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Microbial Ecology

, Volume 75, Issue 1, pp 193–203 | Cite as

Namib Desert Soil Microbial Community Diversity, Assembly, and Function Along a Natural Xeric Gradient

  • Vincent Scola
  • Jean-Baptiste Ramond
  • Aline Frossard
  • Olivier Zablocki
  • Evelien M. Adriaenssens
  • Riegardt M. Johnson
  • Mary Seely
  • Don A. Cowan
Soil Microbiology

Abstract

The hyperarid Namib desert is a coastal desert in southwestern Africa and one of the oldest and driest deserts on the planet. It is characterized by a west/east increasing precipitation gradient and by regular coastal fog events (extending up to 75 km inland) that can also provide soil moisture. In this study, we evaluated the role of this natural aridity and xeric gradient on edaphic microbial community structure and function in the Namib desert. A total of 80 individual soil samples were collected at 10-km intervals along a 190-km transect from the fog-dominated western coastal region to the eastern desert boundary. Seventeen physicochemical parameters were measured for each soil sample. Soil parameters reflected the three a priori defined climatic/xeric zones along the transect (“fog,” “low rain,” and “high rain”). Microbial community structures were characterized by terminal restriction fragment length polymorphism fingerprinting and shotgun metaviromics, and their functional capacities were determined by extracellular enzyme activity assays. Both microbial community structures and activities differed significantly between the three xeric zones. The deep sequencing of surface soil metavirome libraries also showed shifts in viral composition along the xeric transect. While bacterial community assembly was influenced by soil chemistry and stochasticity along the transect, variations in community “function” were apparently tuned by xeric stress.

Keywords

Aridity gradient Xeric stress Edaphic desert microbial communities Extracellular enzyme activities Dryland 

Notes

Acknowledgments

We thank the South African National Research Foundation (NRF; grant N00113-95565), the University of Pretoria and the Genomics Research Institute for the financial support. We also thank the staff of the Gobabeb Research and Training Centre (Namibia) for their support in the field; the Soil, Water and Plant Analysis Laboratory of the University of Pretoria for their help with the soil physicochemical analyses; and the Sequencing Facility of the University for the T-RFLP runs and the sequencing of the metaviromes.

Supplementary material

248_2017_1009_MOESM1_ESM.docx (100 kb)
Supplementary Figure 1 (DOCX 100 kb)
248_2017_1009_MOESM2_ESM.docx (32 kb)
Supplementary Table 1 (DOCX 31 kb)
248_2017_1009_MOESM3_ESM.docx (26 kb)
Supplementary Table 2 (DOCX 25 kb)
248_2017_1009_MOESM4_ESM.docx (20 kb)
Supplementary Table 3 (DOCX 19 kb)

