[en] Cyanobacteria inoculation has recently become an innovative biotechnological tool for restoring degraded arid soils. A major challenge for researchers, however, is the search for suitable species able to cope with water stress under field conditions. The aim of this study was to test the effect of water availability on induced biocrust growth in three different degraded soils from semiarid areas of Almeria (Spain). Three native N-fixing cyano-bacterial strains, Nostoc commune, Scytonema hyalinum and Tolypothrix distorta, were inoculated on soil samples from the study areas, individually and as a consortium. Two different irrigation treatments simulating the water availability in the selected areas, in a dry year (180 mm/year) and a wet year (380 mm/year), were applied for three months under laboratory conditions. Cyanobacteria cover, chlorophyll a spectral absorption (Chla spectral absorption), soil organic carbon (SOC) and total exopolysaccharide (EPS) gains were measured as indicators of biocrust development. Cyanobacteria crust cover, SOC and EPS gains were higher in inoculated soils than in
uninoculated soils. Even though the hydration regime had a generally significant effect on cyanobacteria cover, Chla spectral absorption and EPS, similar biocrust development and improvement in edaphic conditions were observed under both hydration regimes for all treatments. Of the candidate inoculants, N. commune showed remarkably higher performance under dry conditions than the rest, providing evidence of high potential for growing under water-limited conditions and being a good candidate inoculant for restoration of arid degraded areas.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Román, JR; University of Almería > Agronomy
Roncero Ramos, Beatriz ; Université de Liège - ULiège > Département des sciences de la vie > Centre d'ingénierie des protéines
Rodríguez-Caballero, Emilio; University of Almería > Agronomy
Chamizo, S; University of Almería > Agronomy
Cantón, Y; University of Almería > Agronomy
Language :
English
Title :
Effect of water availability on induced cyanobacterial biocrust development
Publication date :
2021
Journal title :
Catena
ISSN :
0341-8162
eISSN :
1872-6887
Publisher :
Elsevier, Netherlands
Volume :
197
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
RESUCI project (CGL2014-59946-R); REBIOARID project (RTI2018-101921-B-I00); Spanish National Plan for Research; RH2O-ARID (P18-RT-5130); FPU predoctoral fellowship (FPU14/05806); Special Funds for Research, IPD-STEMA Programme; HIPATIA-UAL postdoctoral fellowship
Funders :
EU - European Union ERDF - European Regional Development Fund Junta de Andalucía ULiège - Université de Liège UAL - University of Almería
Abiven, S., Menasseri, S., Chenu, C., 2009. The effects of organic inputs over time on soil aggregate stability - A literature analysis. Soil Biol. Biochem. https://doi.org/10.1016/j.soilbio.2008.09.015.
Acea, M., Cyanobacterial inoculation of heated soils: effect on microorganisms of C and N cycles and on chemical composition in soil surface. Soil Biol. Biochem. 35 (2003), 513–524, 10.1016/S0038-0717(03)00005-1.
Adessi, A., Cruz de Carvalho, R., De Philippis, R., Branquinho, C., Marques da Silva, J., Microbial extracellular polymeric substances improve water retention in dryland biological soil crusts. Soil Biol. Biochem. 116 (2018), 67–69, 10.1016/j.soilbio.2017.10.002.
Antoninka, A., Bowker, M.A., Reed, S.C., Doherty, K., Production of greenhouse-grown biocrust mosses and associated cyanobacteria to rehabilitate dryland soil function. Restor. Ecol., 1–12, 2015, 10.1111/rec.12311.
Ayuso, S.V., Silva, A.G., Nelson, C., Barger, N.N., Garcia-Pichel, F., Microbial nursery production of high-quality biological soil crust biomass for restoration of degraded dryland soils. Appl. Environ. Microbiol., 83, 2017, 10.1128/AEM.02179-16.
Belnap, J., Weber, B., Büdel, B., Biological Soil Crusts as an Organizing Principle in Drylands. Weber, B., Büdel, B., Belnap, J., (eds.) Biological Soil Crust: An Organizing Principle in Drylands, 2016, Ecological Studies, Springer, Berlin, 3–15.
