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The formation of biocrust and improvement of soil properties by the exopolysaccharide-producing cyanobacterium: a biogeotechnological study

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Abstract

Biocrusts are specialized and complex microbial products playing important roles in the soil biogeochemistry and dune stabilization of dryland ecosystem all over the world. The objectives were to (1) isolate and identify the most predominant EPS-producing cyanobacterium from a dry land of Iran (Segzi plain) and (2) study cyanobacterial inoculation affecting the formation of biocrust and improvement of soil chemico- and biological properties. The most predominant EPS-producing isolated cyanobacterium was identified as Microcoleus vaginatus ATHK43 (MW433686 NCBI accession number) and utilized as soil inoculants. Surface and sub-surface soil chemical (pH, EC, CEC, cations content) and biological properties (chlorophyll a, organic carbon, total N, EPS contents, and invertase and dehydrogenase activities) were investigated during the formation and development of biocrust. The biocrust significantly (P < 0.01) increased EC, total N, K, Ca, Mg, CEC, EPS amount, chlorophyll a, and organic carbon (C) contents of the surface soil. A high and significant correlation was found between chlorophyll content with organic C (R2 = 0.98), N (R2 = 0.98), and EPS amount (R2 = 0.96) of biocrust in the surface soil. The activities of dehydrogenase and invertase enzymes were also significantly increased (P < 0.01) after 90 days of inoculation. In conclusion, such alterations in the soil chemico- and biological properties play an important role in nutrient cycling and improvement of soil structure, fertility, and stability. So, the formation of biocrust by bacterial inoculation can be used as a cost-effective and sustainable biogeotechnological method for re-establishment and enhancement of soil properties in dry and semi-dry lands.

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References

  1. Abed RM, 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

    Article  Google Scholar 

  2. Baligh, P., Honarjoo, N., Jalalian, A., Totonchi, A., 2021. Soil chemical and microbial properties affected by land use type in a unique ecosystem (Fars, Iran). Biomass Conversion and Biorefinery in press

  3. Belnap J, Weber B (2013) Biological soil crusts as an integral component of desert environments. Ecol Process 2:11

    Article  Google Scholar 

  4. Bremner JM (1996) Nitrogen total. In: Sparks DL (ed) Methods of soil analysis part 3: chemical methods, SSSA Book Series 5, Soil Science Society of America, Madison, Wisconsin, p 1085–1122

  5. Caesar J, Tamm A, Ruckteschler N, Leifke AL, Weber B (2018) Revisiting chlorophyll extraction methods in biological soil crusts–methodology for determination of chlorophyll a and chlorophyll a+ b as compared to previous methods. Biogeosciences 15:1415–1424

    Article  Google Scholar 

  6. Chamizo S, Adessi A, Mugnai G, Simiani A, De Philippis R (2019) Soil type and cyanobacteria species influence the macromolecular and chemical characteristics of the polysaccharidic matrix in induced biocrusts. Microb Ecol 78:482–493

    Article  Google Scholar 

  7. Chauvat, F., Cassier-Chauvat, C., 2021. Genomics of cyanobacteria: new insights and lessons for shaping our future-A follow-up of volume 65: genomics of cyanobacteria. Advances in Botanical Research, Volume 100 1st EditionPast, Current and Future Topics, pp.213 – 235 https://doi.org/10.1016/bs.abr.2021.01.007ff. ffhal-03368156f

  8. Cheng C, Gao M, Zhang Y, Long M, Wu Y, Li X (2021) Effects of disturbance to moss biocrusts on soil nutrients, enzyme activities, and microbial communities in degraded karst landscapes in southwest China. Soil Biology and Biochemistry 152:108065

    Article  Google Scholar 

  9. Chu J, Ivanov V, He J, Maeimi M, Wu S (2015) Use of biogeotechnologies for soil improvement. In Ground improvement case histories. Butterworth-Heinemann, Elsevier, Holland, p 571–589