References

  1. 1.
    Laity JJ (2009) Deserts and desert environments. John Wiley & Sons, UK, Google Scholar
  2. 2.
    Gilbert N (2011) Science enters desert debate: United Nations considers creating advisory panel on land degradation akin to IPCC Nature 477:262–263CrossRefPubMedGoogle Scholar
  3. 3.
    Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems Nat Rev Microbiol 10:551–562. doi: 10.1038/nrmicro2831 CrossRefPubMedGoogle Scholar
  4. 4.
    Makhalanyane TP, Valverde A, Gunnigle E, Frossard A, Ramond J-B, Cowan DA (2015) Microbial ecology of hot desert edaphic systems FEMS Microbiol. Rev. 39:203–221. doi: 10.1093/femsre/fuu011 CrossRefPubMedGoogle Scholar
  5. 5.
    Lynch RC, King AJ, Farías ME, Sowell P, Vitry C, Schmidt SK (2012) The potential for microbial life in the highest-elevation (>6000 m asl) mineral soils of the Atacama region J Geophys Res-Biogeo 117(G2). doi: 10.1029/2012JG001961
  6. 6.
    Neilson JW, Quade J, Ortiz M, Nelson WM, Legatzki A, Tian F, LaComb M, Betancourt JL, Wing RA, Soderlund CA, Maier RM (2012) Life at the hyperarid margin: novel bacterial diversity in arid soils of the Atacama desert, Chile Extremophiles 16:553–566. doi: 10.1007/s00792-012-0454-z CrossRefPubMedGoogle Scholar
  7. 7.
    Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Wall DH, Caporaso JG (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes P Nat Acad Sci USA 109:21390–21395. doi: 10.1073/pnas.1215210110 CrossRefGoogle Scholar
  8. 8.
    Van Horn DJ, Okie JG, Buelow HN, Gooseff MN, Barrett JE, Takacs-Vesbach CD (2014) Soil microbial responses to increased moisture and organic resources along a salinity gradient in a polar desert Appl Environ Microb 80:3034–3043. doi: 10.1128/AEM.03414-13 CrossRefGoogle Scholar
  9. 9.
    Seager R, Ting M, Held I, et al. (2007) Model projections of an imminent transition to a more arid climate in southwestern North America Science 316:1181–1184. doi: 10.1126/science.1139601 CrossRefPubMedGoogle Scholar
  10. 10.
    Tsonis AA, Elsner JB, Hunt AG, Jagger TH (2005) Unfolding the relation between global temperature and ENSO Geophys. Res. Lett. 32(9). doi: 10.1029/2005GL022875
  11. 11.
    Belnap J, Welter JR, Grimm NB, Barger N, Ludwig JA (2005) Linkages between microbial and hydrologic processes in arid and semiarid watersheds Ecology 86:298–307. doi: 10.1890/03-0567 CrossRefGoogle Scholar
  12. 12.
    Seely M, Pallett J (2008) Namib: secrets of a desert uncovered. Venture Publications, Windhoek, Google Scholar
  13. 13.
    Lancaster J, Lancaster N, Seely MK (1984) Climate of the central Namib desert Modoqua 14:5–61Google Scholar
  14. 14.
    Eckardt FD, Soderberg K, Coop LJ, Muller AA, Vickery KJ, Grandin RD, Jack C, Kapalanga TS, Henschel J (2013) The nature of moisture at Gobabeb, in the central Namib desert J. Arid Environ. 93:7–19. doi: 10.1016/j.jaridenv.2012.01.011 CrossRefGoogle Scholar
  15. 15.
    Hamilton WJ, Seely MK (1976) Fog basking by the Namib desert beetle, Onymacris unguicularis Nature 262:284–285. doi: 10.1038/262284a0 CrossRefGoogle Scholar
  16. 16.
    Nørgaard T, Dacke M (2010) Fog-basking behaviour and water collection efficiency in Namib desert darkling beetles Front. Zool. 7:23. doi: 10.1186/1742-9994-7-23 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Ebner M, Miranda T, Roth-Nebelsick A (2011) Efficient fog harvesting by Stipagrostis sabulicola (Namib dune bushman grass) J. Arid Environ. 75:524–531. doi: 10.1016/j.jaridenv.2011.01.004 CrossRefGoogle Scholar
  18. 18.
    Stomeo F, Valverde A, Pointing SB, McKay CP, Warren-Rhodes KA, Tuffin MI, Seely M, Cowan DA (2013) Hypolithic and soil microbial community assembly along an aridity gradient in the Namib desert Extremophiles 17:329–337. doi: 10.1007/s00792-013-0519-7 CrossRefPubMedGoogle Scholar
  19. 19.
    Warren-Rhodes KA, McKay CP, Boyle LN, et al. (2013) Physical ecology of hypolithic communities in the central Namib desert: the role of fog, rain, rock habitat, and light J Geophys Res-Biogeo 118:1451–1460. doi: 10.1002/jgrg.20117 CrossRefGoogle Scholar