Bu, C., Wu, S., Yang, Y., Zheng, M., Identification of factors influencing the restoration of cyanobacteria-dominated biological soil crusts. PLoS ONE 9 (2014), 1–8, 10.1371/journal.pone.0090049.
Cantón, Y., Chamizo, S., Rodríguez-Caballero, E., Lázaro, R., Roncero-Ramos, B., Román, J.R., Solé-Benet, A., Water Regulation in Cyanobacterial Biocrusts from Drylands: Negative Impacts of Anthropogenic Disturbance. Water, 12, 2020, 720, 10.3390/w12030720.
Chamizo, S., Cantón, Y., Miralles, I., Domingo, F., Biological soil crust development affects physicochemical characteristics of soil surface in semiarid ecosystems. Soil Biol. Biochem. 49 (2012), 96–105, 10.1016/j.soilbio.2012.02.017.
Chamizo, S., Rodríguez-Caballero, E., Román, J.R., Cantón, Y., Effects of biocrust on soil erosion and organic carbon losses under natural rainfall. Catena 148 (2017), 117–125, 10.1016/j.catena.2016.06.017.
Chamizo, S., Mugnai, G., Rossi, F., Certini, G., De Philippis, R., Cyanobacteria inoculation improves soil stability and fertility on different textured soils: Gaining insights for applicability in soil restoration. Front. Environ. Sci., 6, 2018, 10.3389/fenvs.2018.00049.
Chamizo, S., Adessi, A., Mugnai, G., Simiani, A., De Philippis, R., Soil Type and Cyanobacteria Species Influence the Macromolecular and Chemical Characteristics of the Polysaccharidic Matrix in Induced Biocrusts. Microb. Ecol. 78 (2019), 482–493, 10.1007/s00248-018-1305-y.
Chaudhary, V.B., Bowker, M.A., O'Dell, T.E., Grace, J.B., Redman, A.E., Rillig, M.C., Johnson, N.C., Untangling the biological contributions to soil stability in semiarid shrublands. Ecol. Appl. 19 (2009), 110–122, 10.1890/07-2076.1.
Childs, E.C., The use of soil moisture characteristics in soil studies. Soil Sci. 50 (1940), 239–252.
Childs, E.C., Collis-George, N., The permeability of porous materials. Proc. Roy. Soc., Ser. A 201 (1950), 392–405.
Colica, G., Li, H., Rossi, F., Li, D., Liu, Y., De Philippis, R., Microbial secreted exopolysaccharides affect the hydrological behavior of induced biological soil crusts in desert sandy soils. Soil Biol. Biochem. 68 (2014), 62–70, 10.1016/j.soilbio.2013.09.017.
Cowie, A.L., Orr, B.J., Castillo Sanchez, V.M., Chasek, P., Crossman, N.D., Erlewein, A., Louwagie, G., Maron, M., Metternicht, G.I., Minelli, S., Tengberg, A.E., Walter, S., Welton, S., Land in balance: The scientific conceptual framework for Land Degradation Neutrality. Environ. Sci. Policy 79 (2018), 25–35, 10.1016/j.envsci.2017.10.011.
Dojani, S., Büdel, B., Deutschewitz, K., Weber, B., Rapid succession of Biological Soil Crusts after experimental disturbance in the Succulent Karoo, South Africa. Appl. Soil Ecol. 48 (2011), 263–269, 10.1016/j.apsoil.2011.04.013.
Dojani, S., Kauff, F., Weber, B., Büdel, B., Genotypic and Phenotypic Diversity of Cyanobacteria in Biological Soil Crusts of the Succulent Karoo and Nama Karoo of Southern Africa. Microb. Ecol. 67 (2014), 286–301, 10.1007/s00248-013-0301-5.
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F., 1956. Colorimetric Method for Determination of Sugars and Related Substances. Anal. Chem. https://doi.org/10.1021/ac60111a017.
