Biodiversity and Conservation

, Volume 23, Issue 7, pp 1709–1733 | Cite as

Niche partitioning of bacterial communities in biological crusts and soils under grasses, shrubs and trees in the Kalahari

  • David R. Elliott
  • Andrew D. Thomas
  • Stephen R. Hoon
  • Robin Sen
Original Paper

Abstract

The Kalahari of southern Africa is characterised by sparse vegetation interspersed with microbe-dominated biological soil crusts (BSC) which deliver a range of ecosystem services including soil stabilisation and carbon fixation. We characterised the bacterial communities of BSCs (0–1 cm depth) and the subsurface soil (1–2 cm depth) in an area typical of lightly grazed Kalahari rangelands, composed of grasses, shrubs, and trees. Our data add substantially to the limited amount of existing knowledge concerning BSC microbial community structure, by providing the first bacterial community analyses of both BSCs and subsurface soils of the Kalahari region based on a high throughput 16S ribosomal RNA gene sequencing approach. BSC bacterial communities were distinct with respect to vegetation type and soil depth, and varied in relation to soil carbon, nitrogen, and surface temperature. Cyanobacteria were predominant in the grass interspaces at the soil surface (0–1 cm) but rare in subsurface soils (1–2 cm depth) and under the shrubs and trees. Bacteroidetes were significantly more abundant in surface soils of all areas even in the absence of a consolidated crust, whilst subsurface soils yielded more sequences affiliated to Acidobacteria, Actinobacteria, Chloroflexi, and Firmicutes. The common detection of vertical stratification, even in disturbed sites, suggests a strong potential for BSC recovery after physical disruption, however severe depletion of Cyanobacteria near trees and shrubs may limit the potential for natural BSC regeneration in heavily shrub-encroached areas.

Keywords

Biological soil crust 454 Pyrosequencing Bacterial community Kalahari Sand Carbon Vegetation 

Supplementary material

10531_2014_684_MOESM1_ESM.txt (11 kb)
OR1. Sample metadata and summary statistics, including pyrosequencing barcodes, number of sequences obtained, richness estimates, and diversity measures. This is a tab separated text file based on the sample map used in the QIIME pipeline and other downstream analyses. (TXT 11 kb)
10531_2014_684_MOESM2_ESM.png (429 kb)
OR2: Constrained and unconstrained correspondence analyses of the microbial community including scree plots. (PNG 429 kb)
10531_2014_684_MOESM3_ESM.txt (7 kb)
OR3. Text file containing results from the ADONIS test comparing community structure with respect to vegetation, depth, and month. The test was performed at all taxonomic ranks from phylum to species. (TXT 8 kb)
10531_2014_684_MOESM4_ESM.zip (500 kb)
OR4. Zip file containing plots, statistical tests, and result tables of OTU abundances for the top 9 OTUs in each phylum, and the proteobacterial classes. Files are descriptively named and include for each group of OTUs a zone plot and a carbon plot similar to those shown in Figure 4a and 4b respectively. Boxes represent the interquartile range (IQR), and error bars extend to the most extreme values within 1.5 * IQR of the box (n=6). Median values are shown as a line within the box and outliers are shown as black spots. Sample coding: AG=annual grass, PG=perennial grass, S=shrub, T=tree. Significance and direction of correlation between OTU abundance and soil carbon is indicated by + or – (determined by Spearman test). Significance codes for positive correlation: +++ < 0.001; ++ < 0.01; + <0.05. (ZIP 500 kb)