  20. 20.
    Valverde A, Makhalanyane TP, Seely M, Cowan DA (2015) Cyanobacteria drive community composition and functionality in rock–soil interface communities Mol. Ecol. 24:812–821. doi: 10.1111/mec.13068 CrossRefPubMedGoogle Scholar
  21. 21.
    Frossard A, Ramond J-B, Seely M, Cowan DA (2015) Water regime history drives responses of soil Namib desert microbial communities to wetting events Sci Rep 5:12263. doi: 10.1038/srep12263 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Directorate of Environmental Affairs (2002) Digital atlas of Namibia. Ministry of Environment and Tourism. http://www.uni-koeln.de/sfb389/e/e1/download/atlas_namibia/index_e.htm. Accessed 14 Dec 2016
  23. 23.
    Henschel JR, Seely MK (2008) Ecophysiology of atmospheric moisture in the Namib desert Atmos. Res. 87:362–368. doi: 10.1016/j.atmosres.2007.11.015 CrossRefGoogle Scholar
  24. 24.
    Johnson RM, Ramond J-B, Gunnigle E, Seely M, Cowan DA (2017) Namib desert edaphic bacterial, fungal and archaeal communities assemble through deterministic processes but are influenced by different abiotic parameters. Extremophiles, 1–12. doi: 10.1007/s00792-016-0911-1
  25. 25.
    Zablocki O, Adriaenssens EM, Frossard A, Seely M, Ramond J-B, Cowan DA (2017) Metaviromes of extracellular soil viruses along a Namib desert aridity gradient Genome Announc 5:e01470–e01416. doi: 10.1128/genomeA.01470-16 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    ASTM D (2007) Standard test method for particle-size analysis of soils. Annual Book of ASTM StandardsGoogle Scholar
  27. 27.
    Bouyoucos GJ (1962) Hydrometer method improved for making particle size analyses of soils Agron. J. 54:464–465. doi: 10.2134/agronj1962.00021962005400050028x CrossRefGoogle Scholar
  28. 28.
    Walkley A (1947) A critical examination of a rapid method for determining organic carbon in soils—effect of variations in digestion conditions and of inorganic soil constituents Soil Sci. 63:251–264CrossRefGoogle Scholar
  29. 29.
    Schulte EE, Hopkins BG (1996) Estimation of soil organic matter by weight loss-on-ignition. In: Soil organic matter: analysis and interpretation. Soil Science Society of America Special Publication n° 46, Madison, USA, pp 21–31Google Scholar
  30. 30.
    Keeney DR, Nelson DW (1982) Nitrogen—inorganic forms. In: Methods of Soil Analysis, 2nd ed. Agron Soc Amer, Madison, USA, pp 643–693Google Scholar
  31. 31.
    Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils Soil Sci. 59:39–46CrossRefGoogle Scholar
  32. 32.
    Rhoades JD (1982) Soluble salts. In: Methods of soil analysis, Part 2. Chemical and Microbiological Properties – Agronomy Monograph n°9, 2nd ed. ASA-SSSA, Madison, USA, pp167–178Google Scholar
  33. 33.
    Frossard A, Gerull L, Mutz M, Gessner MO (2012) Disconnet of microbial tructure and function: enzyme activities and bacterial communities in nascent stream corridor ISME J 6:680–691CrossRefPubMedGoogle Scholar
  34. 34.
    Ronca S, Ramond J-B, Jones BE, Seely M, Cowan DA (2014) Namib desert dune/interdune transects exhibit habitat-specific edaphic bacterial communities Front. Microbiol. 6:845–845Google Scholar
  35. 35.
    Green VS, Stott DE, Diack M (2006) Assay for fluorescein diacetate hydrolytic activity: optimization for soil samples Soil Biol. Biochem. 38:693–701. doi: 10.1016/j.soilbio.2005.06.020 CrossRefGoogle Scholar
  36. 36.
    Bickley J, Short JK, McDowell DG, Parkes HC (1996) Polymerase chain reaction (PCR) detection of Listeria monocytogenes in diluted milk and reversal of PCR inhibition caused by calcium ions Lett. Appl. Microbiol. 22:153–158. doi: 10.1111/j.1472-765X.1996.tb01131.x CrossRefPubMedGoogle Scholar
  37. 37.
    Emmerich M, Bhansali A, Lösekann-Behrens T, Schröder C, Kappler A, Behrens S (2012) Abundance, distribution, and activity of Fe (II)-oxidizing and Fe (III)-reducing microorganisms in hypersaline sediments of Lake Kasin, southern Russia Appl. Environ. Microbiol. 78:4386–4399. doi: 10.1128/AEM.07637-11 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Ishii K, Fukui M (2001) Optimization of annealing temperature to reduce bias caused by a primer mismatch in multitemplate PCR Appl. Environ. Microbiol. 67:3753–3755. doi: 10.1128/AEM.67.8.3753-3755.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses P Nat Acad Sci USA 82:6955–6959CrossRefGoogle Scholar
