Abstract
Background and aims
Cyanobacteria from biocrusts can enhance soil function and structure, a critical objective when restoring degraded dryland ecosystems. Large-scale restoration of biodiversity requires direct seeding of native plant species, and bio-priming seeds with cyanobacteria is a potential method of initiating enhanced soil functioning. The utility of cyanobacteria for improving soil is therefore dependent on whether target plant species remain unaffected during its application.
Methods
Cyanobacteria from the genera Microcoleus and Nostoc were isolated from locally-sourced biocrust samples, and cultured under controlled conditions. A two-factor laboratory experiment was conducted including cyanobacteria and the culture growth medium (BG11) as factors. We bio-primed seeds of five species native to Western Australia, commonly used in dryland restoration, by soaking them in the cultures developed, and assessed germination and growth.
Results
We found significant positive effects of seeds bio-primed with cyanobacteria on germination and seedling growth of two species, Senna notabilis and Acacia hilliana, respectively. Importantly, no significant negative effects of cyanobacteria were found for any of the species studied.
Conclusions
Few studies of cyanobacteria effects on regeneration of native species exist. We found that the potential benefits of applying indigenous bacteria via bio-priming seeds would not inhibit plant establishment, and indeed may be beneficial for some species used in dryland restoration.
Similar content being viewed by others
References
Abari AK, Nasr MH, Bayat D (2011) Salt effects on seed germination and seedling emergence of two acacia species. African J Plant Sci 5:52–56
Anaya-Romero M, Abd-Elmabod SK, Muñoz-Rojas M, Castellano G, Ceacero CJ, Alvarez S, Méndez M, De la Rosa D (2015) Evaluating soil threats under climate change scenarios in the Andalusia region, southern Spain. Land Degrad Dev 26:441–449
Antoninka A, Bowker MA, Reed SC, Doherty K (2016) Production of greenhouse-grown biocrust mosses and associated cyanobacteria to rehabilitate dryland soil function. Restor Ecol 24:324–335
Arnold S, Kailichova Y, Knauer J, Ruthsatz AD, Baumgartl T (2014) Effects of soil water potential on germination of co-dominant Brigalow species: implications for rehabilitation of water-limited ecosystems in the Brigalow Belt bioregion. Ecol Eng 70:35–42
Azza Mazher AM, EM FEL-Q, Farahat MM (2007) Responses of ornamental plants and woody trees to salinity. World J Agric Sci 3(3):386–395
Bateman A, Lewandrowski W, Stevens J, Muñoz-Rojas M (2016) Ecophysiological indicators to assess drought responses of arid zone native seedlings in reconstructed soils. Land Degrad Dev. https://doi.org/10.1002/ldr.2660
Bowker MA (2007) Biological soil crust rehabilitation in theory and practice: an underexploited opportunity. Restor Ecol 15:13–23
Büdel B, Dulic T, Darienko T, Rybalka N, Friedl T (2016) Cyanobacteria and algae of biological soil crusts. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Springer international publishing, Cham, pp 55–80
Büdel B, Williams WJ, Reichenberger H (2018) Annual net primary productivity of a cyanobacteria-dominated biological soil crust in the Gulf Savannah, Queensland, Australia. Biogeosciences 15(2):491–505
Chamizo S, Cantón Y, Miralles I, Domingo F (2012) Biological soil crust development affects physicochemical characteristics of soil surface in semiarid ecosystems. Soil Biol Biochem 49:96–105
Chilton AM, Neilan BA, Eldridge DJ (2017) Biocrust morphology is linked to marked differences in microbial community composition. Plant Soil. https://doi.org/10.1007/s11104-017-3442-3
Chittapun S, Limbipichai S, Amnuaysin N, Boonkerd R, Charoensook M (2017) Effects of using cyanobacteria and fertilizer on growth and yield of rice, Pathum Thani I: a pot experiment. J Appl Phycol. https://doi.org/10.1007/s10811-017-1138-y
Commander LE, Golos PJ, Miller BP, Merritt DJ (2017) Seed germination traits of desert perennials. Plant Ecol 218:1077–1091
Debez A, Ben Hamed K, Grignon C et al (2004) Salinity effects on germination, growth, and seed production of the halophyte Cakile Maritima. Plant Soil 262:179–189
Elliott DR, Thomas AD, Hoon SR, Sen R (2014) Niche partitioning of bacterial communities in biological crusts and soils under grasses, shrubs and trees in the Kalahari. Biodivers Conserv 23:1709–1733