Fernandes, V.M.C., Machado de Lima, N.M., Roush, D., Rudgers, J., Collins, S.L., Garcia-Pichel, F., Exposure to predicted precipitation patterns decreases population size and alters community structure of cyanobacteria in biological soil crusts from the Chihuahuan Desert. Environ. Microbiol. 20 (2018), 259–269, 10.1111/1462-2920.13983.
Franzluebbers, A., Water infiltration and soil structure related to organic matter and its stratification with depth. Soil Tillage Res. 66 (2002), 197–205.
Giraldo-Silva, A., Nelson, C., Barger, N.N., Garcia-Pichel, F., Nursing biocrusts: isolation, cultivation, and fitness test of indigenous cyanobacteria. Restor. Ecol. 27 (2019), 793–803, 10.1111/rec.12920.
Giraldo-Silva, A., Nelson, C., Penfold, C., Barger, N.N., Garcia-Pichel, F., 2019b. Effect of preconditioning to the soil environment on the performance of 20 cyanobacterial strains used as inoculum for biocrust restoration. Restor. Ecol. https://doi.org/10.1111/rec.13048.
Harel, Y., Ohad, I., Kaplan, A., Activation of photosynthesis and resistance to photoinhibition in cyanobacteria within biological desert crust. Plant Physiol. 136 (2004), 3070–3079, 10.1104/pp.104.047712.
Helm, R.F., Huang, Z., Edwards, D., Leeson, H., Peery, W., Potts, M., Structural characterization of the released polysaccharide of desiccation-tolerant Nostoc commune DRH-1. J. Bacteriol. 182 (2000), 974–982, 10.1128/JB.182.4.974-982.2000.
Hill, D.R., Keenan, T.W., Helm, R.F., Potts, M., Crowe, L.M., Crowe, J.H., Extracellular polysaccharide of Nostoc commune (Cyanobacteria) inhibits fusion of membranes vesicles during desiccation. J. Appl. Phycol. 9 (1997), 237–248, 10.1023/A:1007965229567 14.
Kheirfam, H., Sadeghi, S.H., Zarei Darki, B., Homaee, M., Controlling rainfall-induced soil loss from small experimental plots through inoculation of bacteria and cyanobacteria. Catena 152 (2017), 40–46, 10.1016/j.catena.2017.01.006.
Kubečková, K., Johansen, J.R., Warren, S.D., Sparks, R., 2009. Development of immobilized cyanobacterial amendments for reclamation of microbiotic soil crusts. Arch. Hydrobiol. Suppl. Algol. Stud. https://doi.org/10.1127/1864-1318/2003/0109-0341.
Lange, O.L., Photosynthesis of Soil Crust Biota as Dependent on Environmental Factors. Belnap, J., Lange, O.L., (eds.) Biological Soil Crust: Structure, Function and Management, 2001, Ecological Studies, Springer, Berlin, 217–240.
Maestre, F.T., Martín, N., Díez, B., López-Poma, R., Santos, F., Luque, I., Cortina, J., Watering, fertilization, and slurry inoculation promote recovery of biological crust function in degraded soils. Microb. Ecol. 52 (2006), 365–377, 10.1007/s00248-006-9017-0.
Mager, D.M., Carbohydrates in cyanobacterial soil crusts as a source of carbon in the southwest Kalahari. Botswana. Soil Biol. Biochem. 42 (2010), 313–318, 10.1016/j.soilbio.2009.11.009.
Malam Issa, O., Défarge, C., Le Bissonnais, Y., Marin, B., Duval, O., Bruand, A., D'Acqui, L.P., Nordenberg, S., Annerman, M., Effects of the inoculation of cyanobacteria on the microstructure and the structural stability of a tropical soil. Plant Soil 290 (2007), 209–219, 10.1007/s11104-006-9153-9.
Mazor, G., Kidron, G.J., Vonshak, A., Abeliovich, A., The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts. FEMS Microbiol. Ecol. 21 (1996), 121–130, 10.1016/0168-6496(96)00050-5.
Mingorance, M.D., Barahona, E., Fernández-Gálvez, J., Guidelines for improving organic carbon recovery by the wet oxidation method. Chemosphere 68 (2007), 409–413, 10.1016/j.chemosphere.2007.01.021.
