Advertisement

Biology and Fertility of Soils

, Volume 55, Issue 4, pp 393–403 | Cite as

Soil bacterial community associated with the dioecious Acanthosicyos horridus in the Namib Desert

  • Adrian Unc
  • Gillian Maggs-Kölling
  • Eugene Marais
  • Chen Sherman
  • Tirza Doniger
  • Yosef SteinbergerEmail author
Original Paper
  • 82 Downloads

Abstract

Plant clusters govern soil microbiology in desert systems. Female Acanthosicyos horridus plants in the Namib Desert are preferentially accessed by grazers, especially during fruit availability. We hypothesized that this differential grazing affects the taxonomic diversity of soil bacterial populations. Sampling was carried out at three locations on a northwest-to-southeast transect starting at the Kuiseb Delta, near the shores of the Atlantic in the western Namib Desert, and extending inland over a distance of 140 km. Analyses of the soil samples showed that proximity to the sea had a strong impact on soil salinity. Soil pH and organic matter content were generally not significantly correlated with the presence or absence of plants and varied little and non-uniformly along the transect. A. horridus presence led to distinct under-canopy bacterial-community diversity in contrast with the non-vegetated spaces between shrubs. However, plant gender has only a marginal, statistically insignificant impact on the bacterial-diversity properties, thus not supporting our hypothesis. Therefore, the taxonomic diversity of the bacterial community in Namib Desert soils vegetated with A. horridus is primarily governed by the presence or absence of plants and by proximity to the ocean.

Keywords

Soil microbial community Namib Desert Acanthosicyos horridus Plant gender 

Notes

Acknowledgments

Special thanks to Mrs. Sharon Victor for her useful comments and Ms. Tea Colin for her assistance in the laboratory work. We thank the members of the Soil Ecology Lab at Bar-Ilan University for valuable discussions and technical assistance.

Funding sources

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Our research did not involve human participants or animals. All authors agree to the submission of this manuscript.

Supplementary material

374_2019_1358_MOESM1_ESM.docx (6.6 mb)
ESM 1 (DOCX 6782 kb)

