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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
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
Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutationl multivariate analysis of variance. Department of Statistics, University of Auckland, New Zealand
Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268. https://doi.org/10.1890/02-0274
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
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
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
Berry C (2003) Aspects of phenology and condition of inland and coastal !Nara plants in the Namib-Naukluft Park, Namibia. Dinteria 28:1–18
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
Cloudsley-Thompson JL (1996) Biotic interaction in arid lands. Springer-Verlag, Berlin
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
Coleman D, Crossley D (2004) Fundamentals of soil ecology. Academic Press, New York
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 27:95–117
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 72:5069–5072
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
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
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
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, Berlin
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
Evenari ME, Shanan L, Tadmor W (1982) The Negev: the challenge of a desert, 2nd edn. Harvard University Press, Cambridge
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 73:7059–7066
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
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
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
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
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
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
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,
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
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
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
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 68:1854–1863
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
Louw GN, Seely MK (1982) Ecology of desert organisms. Longman Group Ltd., London
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235
Lynch MDJ, Neufeld JD (2015) Ecology and exploration of the rare biosphere. Nat Rev Microbiol 13:217–229. https://doi.org/10.1038/nrmicro3400
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
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, Berlin
Maun MA (2009) The biology of coastal sand dunes. Oxford University Press, Oxford
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, Berlin
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
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
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
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
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, Berlin
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
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
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
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
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
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
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, Berlin
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
Schlesinger WH, Pilmanis AM (1998) Plant-soil interactions in deserts. Biogeochemistry 42:169–187. https://doi.org/10.1023/A:1005939924434
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
Soil and Plant Analysis Council Inc. (1999) Soil analysis handbook of reference methods. CRC Press, Boca Raton
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
Tilman GD (1984) Plant dominance along an experimental nutrient gradient. Ecology 65:1445–1453. https://doi.org/10.2307/1939125
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
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
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
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
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 80:3034–3043
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
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
Whitford WG (2002) Ecology of desert systems. Academic Press, New York
Willis AJ (1989) Coastal sand dunes as biological systems. Proc R Soc Edinb B Biol 96B:17–36. https://doi.org/10.1017/S0269727000010836
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
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
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
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
Zvyagintsev DG, Zenova GM, Oborotov GV (2009) Moderately haloalkaliphilic actinomycetes in salt-affected soils. Eurasian Soil Sci 42:1515–1520
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 6782 kb)
Rights and permissions
About this article
Cite this article
Unc, A., Maggs-Kölling, G., Marais, E. et al. Soil bacterial community associated with the dioecious Acanthosicyos horridus in the Namib Desert. Biol Fertil Soils 55, 393–403 (2019). https://doi.org/10.1007/s00374-019-01358-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-019-01358-7