Erickson TE, Barrett RL, Symons DR, Turner SR, Merritt DJ (2016) An atlas to the plants and seeds of the Pilbara region. In: Erickson TE, Barrett RL, Merritt DJ, Dixon KW (eds) Pilbara seed atlas and field guide: plant restoration in Australia's arid northwest. CSIRO Publishing, Dickson, pp 43–256
Erickson TE, Muñoz-Rojas M, Kildisheva OA, Stokes BA, White SA, Heyes JL, Dalziell EL, Lewandrowski W, James JJ, Madsen MD, Turner SR, Merritt DJ (2017) Benefits of adopting seed-based technologies for rehabilitation in the mining sector: a Pilbara perspective. Aust J Bot 65:646. https://doi.org/10.1071/BT17154
Escudero A, de la Martínez I, Cruz A, Otáora MAG, Maestre FT (2007) Soil lichens have species-specific effects on the seedling emergence of three gypsophile plant species. J Arid Environ 70:18–28
Garcia-Pichel F, Prufert-Bebout L, Muyzer G (1996) Phenotypic and phylogenetic analyses show Microcoleus Chthonoplastes to be a cosmopolitan cyanobacterium. Appl Environ Microbiol 62:3284–3291
Garcia-Pichel F, Loza V, Marusenko Y, Mateo P, Potrafka RM (2013) Temperature drives the continental-scale distribution of key microbes in topsoil communities. Science 340:1574–1577
George B, Pancha I, Desai C, Chokshi K, Paliwal C, Ghosh T, Mishra S (2014) Effects of different media composition, light intensity and photoperiod on morphology and physiology of freshwater microalgae Ankistrodesmus falcatus – a potential strain for bio-fuel production. Bioresour Technol 17:1367–1374
Hosseini M, Powell A, Bingham I (2002) Comparison of the seed germination and early seedling growth of soybean in saline conditions. Seed Sci Res 12(3):165–172. https://doi.org/10.1079/SSR2002108
Jiménez-Alfaro B, Silveira FAO, Fidelis A, Poschlod P, Commander LE (2016) Seed germination traits can contribute better to plant community ecology. J Veg Sci 27:637–645. https://doi.org/10.1111/jvs.12375
Keesstra S, Nunes J, Novara A, Finger AD, Kalantari Z, Cerdà A (2018) The superior effect of nature based solutions in land management for enhancing ecosystem services. Sci Total Environ 610:997–1009. https://doi.org/10.1016/j.scitotenv.2017.08.077
Kim S, Rayburn AL, Voigt T, Parrish A, Lee DK (2012) Salinity effects on germination and plant growth of prairie cordgrass and switchgrass. Bioenerg Res 5:225–235. https://doi.org/10.1007/s12155-011-9145-3
Kneller T, Harris R, Bateman A, Muñoz-Rojas M (2018) Native-plant amendments and topsoil addition to enhance soil quality in post-mining arid grasslands. Sci Total Environ 621:744–752. https://doi.org/10.1016/j.scitotenv.2017.11.219
Larson JE, Funk JL (2016) Regeneration: an overlooked aspect of trait-based plant community assembly models. J Ecol 104:1284–1298
Liu R, Li K, Zhang H, Zhu J, Joshi D (2014) Spatial distribution of microbial communities associated with dune landform in the Gurbantunggut Desert, China. J. Microbiol 52(11):898–907
McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A et al (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618
Miller BP, Sinclair EA, Menz MHM, Elliott CP, Bunn E, Commander LE, Dalziell E, David E, Davis B, Erickson TE, Golos PJ, Krauss SL, Lewandrowski W, Mayence CE, Merino-Martín L, Merritt DJ, Nevill PG, Phillips RD, Ritchie AL, Ruoss S, Stevens JC (2017) A framework for the practical science necessary to restore sustainable, resilient, and biodiverse ecosystems. Restor Ecol 25(4):605–617
Muñoz-Rojas M, Erickson TE, Martini DC, Dixon KW, Merritt DJ (2016a) Climate and soil factors influencing seedling recruitment of plant species used for dryland restoration. Soil 2:287–298. https://doi.org/10.5194/soil-2-287-2016
Muñoz-Rojas M, Erickson TE, Dixon KW, Merritt DJ (2016b) Soil quality indicators to assess functionality of restored soils in degraded semiarid ecosystems. Restor Ecol 24:S43–S52
Nunes da Rocha U, Cadillo-Quiroz H, Karaoz U, Rajeev L, Klitgord N, Dunn S, Truong V, Buenrostro M, Bowen BP, Garcia-Pichel F, Mukhopadhyay A, Northen TR, Brodie EL (2015) Isolation of a significant fraction of non-phototroph diversity from a desert biological soil crust. Front Microbiol 6:277
O’Callaghan M (2016) Microbial inoculation of seed for improved crop performance: issues and opportunities. Appl Microbiol Biotechnol 100:5729–5746
Ooi MKJ (2007) Dormancy classification and potential dormancy-breaking cues for shrub species from fire-prone south-eastern Australia. In: Adkin S, Ashmore S, Navie SC (eds) Seeds: biology, development and ecology. CABI, Wallingford, pp 205–216