  10. Couradeau E, Karaoz U, Lim HC, Da Rocha UN, Northen T, Brodie E, Garcia-Pichel F (2016) Bacteria increase arid-land soil surface temperature through the production of sunscreens. Nat Commun 7:1–7

    Article  Google Scholar 

  11. Delattre C, Pierre G, Laroche C, Michaud P (2016) Production, extraction and characterization of microalgal and cyanobacterial exopolysaccharides. Biotechnol Adv 34:1159–1179

    Article  Google Scholar 

  12. Dubois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  Google Scholar 

  13. Fan B, McHugh AD, Guo S, Ma Q, Zhang J, Zhang X, Zhang W, Du J, Yu Q, Zhao C (2018) Factors influencing the natural regeneration of the pioneering shrub Calligonummongolicum in sand dune stabilization plantations in arid deserts of northwest China. Ecol Evol 8:2975–2984

    Article  Google Scholar 

  14. 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

    Article  Google Scholar 

  15. Gholamhosseinian A, Sepehr A, Emadodin I (2020) The effects of biocrusts on soil parameters in a semi-arid pediment at north-eastern Iran. Revista de Geomorfologie 22:5–19

    Article  Google Scholar 

  16. Gholamhosseinian A, Sepehr A, Lajayer BA, Delangiz N, Astatkie T (2021) Biological soil crusts to keep soil alive, rehabilitate degraded soil, and develop soil habitats. In Microbial Polymers. Springer, Singapore, pp 289–309

    Google Scholar 

  17. Guo Y, Zhao H, Zuo X, Drake S, Zhao X (2008) Biological soil crust development and its topsoil properties in the process of dune stabilization, Inner Mongolia, China. Environ Geol 54:653–662

    Article  Google Scholar 

  18. Kim KH, Jahan SA, Kabir E (2013) A review on human health perspective of air pollution with respect to allergies and asthma. Environ Int 59:41–52

    Article  Google Scholar 

  19. Lanyon LE, Heald WR (1983) Magnesium, calcium, strontium, and barium. Methods of Soil Analysis: Part 2 Chemical and Microbiological Properties 9:247–262

    Google Scholar 

  20. Lebrun JD, Trinsoutrot-Gattin I, Vinceslas-Akpa M, Bailleul C, Brault A, Mougin C, Laval K (2012) Assessing impacts of copper on soil enzyme activities in regard to their natural spatiotemporal variation under long-term different land uses. Soil Biol Biochem 49:150–156

    Article  Google Scholar 

  21. Liu Y, Yang H, Li X, Xing Z (2014) Effects of biological soil crusts on soil enzyme activities in revegetated areas of the Tengger Desert, China. Appl Soil Ecol 80:6–14

    Article  Google Scholar 

  22. Mager DM (2010) Carbohydrates in cyanobacterial soil crusts as a source of carbon in the southwest Kalahari, Botswana. Soil Biol Biochem 42:313–318

    Article  Google Scholar 

  23. Mager DM, Thomas AD (2011) Extracellular polysaccharides from cyanobacterial soil crusts: a review of their role in dryland soil processes. J Arid Environ 75:91–97

    Article  Google Scholar 

  24. Maier S, Tamm A, Wu D, Caesar J, Grube M, Weber B (2018) Photoautotrophic organisms control microbial abundance, diversity, and physiology in different types of biological soil crusts. ISME J 12:1032–1046

    Article  Google Scholar 

  25. Mancuso Nichols CA, Garon S, Bowman JP, Raguénès G, Guezennec J (2004) Production of exopolysaccharides by Antarctic marine bacterial isolates. J Appl Microbiol 96:1057–1066

    Article  Google Scholar 

  26. Mekonnen E, Kebede A, Tafesse T, Tafesse M (2020) Application of microbial bioenzymes in soil stabilization. International Journal of Microbiology 2020:1725482

    Article  Google Scholar 

  27. Mehda S, Muñoz-Martín M, Oustani M, Hamdi-Aïssa B, Perona E, Mateo P (2021) Microenvironmental conditions drive the differential cyanobacterial community composition of biocrusts from the Sahara Desert. Microorganisms 9:487