References

  1. Aranibar JN, Anderson IC, Ringrose S, Macko SA (2003) Importance of nitrogen fixation in soil crusts of southern African arid ecosystems: acetylene reduction and stable isotope studies. J Arid Environ 54:345–358CrossRefGoogle Scholar
  2. Bailey VL, Fansler SJ, Stegen JC, McCue LA (2013) Linking microbial community structure to ß-glucosidic function in soil aggregates. ISME J 7(10):2044–2053. doi:10.1038/ismej.2013.87 PubMedCrossRefGoogle Scholar
  3. Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Process 20(15):3159–3178CrossRefGoogle Scholar
  4. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300Google Scholar
  5. Beyschlag W, Wittland M, Jentsch A, Steinlein T (2008) Soil crusts and disturbance benefit plant germination, establishment and growth on nutrient deficient sand. Basic Appl Ecol 9(3):243–252CrossRefGoogle Scholar
  6. Boopathi T, Balamurugan V, Gopinath S, Sundararaman M (2013) Characterization of IAA production by the mangrove cyanobacterium phormidium sp. MI405019 and its influence on tobacco seed germination and organogenesis. J Plant Growth Regul 32(4):758–766CrossRefGoogle Scholar
  7. Bowker MA (2007) Biological soil crust rehabilitation in theory and practice: an underexploited opportunity. Restor Ecol 15(1):13–23CrossRefGoogle Scholar
  8. Bowker MA, Maestre FT, Escolar C (2010) Biological crusts as a model system for examining the biodiversity–ecosystem function relationship in soils. Soil Biol Biochem 42(3):405–417CrossRefGoogle Scholar
  9. Brussard L (2012) Ecosystem services provided by soil biota. In: Diana H Wall (ed) Soil ecology and ecosystem services. Oxford University Press, Oxford, pp 45–58Google Scholar
  10. Büdel B, Darienko T, Deutschewitz K, Dojani S, Friedl T, Mohr KI, Salisch M, Reisser W, Weber B (2009) Southern African biological soil crusts are ubiquitous and highly diverse in drylands, being restricted by rainfall frequency. Microb Ecol 57(2):229–247. doi:10.1007/s00248-008-9449-9 PubMedCrossRefGoogle Scholar
  11. 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, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336PubMedCentralPubMedCrossRefGoogle Scholar
  12. Caruso T, Chan Y, Lacap DC, Lau MCY, McKay CP, Pointing SB (2011) Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J 5:1406–1413PubMedCentralPubMedCrossRefGoogle Scholar
  13. Castillo-Monroy AP, Bowker MA, Maestre FT, Rodríguez-Echeverría S, Martínez I, Barraza-Zepeda CE, Escolar C (2011) Relationships between biological soil crusts, bacterial diversity and abundance, and ecosystem functioning: insights from a semi-arid Mediterranean environment. J Veg Sci 22:165–174CrossRefGoogle Scholar
  14. Chen L, Yang Y, Deng S, Xu Y, Wang G, Liu Y (2012) The response of carbohydrate metabolism to the fluctuation of relative humidity (RH) in the desert soil cyanobacterium Phormidium tenue. Euro J Soil Biol 48:11–16CrossRefGoogle Scholar
  15. Csotonyi JT, Swiderski J, Stackebrandt E, Yurkov V (2010) A new environment for aerobic anoxygenic phototrophic bacteria: biological soil crusts. Environ Microbiol Rep 2(5):651–656PubMedCrossRefGoogle Scholar
  16. 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 72:5069–5072PubMedCentralPubMedCrossRefGoogle Scholar
  17. Dojani S, Kauff F, Weber B, Büdel B (2013) Genotypic and phenotypic diversity of cyanobacteria in biological soil crusts of the succulent karoo and nama karoo of southern Africa. Microb Ecol. doi:10.1007/s00248-013-0301-5 PubMedGoogle Scholar
  18. Dowd S, Callaway T, Wolcott R, Sun Y, McKeehan T, Hagevoort R, Edrington T (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8(1):125PubMedCentralPubMedCrossRefGoogle Scholar
  19. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. doi:10.1093/bioinformatics/btq461 PubMedCrossRefGoogle Scholar
  20. Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5(7):459–462CrossRefGoogle Scholar
  21. Eldridge DJ, Greene RSB (1994) Microbiotic soil crusts: a review of their roles in soil and ecological processes in the rangelands of Australia. Aust J Soil Res 32:389–415CrossRefGoogle Scholar
  22. FAO (1990) Guidelines for soil description. 3rd edn. (revised). Soil resources, management and conservation service, land and water development division, FAO, RomeGoogle Scholar
  23. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88(6):1354–1364PubMedCrossRefGoogle Scholar
  24. Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012a) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017PubMedCentralPubMedCrossRefGoogle Scholar
  25. Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Wall DA, Caporaso JG (2012b) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci USA 109:21390–21395PubMedCentralPubMedCrossRefGoogle Scholar