  40. 40.
    Williamson KE, Radosevich M, Wommack KE (2005) Abundance and diversity of viruses in six Delaware soils Appl. Environ. Microbiol. 71:3119–3125. doi: 10.1128/AEM.71.6.3119-3125.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical and interpretation, 2nd edn. PRIMER-E, Plymouth, Google Scholar
  42. 42.
    Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data Oecologia 129:271–280. doi: 10.1007/s004420100716 CrossRefPubMedGoogle Scholar
  43. 43.
    Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin Ecol. Monogr. 27:325–349. doi: 10.2307/1942268 CrossRefGoogle Scholar
  44. 44.
    Abdo Z, Schüette UM, Bent SJ, Williams CJ, Forney LJ, Joyce P (2006) Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes Environl Microbiol 8:929–938. doi: 10.1111/j.1462-2920.2005.00959.x CrossRefGoogle Scholar
  45. 45.
    Team RC (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2013Google Scholar
  46. 46.
    Roux S, Tournayre J, Mahul A, Debroas D, Enault F (2014) Metavir 2: new tools for viral metagenome comparison and assembled virome analysis BMC Bioinformatics 15:76. doi: 10.1186/1471-2105-15-76 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Maestre FT, Delgado-Baquerizo M, Jeffries TC, et al. (2015) Increasing aridity reduces soil microbial diversity and abundance in global drylands P Nat Acad Sci USA 112:15684–15689. doi: 10.1073/pnas.1516684112 CrossRefGoogle Scholar
  48. 48.
    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. doi: 10.1007/s00248-010-9727-1 CrossRefPubMedGoogle Scholar
  49. 49.
    Collins SL, Sinsabaugh RL, Crenshaw C, Green L, Porras-Alfaro A, Stursova M, Zeglin LH (2008) Pulse dynamics and microbial processes in aridland ecosystems J. Ecol. 96:413–420. doi: 10.1111/j.1365-2745.2008.01362.x CrossRefGoogle Scholar
  50. 50.
    Sinsabaugh RL, Lauber CL, Weintraub MN, et al. (2008) Stoichiometry of soil enzyme activity at global scale Ecol. Lett. 11:1252–1264. doi: 10.1111/j.1461-0248.2008.01245.x CrossRefPubMedGoogle Scholar
  51. 51.
    Huang J, Yu H, Guan X, Wang G, Guo R (2016) Accelerated dryland expansion under climate change Nat. Clim. Chang. 6:166–171. doi: 10.1038/nclimate2837 CrossRefGoogle Scholar
  52. 52.
    Gombeer S, Ramond J-B, Eckardt FD, Seely M, Cowan DA (2015) The influence of surface soil physicochemistry on the edaphic bacterial communities in contrasting terrain types of the central Namib desert Geobiology 13:494–505. doi: 10.1111/gbi.12144 CrossRefPubMedGoogle Scholar
  53. 53.
    Gustafsson ME, Franzén LG (1996) Dry deposition and concentration of marine aerosols in a coastal area, SW Sweden Atmos. Environ. 30:977–989CrossRefGoogle Scholar
  54. 54.
    Liang T, Chamecki M, Yu X (2016) Sea salt aerosol deposition in the coastal zone: a large eddy simulation study Atmos. Res. 180:119–127. doi: 10.1016/j.atmosres.2016.05.019 CrossRefGoogle Scholar
  55. 55.
    Eckardt FD, Schemenauer RS (1998) Fog water chemistry in the Namib desert, Namibia Atmos. Environ. 32:2595–2599. doi: 10.1016/S1352-2310(97)00498-6 CrossRefGoogle Scholar
  56. 56.
    Eckardt FD, Drake N, Goudie AS, White K, Viles H (2001) The role of playas in pedogenic gypsum crust formation in the central Namib desert: a theoretical model Earth Surf Proc Land 26:1177–1193. doi: 10.1002/esp.264 CrossRefGoogle Scholar
  57. 57.
    Mendelsohn J (2002) Atlas of Namibia: a portrait of the land and its people. New Africa Books (Pty) Ltd.Google Scholar
  58. 58.
    Lozupone CA, Knight R (2007) Global patterns in bacterial diversity P Nat Acad Sci USA 104:11436–11440. doi: 10.1073/pnas.0611525104 CrossRefGoogle Scholar
  59. 59.
    Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. The University of Chicago Press Princeton, New Jersey, Google Scholar