    Article  Google Scholar 

  28. Miralles I, Domingo F, Cantón Y, Trasar-Cepeda C, Leirós MC, Gil-Sotres F (2012) Hydrolase enzyme activities in a successional gradient of biological soil crusts in arid and semi-arid zones. Soil Biol Biochem 53:124–132

    Article  Google Scholar 

  29. Miralles I, de Guevara ML, Chamizo S, Rodríguez-Caballero E, Ortega R, van Wesemael B, Cantón Y (2018) Soil CO2 exchange controlled by the interaction of biocrust successional stage and environmental variables in two semiarid ecosystems. Soil Biol Biochem 124:11–23

    Article  Google Scholar 

  30. Miralles I, Lázaro R, Sánchez-Marañón M, Soriano M, Ortega R (2020) Biocrust cover and successional stages influence soil bacterial composition and diversity in semiarid ecosystems. Science of the Total Environment 709:134654

    Article  Google Scholar 

  31. Miralles I, Trasar-Cepeda C, Soria R, Ortega R, Lucas-Borja ME (2021) Environmental and ecological factors influencing soil functionality of biologically crusted soils by different lichen species in drylands. Sci Total Environ 794:48491

    Article  Google Scholar 

  32. Miransari M, Bahrami HA, Rejali F, Malakouti MJ (2008) Using arbuscular mycorrhiza to alleviate the stress of soil compaction on wheat (Triticumaestivum L.) growth. Soil Biol Biochem 40:1197–1206

    Article  Google Scholar 

  33. MoshabakiIsfahani FM, Tahmourespour A, Hoodaji M, Ataabadi M, Mohammadi A (2018) Characterizing the new bacterial isolates of high yielding exopolysaccharides under hypersaline conditions. J Clean Prod 185:922–928

    Article  Google Scholar 

  34. Muñoz-Rojas M, Román JR, Roncero-Ramos B, Erickson TE, Merritt DJ, Aguila-Carricondo P, Cantón Y (2018) Cyanobacteria inoculation enhances carbon sequestration in soil substrates used in dryland restoration. Sci Total Environ 636:1149–1154

    Article  Google Scholar 

  35. Page A, Miller R, Keeney D (1982) Methods of soil analysis. Part 2. American Society of Agronomy Soil Science Society of America, Madison, WI, USA

    Google Scholar 

  36. Park CH, Li XR, Zhao Y, Jia RL, Hur JS (2017) Rapid development of cyanobacterial crust in the field for combating desertification. PLoS One 12:e0179903

    Article  Google Scholar 

  37. Rengifo MC, Arana C (2017) Disturbances of biological soil crust by fossorial birds increase plant diversity in a Peruvian desert. Biogeosciences Discussions 2017:376

    Google Scholar 

  38. Rossi F, De Philippis R (2015) Role of cyanobacterial exopolysaccharides in phototrophic biofilms and in complex microbial mats. Life 5:1218–1238

    Article  Google Scholar 

  39. Rossi F, Mugnai G, De Philippis R (2018) Complex role of the polymeric matrix in biological soil crusts. Plant Soil 429:19–34

    Article  Google Scholar 

  40. Samolov E, Baumann K, Büdel B, Jung P, Leinweber P, Mikhailyuk T, Karsten U, Glaser K (2020) Biodiversity of algae and cyanobacteria in biological soil crusts collected along a climatic gradient in Chile using an integrative approach. Microorganisms 8:1047

    Article  Google Scholar 

  41. Sepehr A, Hassanzadeh M, Rodriguez-Caballero E (2019) The protective role of cyanobacteria on soil stability in two Aridisols in northeastern Iran. Geoderma Regional 16:e00201

    Article  Google Scholar 

  42. Singh RP, Yadav P, Kujur R, Pandey KD, Gupta RK (2022) Cyanobacteria and salinity stress tolerance. In: Cyanobacterial lifestyle and its applications in biotechnology. Academic Press, Elsevier, Holland, p 253–280

