Skip to main content

Advertisement

SpringerLink
Log in

Isolation and submerged culture biomass production of the arid land cyanobacteria Microcoleus spp., an investigation on its utilization for biological soil crust restoration

  • Original Article
  • Published:
Environmental Earth Sciences Aims and scope Submit manuscript

Abstract

Biological soil crust (BSC) restoration could effectively contribute in reducing several adverse environmental impacts such as soil erodibility. The usefulness of the microorganism constituent of the arid land (e.g., desert land cyanobacteria Microcoleus) for the BSC restoration has already been introduced, not only by laboratory studies but also by many other field investigations. In order to isolate the soil cyanobacteria with a potential to support BSC succession, soil samples from the southwestern dry lands in Iran were taken, soils serial dilution was prepared and submerged, and streaking-plate methods were applied. The newly isolated native cyanobacterium was identified as the Microcoleus on the genus level following the standard references. The isolated cyanobacterium was cultured phototrophically using five different media consisting of BBM, BG-11, F/2, Jourdan, and artificial wastewater submerged batch. Microcoleus spp. was found in all sites soil samples. The maximum biomass was achieved in the Jourdan submerged culture medium with an amount of 0.88 g/L. The cell density in this culture medium was increased up to 20 times of the initial cell density during 7 days of the cultivation. The specific biomass growth rate was calculated to be in a range of 0.03–0.057 per day. The preliminary experiments and reported restoration activities of Microcoleus submerged cultures were shown to have the potential for providing the soil with the inoculant for the restoration of the degraded arid lands such as Middle East region.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abed RMM, Al Kharusi S, Schramm A, Robinson MD (2010) Bacterial diversity, pigments and nitrogen fixation of biological desert crusts from the Sultanate of Oman. FEMS Microbiol Ecol 72:418–428. doi:10.1111/j.1574-6941.2010.00854.x

    Article  Google Scholar 

  • Akhani H (2015) Sand storms came from where? Iran Newspaper News code 81500795

  • Albalasmeh AA, Berhe AA, Ghezzehei TA (2013) A new method for rapid determination of carbohydrate and total carbon concentrations using UV spectrophotometry. Carbohydr Polym 97:253–261. doi:10.1016/j.carbpol.2013.04.072

    Article  Google Scholar 

  • Alwathnani H, Johansen JR (2011) Cyanobacteria in soils from a Mojave desert ecosystem. Monogr Western N Am Nat 5:71–89. doi:10.3398/042.005.0103

    Article  Google Scholar 

  • Belnap J (2013) Some like it hot, some not. Science 340:1533–1534. doi:10.1126/science.1240318

    Article  Google Scholar 

  • Belnap J, Phillips SL, Witwicki DL, Miller ME (2008) Visually assessing the level of development and soil surface stability of cyanobacterially dominated biological soil crusts. J Arid Environ 72:1257–1264. doi:10.1016/j.jaridenv.2008.02.019

    Article  Google Scholar 

  • Belnap J, Wilcox BP, Van Scoyoc MW, Phillips SL (2013) Successional stage of biological soil crusts: an accurate indicator of ecohydrological condition. Ecohydrology 6:474–482. doi:10.1002/eco.1281

    Article  Google Scholar 

  • Bowker MA (2007) Biological soil crust rehabilitation in theory and practice: an underexploited opportunity. Restor Ecol 15:13–23. doi:10.1111/j.1526-100X.2006.00185.x

    Article  Google Scholar 

  • Briggs AL, Morgan JW (2012) Post-cultivation recovery of biological soil crusts in semi-arid native grasslands, southern Australia. J Arid Environ 77:84–89. doi:10.1016/j.jaridenv.2011.10.002

    Article  Google Scholar 

  • Caicedo NH, Heyduck-Söller B, Fischer U, Thöming J (2011) Bioproduction of antimicrobial compounds by using marine filamentous cyanobacterium cultivation. J Appl Phycol 23:811–818. doi:10.1007/s10811-010-9580-0

    Article  Google Scholar 

  • Campbell SE (1979) Soil stabilization by a prokaryotic desert crust: implications for Precambrian land biota. Origins Life 9:335–348. doi:10.1007/BF00926826

    Article  Google Scholar 

  • Choobari OA, Zawar-Reza P, Sturman A (2014) The global distribution of mineral dust and its impacts on the climate system: a review. Atmos Res 138:152–165. doi:10.1016/j.atmosres.2013.11.007

    Article  Google Scholar 

  • Christenson L, Sims R (2011) Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol Adv 29:686–702

    Article  Google Scholar 

  • De Oteyza TG, Grimalt JO, Diestra E, Solé A, Esteve I (2004) Changes in the composition of polar and apolar crude oil fractions under the action of Microcoleus consortia. Appl Microbiol Biotechnol 66:226–232. doi:10.1007/s00253-004-1694-3