Mugnai, G., Rossi, F., Felde, V.J.M.N.L., Colesie, C., Büdel, B., Peth, S., Kaplan, A., De Philippis, R., Development of the polysaccharidic matrix in biocrusts induced by a cyanobacterium inoculated in sand microcosms. Biol. Fertil. Soils 54 (2018), 27–40, 10.1007/s00374-017-1234-9.
Mugnai, G., Rossi, F., Chamizo, S., Adessi, A., De Philippis, R., The role of grain size and inoculum amount on biocrust formation by Leptolyngbya ohadii. Catena, 184, 2020, 10.1016/j.catena.2019.104248.
Muñoz-Martín, M.Á., Becerra-Absalón, I., Perona, E., Fernández-Valbuena, L., Garcia-Pichel, F., Mateo, P., Cyanobacterial biocrust diversity in Mediterranean ecosystems along a latitudinal and climatic gradient. New Phytol. 221 (2019), 123–141, 10.1111/nph.15355.
Muñoz-Rojas, M., Román, J.R., Roncero-Ramos, B., Erickson, T.E., Merritt, D.J., Aguila-Carricondo, P., Cantón, Y., Cyanobacteria inoculation enhances carbon sequestration in soil substrates used in dryland restoration. Sci. Total Environ. 636 (2018), 1149–1154, 10.1016/j.scitotenv.2018.04.265.
Potts, M., Mechanisms of desiccation tolerance in cyanobacteria. Eur. J. Phycol. 34 (1999), 319–328, 10.1080/09670269910001736382.
Rajeev, L., Da Rocha, U.N., Klitgord, N., Luning, E.G., Fortney, J., Axen, S.D., Shih, P.M., Bouskill, N.J., Bowen, B.P., Kerfeld, C.A., Garcia-Pichel, F., Brodie, E.L., Northen, T.R., Mukhopadhyay, A., Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust. ISME J. 7 (2013), 2178–2191, 10.1038/ismej.2013.83.
Reed, S.C., Coe, K.K., Sparks, J.P., Housman, D.C., Zelikova, T.J., Belnap, J., Changes to dryland rainfall result in rapid moss mortality and altered soil fertility. Nat. Clim. Chang. 2 (2012), 752–755, 10.1038/nclimate1596.
Rippka, R., Deruelles, J., Waterbury, J.B., Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111 (1979), 1–61.
Román, J.R., Roncero-Ramos, B., Chamizo, S., Rodríguez-Caballero, E., Cantón, Y., Restoring soil functions by means of cyanobacteria inoculation: Importance of soil conditions and species selection. L. Degrad. Dev. 29 (2018), 3184–3193, 10.1002/ldr.3064.
Román, J.R., Rodríguez-Caballero, E., Rodríguez-Lozano, B., Roncero-Ramos, B., Chamizo, S., Águila-Carricondo, P., Cantón, Y., Spectral response analysis: An indirect and non-destructive methodology for the chlorophyll quantification of biocrusts. Remote Sens., 11, 2019, 10.3390/rs11111350.
Roncero-Ramos, B., Muñoz-Martín, M.A., Cantón, Y., Chamizo, S., Rodríguez-Caballero, E., Mateo, P., Land degradation effects on composition of pioneering soil communities: An alternative successional sequence for dryland cyanobacterial biocrusts. Soil Biol. Biochem., 146, 2020, 10.1016/j.soilbio.2020.107824.
Roncero-Ramos, B., Muñoz-Martín, M.Á., Chamizo, S., Fernández-Valbuena, L., Mendoza, D., Perona, E., Cantón, Y., Mateo, P., Polyphasic evaluation of key cyanobacteria in biocrusts from the most arid region in Europe. PeerJ, 7, 2019, e6169, 10.7717/peerj.6169.
Roncero-Ramos, B., Román, J.R., Rodríguez-Caballero, E., Chamizo, S., Águila-Carricondo, P., Mateo, P., Cantón, Y., Assessing the influence of soil abiotic and biotic factors on Nostoc commune inoculation success. Plant Soil 444 (2019), 57–70, 10.1007/s11104-019-04239-y.