  43. Smith HD, Baqué M, Duncan AG, Lloyd CR, McKay CP, Billi D (2014) Comparative analysis of cyanobacteria inhabiting rocks with different light transmittance in the Mojave Desert: a Mars terrestrial analogue. Int J Astrobiol 13:271–277

    Article  Google Scholar 

  44. Swenson TL, Karaoz U, Swenson JM, Bowen BP, Northen TR (2018) Linking soil biology and chemistry in biological soil crust using isolate exometabolomics. Nat Commun 9:1–10

    Article  Google Scholar 

  45. Swenson TL, Couradeau E, Bowen BP, De Philippis R, Rossi F, Mugnai G, Northen TR (2018) A novel method to evaluate nutrient retention by biological soil crust exopolymeric matrix. Plant Soil 429:53–64

    Article  Google Scholar 

  46. Tahmourespour A, Ahmadi A, Fesharaki M (2020) The anti-tumor activity of exopolysaccharides from Pseudomonas strains against HT-29 colorectal cancer cell line. Int J Biol Macromol 149:1072–1076

    Article  Google Scholar 

  47. UNEP, Wmo, UNCCD, (2016) Global assessment of sand and dust storms. ISBN: 978–92–807–3551–2. United Nations Environment Programme, Nairobi

    Google Scholar 

  48. 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

    Article  Google Scholar 

  49. Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38

    Article  Google Scholar 

  50. Xu JS, Xu HH, Xiao H, Tong L, Snape CE, Wang CJ, He J (2016) Aerosol composition and sources during high and low pollution periods in Ningbo, China. Atmos Res 178:559–569

    Article  Google Scholar 

  51. Xu HF, Raanan H, Dai GZ, Oren N, Berkowicz S, Murik O, Kaplan A, Qiu BS (2021) Reading and surviving the harsh conditions in desert biological soil crust: the cyanobacterial viewpoint. FEMS Microbiology Reviews 45:fuab036

    Article  Google Scholar 

  52. Yaghmaei L, Soltani S, Khodagholi M (2009) Bioclimatic classification of Isfahan province using multivariate statistical methods. International Journal of Climatology: A Journal of the Royal Meteorological Society 29:1850–1861

    Article  Google Scholar 

  53. Zhang W, Zhang G, Liu G, Dong Z, Chen T, Zhang M, Dyson PJ, An L (2012) Bacterial diversity and distribution in the southeast edge of the Tengger Desert and their correlation with soil enzyme activities. J Environ Sci 24:2004–2011

    Article  Google Scholar 

  54. Zheng Y, Xu M, Zhao J, Bei S, Hao L (2011) Effects of inoculated Microcoleusvaginatus on the structure and function of biological soil crusts of desert. Biol Fertil Soils 47:473–480

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank very much the international publisher, AbtinBerkeh Scientific Ltd. Company (https://AbtinBerkeh.com), Isfahan, Iran, for editing the manuscript, and revising it according to the journal format.

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Authors and Affiliations

  1. Department of Soil Sciences, Islamic Azad University, Isfahan (Khorasgan) Branch, Isfahan, Iran

    Amir Karimi & Mehran Hoodaji

  2. Department of Basic Medical Sciences, Islamic Azad University, Isfahan (Khorasgan) Branch, Isfahan, Iran

    Arezoo Tahmourespour

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  1. Amir Karimi
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  2. Arezoo Tahmourespour
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  3. Mehran Hoodaji
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AK conducted the experiments and collected and analyzed data, AT supervised the research and wrote the first draft, and MH co-supervised the research.

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Correspondence to Arezoo Tahmourespour.

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Karimi, A., Tahmourespour, A. & Hoodaji, M. The formation of biocrust and improvement of soil properties by the exopolysaccharide-producing cyanobacterium: a biogeotechnological study. Biomass Conv. Bioref. 13, 15489–15499 (2023). https://doi.org/10.1007/s13399-022-02336-0

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