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Ecological Research

, Volume 33, Issue 3, pp 629–640 | Cite as

Biological crusts of serpentine and non-serpentine soils from the Barberton Greenstone Belt of South Africa

  • Arthurita VenterEmail author
  • Stefan Siebert
  • Nishanta Rajakaruna
  • Sandra Barnard
  • Anatoliy Levanets
  • Arshad Ismail
  • Mushal Allam
  • Bianca Peterson
  • Tomasz Sanko
Special Feature Ultramafic Ecosystems: Proceedings of the 9th International Conference on Serpentine Ecology

Abstract

Climate and geography can influence biological soil crust (BSC) community composition, but local heterogeneity in variables such as soil characteristics or microclimate gradients can also impact cryptogamic diversity. Heavy metals and nutrient imbalances in serpentine soils are known to influence the distributions of higher plants, but cryptogamic species appear to be more tolerant of substrate. The aim of this study was to compare the cryptogamic composition of serpentine and non-serpentine soils by using integrative taxonomy, which combines morphological and DNA barcoding data, to determine how soil characteristics in combination with rainfall can influence BSC community composition. Samples from serpentine and non-serpentine soils were enumerated and total genomic DNA was isolated from the soil samples. Analyses of the 16S rRNA gene and ITS sequences were done using the quantitative insights into microbial ecology (QIIME) workflow to determine which eukaryotic microorganisms were present in the samples. Sixty genera from the Cyanophyceae (38), Chlorophyceae (10), Bacillariophyceae (6), Eustigmatophyceae (4), Trebouxiophyceae (1) and Xanthophyceae (1) classes were detected with this approach. Results confirm that algae and cyanobacteria are tolerant of most substrates and can even colonize environments with high levels of heavy metal and nutrient imbalances, if moisture is present. Genera such as Acaryochloris, Annamia, Brasilonema, Chrocosphaera, Halomicronema, Planktothricoides, Rubidibacter, and Toxopsis are reported for the first time for South African soil.

Keywords

Algae Cyanobacteria Metagenomics Microbial diversity Serpentine geoecology 

Notes

Acknowledgements

We want to thank the staff at Eko-Analitika, North-West University, Potchefstroom for the soil analyses, Gustav Havenga for drawing the map of the study area and the National Geographic Society for financial assistance (NGS Grant #9774-15). We also thank two anonymous reviewers for their constructive comments, which helped us improve the manuscript.