  60. 60.
    Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community ISME J 4:337–345. doi: 10.1038/ismej.2009.122 CrossRefPubMedGoogle Scholar
  61. 61.
    Vellend M (2010) Conceptual synthesis in community ecology Q. Rev. Biol. 85:183–206. doi: 10.1086/652373 CrossRefPubMedGoogle Scholar
  62. 62.
    Nemergut DR, Schmidt SK, Fukami T, et al. (2013) Patterns and processes of microbial community assembly Microbiol Mol Biol R 77:342–356. doi: 10.1128/MMBR.00051-12 CrossRefGoogle Scholar
  63. 63.
    Leibold MA, Holyoak M, Mouquet N, et al. (2004) The metacommunity concept: a framework for multi-scale community ecology Ecol. Lett. 7:601–613. doi: 10.1111/j.1461-0248.2004.00608.x CrossRefGoogle Scholar
  64. 64.
    Boerner REJ, Brinkman JA, Smith A (2005) Seasonal variations in enzyme activity and organic carbon in soil of a burned and unburned hardwood forest Soil Biol. Biochem. 37:1419–1426. doi: 10.1016/j.soilbio.2004.12.012 CrossRefGoogle Scholar
  65. 65.
    Cunha A, Almeida A, Coelho FJRC, Gomes NCM, Oliveira V, Santos AL (2010) Bacterial extracellular enzymatic activity in globally changing aquatic ecosystems Current research, technology and education topics in applied microbiology and microbial biotechnology 1:124–135Google Scholar
  66. 66.
    Henry HAL (2012) Soil extracellular enzyme dynamics in a changing climate Soi Biol Biochem 47:53–59. doi: 10.1016/j.soilbio.2011.12.026 CrossRefGoogle Scholar
  67. 67.
    Ladwig LM, Sinsabaugh RL, Collins SL, Thomey ML (2015) Soil enzyme responses to varying rainfall regimes in Chihuahuan desert soils Ecosphere 6:1–10. doi: 10.1890/ES14-00258.1 CrossRefGoogle Scholar
  68. 68.
    Bruder K, Malki K, Cooper A, Sible E, Shapiro JW, Watkins SC, Putonti C (2016) Freshwater metaviromics and bacteriophages: a current assessment of the state of the art in relation to bioinformatic challenges Evol. Bioinformatics Online 12:25Google Scholar
  69. 69.
    Zablocki O, Adriaenssens EM, Cowan D (2016) Diversity and ecology of viruses in hyperarid desert soils Appl. Environ. Microbiol. 82:770–777. doi: 10.1128/AEM.02651-15 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Adriaenssens EM, van Zyl LJ, Cowan DA, Trindade MI (2016) Metaviromics of Namib desert salt pans: a novel lineage of haloarchaeal salterproviruses and a rich source of ssDNA viruses Viruses 8:14. doi: 10.3390/v8010014 CrossRefPubMedCentralGoogle Scholar
  71. 71.
    Prestel E, Regeard C, Salamitou S, Neveu J, DuBow MS (2013) The bacteria and bacteriophages from a mesquite flats site of the Death Valley desert Anton van Leeuw 103:1329–1341. doi: 10.1007/s10482-013-9914-4 CrossRefGoogle Scholar
  72. 72.
    Sepulveda BP, Redgwell T, Rihtman B, Pitt F, Scanlan DJ, Millard A (2016) Marine phage genomics: the tip of the iceberg FEMS Microbiol. Lett. 363:fnw158. doi: 10.1093/femsle/fnw158 CrossRefGoogle Scholar
  73. 73.
    Hesse U, van Heusden P, Kirby BM, Olonade I, van Zyl LJ, Trindade M (2017) Virome assembly and annotation: a surprise in the Namib desert Front. Microbiol. 8:13. doi: 10.3389/fmicb.2017.00013 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Thurber RV (2009) Current insights into phage biodiversity and biogeography Curr Opin in Microbiol 12:582–587. doi: 10.1016/j.mib.2009.08.008 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Centre for Microbial Ecology and Genomics (CMEG), Department of MicrobiologyUniversity of PretoriaPretoriaSouth Africa
  2. 2.Centre for Microbial Ecology and Genomics (CMEG), Department of GeneticsUniversity of PretoriaPretoriaSouth Africa
  3. 3.Swiss Federal Institute for Forest, Snow and Landscape Research (WSL)BirmensdorfSwitzerland
  4. 4.Institute for Microbial Biotechnology and MetagenomicsUniversity of the Western CapeCape TownSouth Africa
  5. 5.Institute of Integrative BiologyUniversity of LiverpoolLiverpoolUK
  6. 6.Gobabeb Research and Training CentreWalvis BayNamibia
  7. 7.Desert Research Foundation of Namibia (DRFN)WindhoekNamibia

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