References

  1. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169Google Scholar
  2. Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutationl multivariate analysis of variance. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  3. Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268.  https://doi.org/10.1890/02-0274 CrossRefGoogle Scholar
  4. Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Meier-Kolthoff JP, Klenk HP, Clement C, Ouhdouch Y, van Wezel GP (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80:1–43.  https://doi.org/10.1128/MMBR.00019-15 CrossRefGoogle Scholar
  5. Battistuzzi FU, Hedges SB (2009) A major clade of prokaryotes with ancient adaptations to life on land. Mol Biol Evol 26:335–343.  https://doi.org/10.1093/molbev/msn247 CrossRefGoogle Scholar
  6. Battistuzzi FU, Feijao A, Hedges SB (2004) A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol Biol 4:44.  https://doi.org/10.1186/1471-2148-4-44 CrossRefGoogle Scholar
  7. Berry C (2003) Aspects of phenology and condition of inland and coastal !Nara plants in the Namib-Naukluft Park, Namibia. Dinteria 28:1–18Google Scholar
  8. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336.  https://doi.org/10.1038/nmeth.f.303 CrossRefGoogle Scholar
  9. Cloudsley-Thompson JL (1996) Biotic interaction in arid lands. Springer-Verlag, BerlinCrossRefGoogle Scholar
  10. Coleman DC (1994) The microbial loop concept as used in terrestrial soil ecology studies. Microb Ecol 28:245–250.  https://doi.org/10.1007/BF00166814 CrossRefGoogle Scholar
  11. Coleman D, Crossley D (2004) Fundamentals of soil ecology. Academic Press, New YorkGoogle Scholar
  12. Cowles HC (1899) The ecological relations of the vegetation on the sand dunes of Lake Michigan. Part I. Geographical relations of the dune floras. Bot Gaz 27:95–117CrossRefGoogle Scholar
  13. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072CrossRefGoogle Scholar
  14. Ding GC, Piceno YM, Heuer H, Weinert N, Dohrmann AB, Carrillo A, Andersen GL, Castellanos T, Tebbe CC, Smalla K (2013) Changes of soil bacterial diversity as a consequence of agricultural land use in a semi-arid ecosystem. PLoS One 8:e59497.  https://doi.org/10.1371/journal.pone.0059497 CrossRefGoogle Scholar
  15. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8:125.  https://doi.org/10.1186/1471-2180-8-125
  16. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461.  https://doi.org/10.1093/bioinformatics/btq461 CrossRefGoogle Scholar
  17. Eldridge DJ (2003) Biological soil crusts and water relations in Australian deserts. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, BerlinGoogle Scholar
  18. Eldridge DJ, Zaady E, Shachak M (2000) Infiltration through three contrasting biological soil crusts in patterned landscapes in the Negev, Israel. Catena 40:323–336.  https://doi.org/10.1016/S0341-8162(00)00082-5 CrossRefGoogle Scholar
  19. Evenari ME, Shanan L, Tadmor W (1982) The Negev: the challenge of a desert, 2nd edn. Harvard University Press, CambridgeCrossRefGoogle Scholar
  20. Fierer N, Breitbart M, Nulton J, Salamon P, Lozupone C, Jones R, Robeson M, Edwards RA, Felts B, Rayhawk S, Knight R, Rohwer F, Jackson RB (2007) Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Appl Environ Microbiol 73:7059–7066CrossRefGoogle Scholar
  21. Goodfellow M (2015) Actinomycetales. In: Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J, DeVos P, Hedlund B, Dedysh S (eds) Bergey’s manual of systematics of archaea and bacteria.  https://doi.org/10.1002/9781118960608.obm00005
  22. Gupta RS (2004) The phylogeny and signature sequences characteristics of Fibrobacteres, Chlorobi, and Bacteroidetes. Crit Rev Microbiol 30:123–143.  https://doi.org/10.1080/10408410490435133 CrossRefGoogle Scholar
  23. Hahnke RL, Meier-Kolthoff JP, Garcia-Lopez M, Mukherjee S, Huntemann M, Lvanova NN, Woyke T, Kyrpides NC, Klenk HP, Goker M (2016) Genome-based taxonomic classification of Bacteroidetes. Frontiers in Microbiology 7:article 2003.  https://doi.org/10.3389/fmicb.2016.02003 CrossRefGoogle Scholar
  24. Hammer Ø, Harper DAT, Ryan PD (2001) Past: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):4. http://palaeo-electronica.org/2001_1/past/issue1_01.htm
  25. Heulin T, Barakat M, Christen R, Lesourd M, Sutra L, De Luca G, Achouak W (2003) Ramlibacter tataouinensis gen. nov., sp nov., and Ramlibacter henchirensis sp nov., cyst-producing bacteria isolated from subdesert soil in Tunisia. Int J Syst Evol Microbiol 53:589–594.  https://doi.org/10.1099/ijs.0.02482-0 CrossRefGoogle Scholar
  26. Hulsen T, de Vlieg J, Alkema W (2008) BioVenn—a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9:488.  https://doi.org/10.1186/1471-2164-9-488 CrossRefGoogle Scholar