References

  1. Alexander EB, Coleman RG, Keeler-Wolf T, Harrison SP (2007) serpentine geoecology of western North America: geology, soils and vegetation. Oxford University Press, New YorkGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  3. Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/. Accessed 12 May 2017
  4. Baker CCM (2016) Entrez_qiime: a utility for generating QIIME input files from the NCBI databases. http://github.com/bakerccm/entrez_qiime release v2.0
  5. Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Process 20:3159–3178.  https://doi.org/10.1002/hyp.6325 CrossRefGoogle Scholar
  6. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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 57:229–247CrossRefPubMedGoogle Scholar
  8. Cabala J, Rahmonov O, Jablonska M, Teper E (2011) Soil algal colonization and its ecological role in an environment polluted by past Zn–Pb mining and smelting activity. Water Air Soil Pollut 215:339–348CrossRefGoogle Scholar
  9. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010a) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267CrossRefPubMedGoogle Scholar
  10. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Gonzalez Pena A, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald C, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010b) QIIME allows analysis of high-throughput community sequencing data. Nat Methods.  https://doi.org/10.1038/nmeth.f.303 PubMedPubMedCentralCrossRefGoogle Scholar
  11. Castle S (2010) Chlorophyll-a double extraction with methanol. Arid Lands Ecology Laboratory. http://www.colorado.edu accessed. Accessed 13 Feb 2012
  12. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dojani S, Kauff F, Weber B, Büdel B (2014) Genotypic and phenotypic diversity of cyanobacteria in biological soil crusts of the Succulent Karoo and Nama Karoo of southern Africa. Microb Ecol 67:286–301.  https://doi.org/10.1007/s00248-013-0301-5 CrossRefPubMedGoogle Scholar
  14. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefPubMedGoogle Scholar
  15. Ettl H, Gärtner G, Heynig H, Mollenhauer D, Komárek J, Anagnostidis K (1999) Süsswasser von Mittleeuropa: Cyanoprokaryota, Teil 1: Chroococcales. Gustav Fischer Verlag, StuttgartGoogle Scholar
  16. Henriques M, Silva A, Rocha J (2007) Extraction and quantification of pigments from marine microalgae: a simple and reproducible method. Formatex 1:586–593Google Scholar
  17. Hindak F (2008) Atlas of Cyanophytes. VEDA, BratislavaGoogle Scholar
  18. Hötzel G, Croome R (1999) A phytoplankton methods manual for Australian freshwaters. Canberra: Land and Water Resources Research and Development Corporation Occasional Paper 22/99Google Scholar
  19. Hüber-Pestalozzi G (1961) Das Phytoplankton des Süsswassers: Systematik und Biologie Tiel 5: Chlorophyceae (Grünalgen). Ordnung: Volvocales. E Schweizerbart’sche. Verlagbuchhandlung, StuttgartGoogle Scholar
  20. John DM, Whitton BA, Brook AJ (2002) Freshwater algal flora of the British Isles: a guide to freshwater and terrestrial algae. Cambridge University Press, CambridgeGoogle Scholar
  21. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1CrossRefPubMedGoogle Scholar
  22. Komárek J, Anagnostidis K (2005) Cyanoprokaryota: Oscillatoriales. Spektrum Akademischer Verlag, HeidelbergGoogle Scholar
  23. Krüger GHJ (1978) The effect of physico-chemical factors on the growth relevant to the mass culture of Microsystis under sterile conditions. PhD thesis, University of the Orange Free State, South AfricaGoogle Scholar
  24. Lamprinou V, Skaraki K, Kotoulas G, Economou-Amilli A, Pantazidou A (2012) Toxopsis calypsus gen. nov., sp. nov. (Cyanobacteria, Nostocales) from cave ‘Francthi’, Peloponnese, Greece: a morphological and molecular evaluation. Int J Syst Evol Microbiol 62:2870–2877.  https://doi.org/10.1099/ijs.0.038679-0 CrossRefPubMedGoogle Scholar
  25. Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD (2012) PANDAseq: paired-end assembler for illumina sequences. BMC Bioinform 13:31. http://www.biomedcentral.com/1471-2105/13/31. Accessed 12 May 2017
  26. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618CrossRefPubMedGoogle Scholar
  27. Mucina L, Rutherford MC (2006) The vegetation of South Africa, Lesotho and Swaziland. Strelitzia 19. SANBI, PretoriaGoogle Scholar
  28. NSSSA (Non-Affiliated Soil Analysis Work Committee, Soil Science Society of South Africa) (1990) Handbook of standard soil testing methods for advisory purposes. Soil Science Society of South Africa, PretoriaGoogle Scholar
  29. Orlekowsky T, Venter A, Van Wyk F, Levanets A (2013) Cyanobacteria and algae of gold mine tailings in the Northwest Province of South Africa. Nova Hedwiga 97:281–294CrossRefGoogle Scholar
  30. Pessoa-Filho M, Barreto CC, Dos Reis Junior FB, Fragoso RR, Costa FS, Mendes De Caralho, De Andrade LRM (2015) Microbiological functioning, diversity and structure of bacterial communities in ultramafic soils from a tropical savanna. Antonie Van Leeuwenhoek 107:935–949CrossRefPubMedGoogle Scholar
  31. Pires AC, Marinoni L (2010) DNA barcoding and traditional taxonomy unified through Integrative Taxonomy: a view that challenges the debate questioning both methodologies. Biota Neotropica 10: http://www.biotaneotropica.org.br/v10n2/en/abstract?thematic-review+bn03110022010. Accessed 12 May 2017
  32. Rajakaruna NB, Harris TB, Alexander EB (2009) Serpentine geoecology of Eastern North America: a review. Rhodora 111:21–108CrossRefGoogle Scholar
  33. Schulz K, Mikhailyuk T, Drebler M, Leinweber P, Karsten U (2016) Biological soil crusts from coastal dunes at the Baltic Sea: cyanobacterial and algal biodiversity and related soil properties. Microb Ecol 71:178–193CrossRefPubMedGoogle Scholar
  34. Shade A (2015) Intro to QIIME for amplicon analysis. https://tinyurl.com/y84hkzn5. Accessed 12 May 2017
  35. Smith MA, Rodriquez JJ, Whitfield JB, Deans AR, Janzen DH, Hallwachs W, Hebert PDN (2008) Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. PNAS 105:12359–12364CrossRefPubMedPubMedCentralGoogle Scholar
  36. Taylor JC, Harding WR, Archibald CGM (2007) An illustrated guide to some common diatom species from South Africa. WRC report TT282/07Google Scholar
  37. Ter Braak CJF, Smilauer P (1998) CANOCO Reference Manual and User’s Guide to Canoco for Windows: Software for Canonical Community Ordination v 4. Microcomputer Power. Ithaca, New YorkGoogle Scholar
  38. US EPA (1996) Method 3050B. Acid digestion of sediments, sludges, and soils. http://www.epa.gov/wastes/hazard/testmethods/sw846/online/3_series.htm. Accessed 8 Aug 2017
  39. Venter A, Levanets A, Siebert S, Rajakaruna N (2015) A preliminary survey of the diversity of soil algae and cyanoprokaryotes on mafic and ultramafic substrates in South Africa. Aust J Bot 63:341–352.  https://doi.org/10.1071/BT14207 CrossRefGoogle Scholar
  40. 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 73:5261–5267CrossRefPubMedPubMedCentralGoogle Scholar
  41. Wehr JD, Sheath RG (2003) Freshwater algae of North America, ecology and classification. Academic Press, LondonGoogle Scholar
  42. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press Inc, New York, pp 315–322Google Scholar
  43. Wickham H (2009) Ggplot2: elegant graphics for data analysis. ggplot2: elegant graphics for data analysis, vol 35.  https://doi.org/10.1007/978-0-387-98141-3
  44. Williamson SD, Balkwill K (2015) Plant census and floristic analysis of selected serpentine outcrops of the Barberton Greenstone Belt, Mpumalanga, South Africa. S Afr J Bot 97:133–142.  https://doi.org/10.1016/j.sajb.2014.12.004 CrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2017

Authors and Affiliations

  1. 1.Unit for Environmental Sciences and ManagementNorth-West UniversityPotchefstroomSouth Africa
  2. 2.Biological Sciences DepartmentCalifornia Polytechnic State UniversitySan Luis ObispoUSA
  3. 3.Sequencing Core FacilityNational Institute for Communicable Diseases, A Division of the National Health Laboratory ServiceJohannesburgSouth Africa

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