  26. Garcia-Pichel F, Johnson SL, Youngkin D, Belnap J (2003) Small-scale vertical distribution of bacterial biomass and diversity in biological soil crusts from arid lands in the Colorado plateau. Microb Ecol 46(3):312–321PubMedCrossRefGoogle Scholar
  27. Gundlapally SR, Garcia-Pichel F (2006) The community and phylogenetic diversity of biological soil crusts in the Colorado plateau studied by molecular fingerprinting and intensive cultivation. Microb Ecol 52(2):345–357PubMedCrossRefGoogle Scholar
  28. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methé B, DeSantis TZ; Human Microbiome Consortium, Petrosino JF, Knight R, Birren BW (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21(3):494–504. doi:10.1101/gr.112730.110 CrossRefGoogle Scholar
  29. Keskitalo J, Leppäranta M, Arvola L (2013) First records of primary producers of epiglacial and supraglacial lakes in western dronning maud land, Antarctica. Polar Biol 36(10):1441–1450CrossRefGoogle Scholar
  30. Klappenbach JA, Dunbar JM, Schmidt TM (2000) rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol 66(4):1328–1333PubMedCentralPubMedCrossRefGoogle Scholar
  31. Lal R (2004) Carbon sequestration in dryland ecosystems. Environ Manage 33(4):528–544PubMedCrossRefGoogle Scholar
  32. Lan S, Zhang Q, Wu L, Liu Y, Zhang D, Hu C (2014) Artificially accelerating the reversal of desertification: cyanobacterial inoculation facilitates the succession of vegetation communities. Environ Sci Technol. doi:10.1021/es403785j PubMedGoogle Scholar
  33. Lidstrom ME, Chistoseerdova L (2002) Plants in the pink: cytokinin production by Methylobacterium. J Bacteriol 184:1818PubMedCentralPubMedCrossRefGoogle Scholar
  34. MacArthur RH, Wilson E (1967) The theory of island biogeography. Princeton University Press, Princeton Google Scholar
  35. Mager DM, Thomas AD (2011) Extracellular polysaccharides from cyanobacterial soil crusts: a review of their role in dryland soil processes. J Arid Environ 75(2):91–97CrossRefGoogle Scholar
  36. McMurdie PJ, Holmes S (2013) phyloseq: an r package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8(4):e61217PubMedCentralPubMedCrossRefGoogle Scholar
  37. Menon M, Yuan Q, Jia X, Dougill AJ, Hoon SR, Thomas AD, Williams RA (2011) Assessment of physical and hydrological properties of biological soil crusts using X-ray microtomography and modeling. J Hydrol 397(1):47–54CrossRefGoogle Scholar
  38. Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M et al (2008) The metagenomics RAST server–a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform 9(1):386CrossRefGoogle Scholar
  39. Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700PubMedCentralPubMedGoogle Scholar
  40. Muyzer G, Brinkhoff T, Nübel U, Santegoeds C, Schäfer H, Waver C. (1998). Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds). Molecular microbial ecology manual. Kluwer Academic Publishers, DordrechtGoogle Scholar
  41. Nagy ML, Pérez 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(2):233–245PubMedCrossRefGoogle Scholar
  42. Nazaries L, Murrell JC, Millard P, Baggs L, Singh BK (2013) Methane, microbes and models: fundamental understanding of the soil methane cycle for future predictions. Environ Microbiol 15(9):2395–2417. doi:10.1111/1462-2920.12149 PubMedCrossRefGoogle Scholar
  43. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens HMH, Wagner H (2013) Vegan: community ecology package. R package version 2.0–10. http://CRAN.R-project.org/package=vegan. Accessed 20 Mar 2014
  44. Patt TE, Cole GC, Hanson RS (1976) Methylobacterium, a new genus of facultatively Methylotrophic bacteria. Int J Syst Bacteriol 26:226–229CrossRefGoogle Scholar
  45. Pereira MC, Dias ACF, vanElsas JD, Salles JF (2012) Spatial and temporal variation of archaeal, bacterial and fungal communities in agricultural soils. PLoS ONE 7:e51554. doi:10.1371/journal.pone.0051554 CrossRefGoogle Scholar
  46. Phosri C, Polme S, Taylor AFS, Koljalg U, Suwannasai N, Tedersoo L (2012) Diversity and community composition of ectomycorrhizal fungi in a dry deciduous dipterocarp forest in Thailand. Biodivers Conserv 21:2287–2298CrossRefGoogle Scholar
  47. Prasse R, Bornkamm R (2000) Effect of microbiotic soil surface crusts on emergence of vascular plants. Plant Ecol 150(1–2):65–75CrossRefGoogle Scholar
  48. R Core Team (2013) R: a language and environment for statistical computing. In: R foundation for statistical computing, Vienna, ISBN 3-900051-07-0, URL http://www.R-project.org/. Accessed 20 Mar 2014
  49. Reynolds JF, Smith DMS, Lambin EF, Turner BL, Mortimore M, Batterbury SP et al (2007) Global desertification: building a science for dryland development. Science 316(5826):847–851PubMedCrossRefGoogle Scholar
  50. Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351PubMedCrossRefGoogle Scholar
