CAS  Google Scholar 

  • Lucker S, Wagner M, Maixner F, Pelletier E, Koch H, Vacherie B, Rattei T, Damste JSS, Spieck E, Le Paslier D, Daims H (2010) A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc Natl Acad Sci USA 107:13479–13484

    Article  PubMed  Google Scholar 

  • Luebert F, Gajardo R (2000) Vegetación de los Andes áridos del norte de Chile. Lazaroa 21:111–130

    Google Scholar 

  • Maddison DR, Maddison WP (2001) MacClade 4: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Maldonado A, Betancourt JL, Latorre C, Villagran C (2005) Pollen analyses from a 50000-yr rodent midden series in the southern Atacama Desert (25°30′S). J Quat Sci 20:493–507

    Article  Google Scholar 

  • McKay CP, Friedmann EI, Gomez-Silva B, Caceres-Villanueva L, Andersen DT, Landheim R (2003) Temperature and moisture conditions for life in the extreme arid region of the Atacama Desert: four years of observations including the El Nino of 1997–1998. Astrobiology 3:393–406

    Article  PubMed  CAS  Google Scholar 

  • Mendez MO, Neilson JW, Maier RM (2008) Characterization of a bacterial community in an abandoned semiarid lead–zinc mine tailing site. Appl Environ Microbiol 74:3899–3907

    Article  PubMed  CAS  Google Scholar 

  • Middleton NJ, Thomas DSG, Programme UNE (1997) World atlas of desertification. Arnold, London

    Google Scholar 

  • Nagy ML, Perez A, Garcia-Pichel F (2005) The prokaryotic diversity of biological soil crusts in the Sonoran Desert (Organ Pipe Cactus National Monument, AZ). FEMS Microbiol Ecol 54:233–245

    Article  PubMed  CAS  Google Scholar 

  • Nicolle JLC, Simmons S, Bathe S, Norris PR (2009) Ferrous iron oxidation and rusticyanin in halotolerant, acidophilic ‘Thiobacillus prosperus’. Microbiology (UK) 155:1302–1309

    Article  CAS  Google Scholar 

  • Pointing SB, Chan Y, Lacap DC, Lau MCY, Jurgens JA, Farrell RL (2010) Highly specialized microbial diversity in hyper-arid polar desert (vol 106, pg 19964, 2009). Proc Natl Acad Sci USA 107:1254

    CAS  Google Scholar 

  • Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig WG, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196

    Article  PubMed  CAS  Google Scholar 

  • Quade J, Rech JA, Betancourt JL, Latorre C, Quade B, Rylander KA, Fisher T (2008) Paleowetlands and regional climate change in the central Atacama Desert, northern Chile. Quat Res 69:343–360

    Article  Google Scholar 

  • Rech JA, Quade J, Hart WS (2003) Isotopic evidence for the source of Ca and S in soil gypsum, anhydrite and calcite in the Atacama Desert, Chile. Geochim Cosmochim Acta 67:575–586

    Article  CAS  Google Scholar 

  • Rech JA, Currie BS, Shullenberger ED, Dunagan SP, Jordan TE, Blanco N, Tomlinson AJ, Rowe HD, Houston J (2010) Evidence for the development of the Andean rain shadow from a Neogene isotopic record in the Atacama Desert, Chile. Earth Planet Sci Lett 292:371–382

    Article  CAS  Google Scholar 

  • Schimel J, Balser TC, Wallenstein M (2007) Microbial stress–response physiology and its implications for ecosystem function. Ecology 88:1386–1394

    Article  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  PubMed  CAS  Google Scholar 

  • Sorokin DY, Lysenko AM, Mityushina LL, Tourova TP, Jones BE, Rainey FA, Robertson LA, Kuenen GJ (2001) Thioalkalimicrobium aerophilum gen. nov., sp. nov. and Thioalkalimicrobium sibericum sp. nov., and Thioalkalivibrio versutus gen. nov., sp. nov., Thioalkalivibrio nitratis sp. nov. and Thioalkalivibrio denitrificans sp. nov., novel obligately alkaliphilic and obligately chemolithoautotrophic sulfur-oxidizing bacteria from soda lakes. Int J Syst Evol Microbiol 51:565–580

    PubMed  CAS  Google Scholar 

  • Sorokin DY, van Pelt S, Tourova TP, Evtushenko LI (2009) Nitriliruptor alkaliphilus gen.nov.,sp. nov., a deep-lineage haloalkaliphilic actinobacterium from soda lakes capable of growth on aliphatic nitriles, and proposal of Nitriliruptoraceae fam. nov. and Nitriliruptorales ord. nov. Int J Syst Evol Microbiol 59:248–253