  27. Huson DH, Beier S, Flade I, Gorska A, El-Hadidi M, Mitra S, Ruscheweyh HJ, Tappu R (2016) MEGAN community edition—interactive exploration and analysis of large-scale microbiome sequencing data Plos Comput Biol 12. doi:  https://doi.org/10.1371/journal.pcbi.1004957,
  28. Jacobson K, van Diepeningen A, Evans S, Fritts R, Gemmel P, Marsho C, Seely M, Wenndt A, Yang XX, Jacobson P (2015) Non-rainfall moisture activates fungal decomposition of surface litter in the Namib Sand Sea. PLOS One 10:e0126977.  https://doi.org/10.1371/journal.pone.0126977 CrossRefGoogle Scholar
  29. Jones SE, Lennon JT (2010) Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci U S A 107:5881–5886.  https://doi.org/10.1073/pnas.0912765107 CrossRefGoogle Scholar
  30. Kawasaki A, Donn S, Ryan PR, Mathesius U, Devilla R, Jones A, Watt M (2016) Microbiome and exudates of the root and rhizosphere of Brachypodium distachyon, a model for wheat. PLoS One 11:e0164533.  https://doi.org/10.1371/journal.pone.0164533 CrossRefGoogle Scholar
  31. Kuske CR, Ticknor LO, Miller ME, Dunbar JM, Davis JA, Barns SM, Belnap J (2002) Comparison of soil bacterial communities in rhizospheres of three plant species and the interspaces in an arid grassland. Appl Environ Microbiol 68:1854–1863CrossRefGoogle Scholar
  32. Logan NA, Vos PD (2015) Bacillus. In: Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J, Vos PD, Hedlund B, Dedysh S (eds) Bergey’s manual of systematics of archaea and bacteria.  https://doi.org/10.1002/9781118960608.gbm00530
  33. Louw GN, Seely MK (1982) Ecology of desert organisms. Longman Group Ltd., LondonGoogle Scholar
  34. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235CrossRefGoogle Scholar
  35. Lynch MDJ, Neufeld JD (2015) Ecology and exploration of the rare biosphere. Nat Rev Microbiol 13:217–229.  https://doi.org/10.1038/nrmicro3400 CrossRefGoogle Scholar
  36. Lynch MDJ, Bartram AK, Neufeld JD (2012) Targeted recovery of novel phylogenetic diversity from next-generation sequence data. ISME J 6:2067–2077.  https://doi.org/10.1038/ismej/2012.50 CrossRefGoogle Scholar
  37. Maun MA (2004) Burial of plants as a selective force in sand dunes. In: Martinez ML, Psuty NP (eds) Coastal dunes ecology and conservation. Springer, BerlinGoogle Scholar
  38. Maun MA (2009) The biology of coastal sand dunes. Oxford University Press, OxfordGoogle Scholar
  39. McBride MJ, Liu W, Lu X, Zhu Y, Zhang W (2014) The family Cytophagaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: other major lineages of Bacteria and the Archaea. Springer, BerlinGoogle Scholar
  40. 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.  https://doi.org/10.1007/s00792-012-0454-z CrossRefGoogle Scholar
  41. Norris PR (2015) Acidimicrobiales. In: Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J, Vos PD, Hedlund B, Dedysh S (eds) Bergey’s manual of systematics of archaea and bacteria.  https://doi.org/10.1002/9781118960608.obm00004
  42. Noy-Meir I (1973) Desert ecosystems: environment and producers. Ann Rev Ecol Syst 4:25–51.  https://doi.org/10.1146/annurev.es.04.110173.000325 CrossRefGoogle Scholar
  43. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara B, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2.4-5. https://CRAN.R-project.org/package=vegan
  44. Olsson PA, Jakobsen I, Wallander H (2003) Foraging and resource allocation strategies of mycorrhizal fungi in a patchy environment. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Springer, BerlinGoogle Scholar
  45. Osman GJ, Zhang T, Lou K, Gao Y, Chang W, Lin O, Yang HM, Huo XD, Wang N (2016) Pontibacter aydingkolensis sp nov., isolated from soil of a salt lake. Int J Syst Evol Microbiol 66:5523–5528.  https://doi.org/10.1099/ijsem.0.001551 CrossRefGoogle Scholar
  46. Prestel E, Salamitou S, Dubow MS (2008) An examination of the bacteriophages and bacteria of the Namib Desert. J Microbiol 46:364–372.  https://doi.org/10.1007/s12275-008-0007-4 CrossRefGoogle Scholar
  47. 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. Antonie Van Leeuwenhoek 103:1329–1341.  https://doi.org/10.1007/s10482-013-9914-4 CrossRefGoogle Scholar
  48. Prigent M, Leroy M, Confalonieri F, Dutertre M, DuBow MS (2005) A diversity of bacteriophage forms and genomes can be isolated from the surface sands of the Sahara Desert. Extremophiles 9:289–296.  https://doi.org/10.1007/s00792-005-0444-5 CrossRefGoogle Scholar
  49. Rajaniemi TK, Allison VJ (2009) Abiotic conditions and plant cover differentially affect microbial biomass and community composition on dune gradients. Soil Biol Biochem 41:102–109.  https://doi.org/10.1016/j.soilbio.2008.10.001 CrossRefGoogle Scholar