    Article  Google Scholar 

  • De-Bashan L (2002) Removal of ammonium and phosphorus ions from synthetic wastewater by the microalgae Chlorella vulgaris coimmobilized in alginate beads with the microalgae growth-promoting bacterium Azospirillum brasilense. Water Res 36:2941–2948. doi:10.1016/S0043-1354(01)00522-X

    Article  Google Scholar 

  • Dettweiler-Robinson E, Ponzetti JM, Bakker JD (2013) Long-term changes in biological soil crust cover and composition. Ecol Process 2:5. doi:10.1186/2192-1709-2-5

    Article  Google Scholar 

  • Díez B, Ininbergs K (2013) Ecological importance of cyanobacteria. Cyanobacteria. Wiley, Chichester, pp 41–63

    Chapter  Google Scholar 

  • Dvořák P, Hašler P, Poulíčková A (2012) Phylogeography of the Microcoleus vaginatus (Cyanobacteria) from three continents—a spatial and temporal characterization. PLoS ONE 7:e40153. doi:10.1371/journal.pone.0040153

    Article  Google Scholar 

  • Etemadi H, Samadi SZ, Sharifikia M (2012) Statistical downscaling of climatic variables in Shadegan wetland, Iran. Open Access Scientific Reports. doi: 10.4172/scientificreports.508

  • Flechtner VR, Johansen JR, Belnap J (2008) The biological soil crusts of the San Nicolas Island: enigmatic algae from a geographically isolated ecosystem. West N Am Nat 68:405–436. doi:10.3398/1527-0904-68.4.405

    Article  Google Scholar 

  • Gerivani H, Lashkaripour GR, Ghafoori M, Jalali N (2011) The source of dust storm in Iran: a case study based on geological information and rainfall data. Carpath J Earth Environ Sci 6:297–308

    Google Scholar 

  • Gómez DA, Aranibar JN, Tabeni S, Villagra PE, Garibotti IA, Atencio A (2012) Biological soil crust recovery after long-term grazing exclusion in the Monte Desert (Argentina). Changes in coverage, spatial distribution, and soil nitrogen. Acta Oecol 38:33–40. doi:10.1016/j.actao.2011.09.001

    Article  Google Scholar 

  • Harper KT, Belnap J (2001) The influence of biological soil crusts on mineral uptake by associated vascular plants. J Arid Environ 47:347–357. doi:10.1006/jare.2000.0713

    Article  Google Scholar 

  • Hu C, Liu Y, Song L, Zhang D (2002) Effect of desert soil algae on the stabilization of fine sands. J Appl Phycol 14:281–292. doi:10.1023/A:1021128530086

    Article  Google Scholar 

  • Hu C, Gao K, Whitton BA (2012) Semi-arid regions and deserts. Ecology of cyanobacteria II. Springer, Dordrecht, pp 345–369

    Chapter  Google Scholar 

  • Kang Z, Kim B-H, Ramanan R, Choi J-E, Yang J-W, Oh H-M, Kim H-S (2015) A cost analysis of microalgal biomass and biodiesel production in open raceways treating municipal wastewater and under optimum light wavelength. J Microbiol Biotechnol 25:109–118. doi:10.4014/jmb.1409.09019

    Article  Google Scholar 

  • Katoh H, Furukawa J, Tomita-Yokotani K, Nishi Y (2012) Isolation and purification of an axenic diazotrophic drought-tolerant cyanobacterium, Nostoc commune, from natural cyanobacterial crusts and its utilization for field research on soils polluted with radioisotopes. Biochim Biophys Acta (BBA) 1817:1499–1505. doi:10.1016/j.bbabio.2012.02.039

    Article  Google Scholar 

  • Komárek J (2013) Phenotypic characters of heterocytous cyanobacteria. In: Süßwasserflora von Mitteleuropa, Bd. 19/3: Cyanoprokaryota. Springer Berlin, pp 7–42

  • Komárek J, Johansen JR (2015) Filamentous cyanobacteria. In: Freshwater algae of North America. Elsevier, pp 135–235

  • Komárek J, Konstantinos A (2005) Süßwasserflora von Mitteleuropa, Bd. 19/2: Cyanoprokaryota: Bd. 2/Part 2: Oscillatoriales (German Edition). Spektrum Akademischer Verlag; 2007 edition

  • Lababpour A (2013) Cultivation of microalga Chlorella vulgaris in municipal wastewater for biomass production. National bioremediation symposium. Sharif University of Technology, Tehran, pp 8–15

    Google Scholar 

  • Lababpour A (2016) Potentials of the microalgae inoculant in restoration of biological soil crusts to combat desertification. Int J Environ Sci Technol 13:2521–2532. doi:10.1007/s13762-016-1074-4