  • Spieck E, Ehrich S, Aamand J, Bock E (1998) Isolation and immunocytochemical location of the nitrite-oxidizing system in Nitrospira moscoviensis. Arch Microbiol 169:225–230

    Article  PubMed  CAS  Google Scholar 

  • Sutcliffe IC (2010) A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol 18:464–470

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2006) PAUP* 4.0 phylogenetic analysis using parsimony, Macintosh Beta v.10. Sinauer Associates, Sunderland

    Google Scholar 

  • Thiel V, Tank M, Neulinger SC, Gehrmann L, Dorador C, Imhoff JF (2010) Unique communities of anoxygenic phototrophic bacteria in saline lakes of Salar de Atacama (Chile): evidence for a new phylogenetic lineage of phototrophic Gammaproteobacteria from pufLM gene analyses. FEMS Microbiol Ecol 74:510–522

    Article  PubMed  CAS  Google Scholar 

  • Tourova TP, Spiridonova EM, Berg IA, Slobodova NV, Boulygina ES, Sorokin DY (2007) Phylogeny and evolution of the family Ectothiorhodospiraceae based on comparison of 16S rRNA, cbbL and nifH gene sequences. Int J Syst Evol Microbiol 57:2387–2398

    Article  PubMed  CAS  Google Scholar 

  • Valenzuela-Encinas C, Neria-Gonzalez I, Alcantara-Hernandez RJ, Estrada-Alvarado I, de la Serna F, Dendooven L, Marsch R (2009) Changes in the bacterial populations of the highly alkaline saline soil of the former lake Texcoco (Mexico) following flooding. Extremophiles 13:609–621

    Article  PubMed  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  PubMed  CAS  Google Scholar 

  • Warren-Rhodes KA, Rhodes KL, Pointing SB, Ewing SA, Lacap DC, Gomez-Silva B, Amundson R, Friedmann EI, McKay CP (2006) Hypolithic cyanobacteria, dry limit of photosynthesis, and microbial ecology in the hyperarid Atacama Desert. Microbiol Ecol 52:389–398

    Article  Google Scholar 

  • Weber CF, King GM (2010) Distribution and diversity of carbon monoxide-oxidizing bacteria and bulk bacterial communities across a succession gradient on a Hawaiian volcanic deposit. Environ Microbiol 12:1855–1867

    Article  PubMed  CAS  Google Scholar 

  • Wierzchos J, Ascaso C, McKay CP (2006) Endolithic cyanobacteria in halite rocks from the hyperarid core of the Atacama Desert. Astrobiology 6:415–422

    Article  PubMed  Google Scholar 

  • Wierzchos J, Camara B, De Los Rios A, Davila AF, Almazo IMS, Artieda O, Wierzchos K, Gomez-Silva B, Mckay C, Ascaso C (2011) Microbial colonization of Ca-sulfate crusts in the hyperarid core of the Atacama Desert: implications for the search for life on Mars. Geobiology 9:44–60

    Article  PubMed  CAS  Google Scholar 

  • Wu DY, Raymond J, Wu M, Chatterji S, Ren QH, Graham JE, Bryant DA, Robb F, Colman A, Tallon LJ, Badger JH, Madupu R, Ward NL, Eisen JA (2009) Complete genome sequence of the aerobic CO-oxidizing thermophile Thermomicrobium roseum. PLoS ONE 4:e4207

    Article  PubMed  Google Scholar 

  • Yamada T, Sekiguchi Y (2009) Cultivation of uncultured Chloroflexi subphyla: significance and ecophysiology of formerly uncultured Chloroflexi ‘Subphylum I’ with natural and biotechnological relevance. Microbes Environ 24:205–216

    Article  PubMed  Google Scholar 

  • Youssef N, Sheik CS, Krumholz LR, Najar FZ, Roe BA, Elshahed MS (2009) Comparison of species richness estimates obtained using nearly complete fragments and simulated pyrosequencing-generated fragments in 16S rRNA gene-based environmental surveys. Appl Environ Microbiol 75:5227–5236

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to express our appreciation to Audrey Copeland for her assistance with the organic carbon analysis, to Yeisoo Yu and Nick Sisneros of the Arizona Genomics Institute for their assistance with 454-pyrosequencing, and to Andrea Byrne and Juliana Gil-Loaiza for generating the site 2547 negative clone library. Funding for this work was supplied by the National Science Foundation Microbial Observatory Grant MCB0604300 and from the Exxon-Mobile COSA Project.

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Correspondence to Julia W. Neilson.

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Communicated by A. Oren.

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Neilson, J.W., Quade, J., Ortiz, M. et al. Life at the hyperarid margin: novel bacterial diversity in arid soils of the Atacama Desert, Chile. Extremophiles 16, 553–566 (2012). https://doi.org/10.1007/s00792-012-0454-z

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