Ooi MKJ, Auld TD, Whelan RJ (2004) Comparison of the cut and tetrazolium tests for assessing seed viability: a study using Australian native Leucopogon species. Ecol Manag Restor 5:141–143
Ooi MKJ, Auld TD, Denham AJ (2009) Climate change and bet-hedging: interactions between increased soil temperatures and seed bank persistence. Glob Chang Biol 15:2375–2386
Park C-H, Li XR, Zhao Y, Jia RL, Hur J-S (2017) Rapid development of cyanobacterial crust in the field for combating desertification. PLoS One 12(6):e0179903. https://doi.org/10.1371/journal.pone.0179903
Parsons RF (2012) Incidence and ecology of very fast germination. Seed Sci Res 22:161–167
Perring MP, Standish RJ, Price JN, Craig MD, Erickson TE, Ruthrof KX, Whiteley AS, Valentine LE, Hobbs RJ (2015) Advances in restoration ecology: rising to the challenges of the coming decades. Ecosphere 6(8):art131
Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10(8):551–562
R Core Team 2017 R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/. Accessed 25 Oct 2017
Rehman S, Harris PJC, Bourne WF, Wilkin J (2000) The relationship between ions, vigour and salinity tolerance of acacia seeds. Plant Soil 220:229–233
Rippka R (1988) Isolation and purification of cyanobacteria. Methods Enzymol 167:3–27
Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22
Rossi F, Li H, Liu Y, De Philippis R (2017) Cyanobacterial inoculation (cyanobacterisation): perspectives for the development of a standardized multifunctional technology for soil fertilization and desertification reversal. Earth Sci Rev 171:28–43
Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310
Singh JS, Kumar A, Rai AN, Singh DP (2016) Cyanobacteria: a precious bioresource in agriculture, ecosystem, and environmental sustainability. Front Microbiol 7:1–9
Song G, Li X, Hui R (2017) Effect of biological soil crusts on seed germination and growth of an exotic and two native plant species in an arid ecosystem. PLoS One 12(10):e0185839
Su YG, Li XR, Zheng JG, Huang G (2009) The effect of biological soil crusts of different successional stages and conditions on the germination of seeds of three desert plants. J Arid Environ 73:931–936
Velasco Ayuso S, Giraldo Silva A, Nelson CJ, Barger NN, Garcia-Pichel F (2016) Microbial nursery production of high-quality biological soil crust biomass for restoration of degraded dryland soils. Appl Environ Microbiol 83:e02179–e02116. https://doi.org/10.1128/AEM.02179-16
Wang W, Liu Y, Li D, Hu C, Rao B (2009) Feasibility of cyanobacterial inoculation for biological soil crusts formation in desert area. Soil Biol Biochem 41:926–929
Williams WJ, Büdel B, Reichenberger H, Rose N (2014) Cyanobacteria in the Australian northern savannah detect the difference between intermittent dry season and wet season rain. Biodivers Conserv 23:1827–1184
Xu Y, Rossi F, Colica G, Deng S, Philippis RD, 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 49:143–152
Zaady E, Gutterman Y, Boeken B (1997) The germination of mucilaginous seeds of Plantago Coronopus, Reboudia pinnata, and Carrichtera Annua on cyanobacterial soil crust from the Negev Desert. Plant Soil 190:247–252
Zhang YM, Belnap J (2015) Growth responses of five desert plants as influenced by biological soil crusts from a temperate desert, China. Ecol Res 30:1037–1045
Zhang Y, Aradottir AL, Serpe M (2016) Interactions of biological soil crusts with vascular plants. Biological Soil Crusts: An Organizing Principle in Drylands. Springer International Publishing, Switzerland, pp 385–406
Acknowledgements
This research project was supported by BHP Billiton Iron Ore Community Development Project (contract no. 8600048550) under the auspices of the Restoration Seedbank Initiative (2013-2018), a partnership between BHP Billiton Iron Ore, The University of Western Australia, and the Botanic Gardens and Parks Authority; and The University of Western Australia Research Collaboration Award 2018 Innovative nature-based strategies for drylands restoration: the potential of indigenous cyanobacteria. MMR acknowledges the support from the Australian Research Council Discovery Early Career Researcher Award (DE180100570).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Fernando T. Maestre.
Rights and permissions
About this article
Cite this article
Muñoz-Rojas, M., Chilton, A., Liyanage, G.S. et al. Effects of indigenous soil cyanobacteria on seed germination and seedling growth of arid species used in restoration. Plant Soil 429, 91–100 (2018). https://doi.org/10.1007/s11104-018-3607-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-018-3607-8