    Article  Google Scholar 

  • Lan S, Wu L, Zhang D, Hu C (2013) Assessing level of development and successional stages in biological soil crusts with biological indicators. Microb Ecol 66:394–403. doi:10.1007/s00248-013-0191-6

    Article  Google Scholar 

  • Lan S, Wu L, Zhang D, Hu C (2015) Effects of light and temperature on open cultivation of desert cyanobacterium Microcoleus vaginatus. Bioresour Technol 182:144–150. doi:10.1016/j.biortech.2015.02.002

    Article  Google Scholar 

  • Laurens LML (2013) Summative mass analysis of algal biomass—integration of analytical procedures. NREL/TP-5100-60943

  • Li H, Rao B, Wang G, Shen S, Li D, Hu C, Liu Y (2014) Spatial heterogeneity of cyanobacteria-inoculated sand dunes significantly influences artificial biological soil crusts in the Hopq Desert (China). Environ Earth Sci 71(1):245–253. doi:10.1007/s12665-013-2428-6

    Article  Google Scholar 

  • Liu Y, Cockell CS, Wang G, Hu C, Chen L, De Philippis R (2008) Control of Lunar and Martian dust—experimental insights from artificial and natural cyanobacterial and algal crusts in the desert of Inner Mongolia, China. Astrobiology 8:75–86. doi:10.1089/ast.2007.0122

    Article  Google Scholar 

  • Markou G, Georgakakis D (2011) Cultivation of filamentous cyanobacteria (blue-green algae) in agro-industrial wastes and wastewaters: a review. Appl Energy 88:3389–3401. doi:10.1016/j.apenergy.2010.12.042

    Article  Google Scholar 

  • Millennium Ecosystem Assessment (2005) Ecosystems and human well-being: desertification synthesis. World Resources Institute, Washington, DC

    Google Scholar 

  • Moghtaderi A, Taghavi M, Rezaei R (2009) Cyanobacteria in biological soil crust of Chadormalu area, Bafq region in central Iran. PJN 8:1083–1092

    Article  Google Scholar 

  • Patel AK, Huang EL, Low-Décarie E, Lefsrud MG (2015) Comparative shotgun proteomic analysis of wastewater-cultured microalgae: nitrogen sensing and carbon fixation for growth and nutrient removal in Chlamydomonas reinhardtii. J Proteome Res 14:3051–3067. doi:10.1021/pr501316h

    Article  Google Scholar 

  • Pattanaik B, Roleda MY, Schumann R, Karsten U (2008) Isolate-specific effects of ultraviolet radiation on photosynthesis, growth and mycosporine-like amino acids in the microbial mat-forming cyanobacterium Microcoleus chthonoplastes. Planta 227:907–916. doi:10.1007/s00425-007-0666-0

    Article  Google Scholar 

  • Pittman JK, Dean AP, Osundeko O (2011) The potential of sustainable algal biofuel production using wastewater resources. Bioresour Technol 102:17–25. doi:10.1016/j.biortech.2010.06.035

    Article  Google Scholar 

  • Pramanik A, Sundararaman M, Das S, Ghosh U, Mukherjee J (2011) Isolation and characterization of cyanobacteria possessing antimicrobial activity from the Sundarbans, the world’s largest tidal mangrove forest. J Phycol 47:731–743. doi:10.1111/j.1529-8817.2011.01017.x

    Article  Google Scholar 

  • Rincon-Florez V, Carvalhais L, Schenk P (2013) Culture-independent molecular tools for soil and rhizosphere microbiology. Diversity 5:581–612. doi:10.3390/d5030581

    Article  Google Scholar 

  • Rossi F, Potrafka RM, Pichel FG, De Philippis R (2012) The role of the exopolysaccharides in enhancing hydraulic conductivity of biological soil crusts. Soil Biol Biochem 46:33–40. doi:10.1016/j.soilbio.2011.10.016

    Article  Google Scholar 

  • Sarchizian I, Ardelean II (2010) Axenic culture of a diazotrophic filamentous cyanobacterium isolated from mesothermal sulphurous springs (Obanul Mare–Mangalia). Roman J Biol Plant Biol 55:47–53

    Google Scholar 

  • Sheykhi Nejad A, Lababpour A, Moazami N (2016) Increasing cyanobacteria Spirulina production with mixing and chemical composition of culture medium. J Plant Res (Persian) 28:344–353

    Google Scholar 

  • Siangbood H, Ramanujam P (2011) A report on thermophilic cyanophyta (cyanobacteria) from Jakrem Hotspring, Meghalaya. Int J Algae 13:178–185. doi:10.1615/InterJAlgae.v13.i2.70