  51. Saul-Tcherkas V, Steinberger Y (2011) Soil microbial diversity in the vicinity of a negev desert shrub–Reaumuria negevensis. Microb Ecol 61(1):64–81. doi:10.1007/s00248-010-9763-x PubMedCrossRefGoogle Scholar
  52. Schmidt MW, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DA, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature. doi:10.1038/nature10386 Google Scholar
  53. Skarpe C (1990) Structure of the woody vegetation in disturbed and undisturbed arid savanna Botswana. Vegetatio 87(1):11–18CrossRefGoogle Scholar
  54. Sloan WT, Lunn M, Woodcock S, Head IM, Nee S, Curtis TP (2006) Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ Microbiol 8(4):732–740PubMedCrossRefGoogle Scholar
  55. Smit E, Leeflang P, Gommans S, van den Broek J, van Mil S, Wernars K (2001) Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl Environ Microbiol 67(5):2284–2291PubMedCentralPubMedCrossRefGoogle Scholar
  56. Stackebrandt E, Goebel BM (1994) A place for DNA–DNA reassociation and 16S ribosomal-RNA sequence-analysis in the present species definition in bacteriology. Int J Syst Evol Microbiol 44:846–849Google Scholar
  57. Steven B, Gallegos-Graves LV, Belnap J, Kuske CR (2013) Dryland soil microbial communities display spatial biogeographic patterns associated with soil depth and soil parent material. FEMS Microbiol Ecol 86(1):101–113. doi:10.1111/1574-6941.12143 PubMedCrossRefGoogle Scholar
  58. Stringer L (2008) Can the UN Convention to combat desertification guide sustainable use of the world’s soils? Front Ecol Environ 6(3):138–144CrossRefGoogle Scholar
  59. Stringer LC, Dougill AJ, Thomas AD, Spracklen DV, Chesterman S, Speranza CI, Rueff H et al (2012) Challenges and opportunities in linking carbon sequestration, livelihoods and ecosystem service provision in drylands. Environ Sci Policy 19:121–135CrossRefGoogle Scholar
  60. Takeda M, Suzuki I, Koizumi JI (2004) Balneomonas flocculans gen. nov., sp. nov., a new cellulose-producing member of the α-2 subclass of Proteobacteria. Syst Appl Microbiol 27(2):139–145PubMedCrossRefGoogle Scholar
  61. Theisen AR, Murrell JC (2005) Facultative methanotrophs revisited. J Bacteriol 187(13):4303–4305PubMedCentralPubMedCrossRefGoogle Scholar
  62. Thomas AD (2012) Impact of grazing intensity on seasonal variations of soil organic carbon and soil CO2 efflux in two semi-arid grasslands in southern Botswana. Philos Trans Royal Soc B 367:3076–3086CrossRefGoogle Scholar
  63. Thomas AD, Dougill AJ (2006) Distribution and characteristics of cyanobacterial soil crusts in the Molopo Basin, South Africa. J Arid Environ 64:270–283CrossRefGoogle Scholar
  64. Thomas AD, Dougill AJ (2007) Spatial and temporal distribution of cyanobacterial soil crusts in the Kalahari: implications for soil surface properties. Geomorphology 85:17–29CrossRefGoogle Scholar
  65. Thomas AD, Hoon SR, Dougill AJ, Mairs H (2012) Soil organic carbon in deserts: examples from the Kalahari. In: Mol L, Sternberg T (eds) Changing deserts: Integrating environments, people and challenges. White Horse Press, CambridgeGoogle Scholar
  66. Thomas F, Hehemann J, Rebuffet E, Czjzek M, Michel G (2011) Environmental and gut Bacteroidetes: the food connection. Frontiers Microbiol 2. doi:10.3049/fmicb.2011.00093
  67. 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 73:5261–5267PubMedCentralPubMedCrossRefGoogle Scholar
  68. Ward D (2009) The Biology of deserts. Oxford University Press, OxfordGoogle Scholar
  69. Weon HY, Kwon SW, Son JA, Jo EH, Kim SJ, Kim YS, Kim BY, Ka JO (2010) Description of Microvirga aerophila sp. nov. and Microvirga aerilata sp. nov., isolated from air, reclassification of Balneimonas flocculans takeda,et al.2004 as Microvirga flocculans comb nov. and emended description of the genus Microvirga. Int J Syst Evol Microbiol 60(11):2596–2600PubMedCrossRefGoogle Scholar
  70. Wu N, Zhang YM, Pan HX, Zhang J (2010) The role of nonphotosynthetic microbes in the recovery of biological soil crusts in the gurbantunggut desert, northwestern China. Arid Land Res Manage 24(1):42–56CrossRefGoogle Scholar
  71. Xu Y, Rossi F, Colica G, Deng S, De Philippis R, Chen L (2013) Use of cyanobacterial polysaccharides to promote shrub performances in desert soils: a potential approach for the restoration of desertified areas. Biol Fertil Soils 49(2):143–152CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • David R. Elliott
    • 1
  • Andrew D. Thomas
    • 2
  • Stephen R. Hoon
    • 1
  • Robin Sen
    • 1
  1. 1.School of Science & the EnvironmentManchester Metropolitan UniversityManchesterUK
  2. 2.Department of Geography and Earth ScienceAberystwyth UniversityAberystwythUK

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