Rossi, F., Li, H., Liu, Y., De Philippis, R., Cyanobacterial inoculation (cyanobacterisation): Perspectives for the development of a standardized multifunctional technology for soil fertilization and desertification reversal. Earth-Science Rev, 2017, 10.1016/j.earscirev.2017.05.006.
Rozenstein, O., Zaady, E., Katra, I., Karnieli, A., Adamowski, J., Yizhaq, H., The effect of sand grain size on the development of cyanobacterial biocrusts. Aeolian Res. 15 (2014), 217–226, 10.1016/j.aeolia.2014.08.003.
Sand-Jensen, K., Jespersen, T.S., Tolerance of the widespread cyanobacterium Nostoc commune to extreme temperature variations (-269 to 105°C), pH and salt stress. Oecologia 169 (2012), 331–339, 10.1007/s00442-011-2200-0.
Satoh, K., Hirai, M., Nishio, J., Yamaji, T., Kashino, Y., Koike, H., Recovery of photosynthetic systems during rewetting is quite rapid in a terrestrial cyanobacterium, nostoc commune. Plant Cell Physiol. 43 (2002), 170–176, 10.1093/pcp/pcf020.
Savitzky, A., Golay, M.J.E., Smoothing and Differentiation of Data by Simplified Least Squares Procedures. Anal. Chem. 36 (1964), 1627–1639, 10.1021/ac60214a047.
Six, J., Bossuyt, H., Degryze, S., Denef, K., A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res, 2004, 10.1016/j.still.2004.03.008.
Sorochkina, K., Velasco Ayuso, S., Garcia-Pichel, F., Establishing rates of lateral expansion of cyanobacterial biological soil crusts for optimal restoration. Plant Soil, 2018, 10.1007/s11104-018-3695-5.
Stark, L.R., Brinda, J.C., Nicholas Mcletchie, D., Oliver, M.J., Extended periods of hydration do not elicit dehardening to desiccation tolerance in regeneration trials of the moss syntrichia caninervis. Int. J. Plant Sci. 173 (2012), 333–343, 10.1086/663970.
Tamaru, Y., Takani, Y., Yoshida, T., Sakamoto, T., Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Appl. Environ. Microbiol. 71 (2005), 7327–7333, 10.1128/AEM.71.11.7327-7333.2005.
Wang, W., Liu, Y., Li, D., Hu, C., Rao, B., Feasibility of cyanobacterial inoculation for biological soil crusts formation in desert area. Soil Biol. Biochem. 41 (2009), 926–929, 10.1016/j.soilbio.2008.07.001.
Weber, B., Bowker, M., Zhang, Y., Belnap, J., Natural Recovery of Biological Soil Crusts After Disturbance. Weber, B., Büdel, B., Belnap, J., (eds.) Biological Soil Crust: An Organizing Principle in Drylands, 2016, Ecological Studies, Springer, Berlin, 479–498.
Wu, Y., Rao, B., Wu, P., Liu, Y., Li, G., Li, D., Development of artificially induced biological soil crusts in fields and their effects on top soil. Plant Soil 370 (2013), 115–124, 10.1007/s11104-013-1611-6.
Xie, Z., Liu, Y., Hu, C., Chen, L., Li, D., Relationships between the biomass of algal crusts in fields and their compressive strength. Soil Biol. Biochem. 39 (2007), 567–572, 10.1016/j.soilbio.2006.09.004.
Zhao, H.L., Guo, Y.R., Zhou, R.L., Drake, S., The effects of plantation development on biological soil crust and topsoil properties in a desert in northern China. Geoderma 160 (2011), 367–372, 10.1016/j.geoderma.2010.10.005.
Zulpa de Caire, G., Storni de Cano, M., Zaccaro de Mulé, M.C., Palma, R.M., Colombo, K., Exopolysaccharide of Nostoc muscorum (Cyanobacteria) in the aggregation of soil particles. J. Appl. Phycol., 1997, 10.1023/A:1007994425799.