    Article  Google Scholar 

  • Sima S, Tajrishy M (2006) Water allocation for wetland environmental water requirements: The case of Shadegan wetland, Jarrahi catchment, Iran. In: World Environmental and Water Resource Congress 2006. American Society of Civil Engineers, Reston, VA, pp 1–10

  • Soil Survey Staff (2011) Soil Survey Laboratory Information Manual. Soil Survey Investigations Report No. 45, Version 2.0. R. In: Burt (ed.). U.S. Department of Agriculture, Natural Resources Conservation Service

  • St. Clair LL, Johansen JR (1986) Rapid stabilization of fire-disturbed sites using a soil crust slurry: inoculation studies. Reclam Reveegtation Res 4:261–269

    Google Scholar 

  • Stefanski R, Sivakumar MVK (2009) Impacts of sand and dust storms on agriculture and potential agricultural applications of a SDSWS. IOP Conf Series Earth Environ Sci 7:12016. doi:10.1088/1755-1307/7/1/012016

    Article  Google Scholar 

  • United Nations Convention to Combat Desertification (UNCCD) (2012) Zero Net Land Degradation, a Sustainable Development Goal for Rio 20+ to Secure the Contribution of Our Planet’s Land and Soil to Sustainable Development, Including Food Security and Poverty Eradication. UNCCD secretariat, Bonn, Germany

  • Urmeneta J, Navarrete A, Huete J, Guerrero R (2003) Isolation and characterization of cyanobacteria from microbial mats of the Ebro Delta, Spain. Curr Microbiol 46:199–204. doi:10.1007/s00284-002-3856-9

    Article  Google Scholar 

  • Veste M, Gao J, Sun B, Breckle S-W (2006) The green great wall—combating desertification in China. Geographische Rundundschan 2:14–20

    Google Scholar 

  • 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. doi:10.1016/j.soilbio.2008.07.001

    Article  Google Scholar 

  • Xie Z, Liu Y, Hu C, Chen L, Li D (2007) Relationships between the biomass of algal crusts in fields and their compressive strength. Soil Biol Biochem 39:567–572. doi:10.1016/j.soilbio.2006.09.004

    Article  Google Scholar 

  • Yue SJ, Liu J, Zheng R, Dai YJ, Jia YY, Jia SR, Su JY (2012) The growth of Nostoc flagelliforme cells in desert soil and its ecological effects. Adv Mater Res 518–523:5500–5505. doi:10.4028/www.scientific.net/AMR.518-523.5500

    Article  Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989

    Google Scholar 

  • Zare-Maivan H (2012) Benthic fauna of Shadegan wetland. J Persian Gulf (Mar Sci) 3:37–44

    Google Scholar 

  • Zhao H-L, Guo Y-R, Zhou R-L, Drake S (2010) Biological soil crust and surface soil properties in different vegetation types of Horqin Sand Land, China. CATENA 82:70–76. doi:10.1016/j.catena.2010.05.002

    Article  Google Scholar 

  • Zheng Y, Xu M, Zhao J, Bei S, Hao L (2011) Effects of inoculated Microcoleus vaginatus on the structure and function of biological soil crusts of desert. Biol Fertil Soils 47:473–480. doi:10.1007/s00374-010-0521-5

    Article  Google Scholar 

  • Zhu H, Cao C, Zhang S, Zhang Y, Zou W (2011) Bioresource Technology pH-control modes in a 5-L stirred-tank bioreactor for cell biomass and exopolysaccharide production by Tremella fuciformis spore. Bioresour Technol 102:9175–9178. doi:10.1016/j.biortech.2011.06.086

    Article  Google Scholar 

  • Zhu L, Hiltunen E, Shu Q, Zhou W, Li Z, Wang Z (2014) Biodiesel production from algae cultivated in winter with artificial wastewater through pH regulation by acetic acid. Appl Energy 128:103–110. doi:10.1016/j.apenergy.2014.04.039

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank National Institute of Genetic Engineering and Biotechnology (940801-I-535). Sayed Majed Mousavi Fard is gratefully acknowledged for helps in providing soil samples.

Author information

Authors and Affiliations

  1. Department of Industrial and Environmental Biotechnology, National Institute of Genetic Engineering and Biotechnology, P.O. Box 14965-161, Tehran, Iran

    Abdolmajid Lababpour & Marzieh Kaviani

Authors
  1. Abdolmajid Lababpour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marzieh Kaviani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdolmajid Lababpour.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lababpour, A., Kaviani, M. Isolation and submerged culture biomass production of the arid land cyanobacteria Microcoleus spp., an investigation on its utilization for biological soil crust restoration. Environ Earth Sci 75, 1495 (2016). https://doi.org/10.1007/s12665-016-6313-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12665-016-6313-y

Keywords

Search

Navigation