  50. Reynolds JF, Kemp PR, Ogle K, Fernandez RJ (2004) Modifying the ‘pulse-reserve’ paradigm for deserts of North America: precipitation pulses, soil water, and plant responses. Oecologia 141:194–210.  https://doi.org/10.1007/s00442-004-1524-4 CrossRefGoogle Scholar
  51. Rosenberg E (2014) The family Chitinophagaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: other major lineages of Bacteria and the Archaea. Springer, BerlinGoogle Scholar
  52. Sarig S, Steinberger Y (1993) Immediate effect of wetting event on microbial biomass and carbohydrate production mediated aggregation in desert soil. Geoderma 56:599–607.  https://doi.org/10.1016/0016-7061(93)90138-B CrossRefGoogle Scholar
  53. Schlesinger WH, Pilmanis AM (1998) Plant-soil interactions in deserts. Biogeochemistry 42:169–187.  https://doi.org/10.1023/A:1005939924434 CrossRefGoogle Scholar
  54. Setia R, Gottschalk P, Smith P, Marschner P, Baldock J, Setia D, Smith J (2013) Soil salinity decreases global soil organic carbon stocks. Sci Total Environ 465:267–272.  https://doi.org/10.1016/j.scitotenv.2012.08.028 CrossRefGoogle Scholar
  55. Soil and Plant Analysis Council Inc. (1999) Soil analysis handbook of reference methods. CRC Press, Boca RatonGoogle Scholar
  56. St'ovicek A, Azatyan A, Soares MIM, Gillor O (2017) The impact of hydration and temperature on bacterial diversity in arid soil mesocosms. Front Microbiol 8. doi:  https://doi.org/10.3389/fmicb.2017.01078
  57. Tilman GD (1984) Plant dominance along an experimental nutrient gradient. Ecology 65:1445–1453.  https://doi.org/10.2307/1939125 CrossRefGoogle Scholar
  58. Tilman D, Reich PB, Knops JMH (2006) Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441:629–632.  https://doi.org/10.1038/nature04742 CrossRefGoogle Scholar
  59. Turner S, Pryer KM, Miao VPW, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small submit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338.  https://doi.org/10.1111/j.1550-7408.1999.tb04612.x CrossRefGoogle Scholar
  60. 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.  https://doi.org/10.1111/mec.13068 CrossRefGoogle Scholar
  61. van der Waal C, Kool A, Meijer SS, Kohi E, Heitkonig IMA, de Boer WF, van Langevelde F, Grant RC, Peel MJS, Slotow R, de Knegt HJ, Prins HHT, de Kroon H (2011) Large herbivores may alter vegetation structure of semi-arid savannas through soil nutrient mediation. Oecologia 165:1095–1107.  https://doi.org/10.1007/s00442-010-1899-3 CrossRefGoogle Scholar
  62. 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 Microbiol 80:3034–3043CrossRefGoogle Scholar
  63. Vestergaard G, Schulz S, Scholer A, Schloter M (2017) Making big data smart-how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484.  https://doi.org/10.1007/s00374-017-1191-3 CrossRefGoogle Scholar
  64. Vik U, Logares R, Blaalid R, Halvorsen R, Carlsen T, Bakke I, Kolsto AB, Okstad OA, Kauserud H (2013) Different bacterial communities in ectomycorrhizae and surrounding soil. Sci Rep 3:3471.  https://doi.org/10.1038/srep03471 CrossRefGoogle Scholar
  65. Whitford WG (2002) Ecology of desert systems. Academic Press, New YorkGoogle Scholar
  66. Willis AJ (1989) Coastal sand dunes as biological systems. Proc R Soc Edinb B Biol 96B:17–36.  https://doi.org/10.1017/S0269727000010836 Google Scholar
  67. Willis A, Harris PJC, Rodrigues BF, Sparks TH (2016) Primary sand-dune plant community and soil properties during the west-coast India monsoon. Eur J Ecol 2:60–71.  https://doi.org/10.1515/eje-2016-0007 CrossRefGoogle Scholar
  68. Yu J, Glazer N, Steinberger Y (2014) Carbon utilization, microbial biomass, and respiration in biological soil crusts in the Negev Desert. Biol Fertil Soils 50:285–293.  https://doi.org/10.1007/s00374-013-0856-9 CrossRefGoogle Scholar
  69. Zavaleta ES, Kettley LS (2006) Ecosystem change along a woody invasion chronosequence in a California grassland. J Arid Environ 66:290–306.  https://doi.org/10.1016/j.jaridenv.2005.11.008 CrossRefGoogle Scholar
  70. Zhou X, Fornara D, Ikenaga M, Akagi I, Zhang RF, Jia ZJ (2016) The resilience of microbial community under drying and rewetting cycles of three forest soils. Front Microbiol 7:1101.  https://doi.org/10.3389/fmicb.2016.01101 Google Scholar
  71. Zvyagintsev DG, Zenova GM, Oborotov GV (2009) Moderately haloalkaliphilic actinomycetes in salt-affected soils. Eurasian Soil Sci 42:1515–1520CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Science and the EnvironmentMemorial University of NewfoundlandCorner BrookCanada
  2. 2.Gobabeb Research and Training CentreNamib-Naukluft ParkNamibia
  3. 3.The Mina and Everard Goodman Faculty of Life SciencesBar-Ilan UniversityRamat-GanIsrael

Personalised recommendations