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Effects of Biological Soil Crusts on Enzyme Activities and Microbial Community in Soils of an Arid Ecosystem

  • Soil Microbiology
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Abstract

Arid ecosystems constitute 41% of land’s surface and play an important role in global carbon cycle. In particular, biological soil crusts (BSC) are known to be a hotspot of carbon fixation as well as mineralization in arid ecosystems. However, little information is available on carbon decomposition and microbes in BSC and key controlling variables for microbial activities in arid ecosystems. The current study, carried out in South Mediterranean arid ecosystem, aimed to evaluate the effects of intact and removed cyanobacteria/lichen crusts on soil properties, soil enzyme activities, and microbial abundances (bacteria and fungi). We compared five different treatments (bare soil, soil with intact cyanobacteria, soil with cyanobacteria removed, soil with intact lichens, and soil with lichens removed) in four different soil layers (0–5, 5–10, 10–15, and 15–20 cm). Regardless of soil treatments, activities of hydrolases and water content increased with increasing soil depth. The presence of lichens increased significantly hydrolase activities, which appeared to be associated with greater organic matter, nitrogen, and water contents. However, phenol oxidase was mainly controlled by pH and oxygen availability. Neither fungal nor bacterial abundance exhibited a significant correlation with enzyme activities suggesting that soil enzyme activities are mainly controlled by edaphic and environmental conditions rather than source microbes. Interestingly, the presence of lichens reduced the abundance of bacteria of which mechanism is still to be investigated.

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References

  1. Yirdaw E, Tigabu M, Monge A (2017) Rehabilitation of degraded dryland ecosystems—review. Silva Fenn. 51. https://doi.org/10.14214/sf.1673

  2. Valentin C, d’Herbès JM, Poesen J (1999) Soil and water components of banded vegetation patterns. Catena 37:1–24

    Google Scholar 

  3. Belnap J, Kaltenecker JH, Rosentreter R, Williams J, Leonard S, Eldridge D (2001) Biological soil crusts: ecology and management. Technical Reference, 1730–1732

  4. Belnap J (1995) Surface disturbances: their role in accelerating desertification. Environ. Monit. Assess. 37:39–57

    CAS  PubMed  Google Scholar 

  5. Liu YM, Li XR, Jia RL, Huang L, Zhou YY, Gao YH (2011) Effects of biological soil crusts on soil nematode communities following dune stabilization in the Tengger Desert, northern China. Appl. Soil Ecol. 49:118–124

    Google Scholar 

  6. Li XR, Wang XP, Li T, Zhang JG (2002) Microbiotic crust and its effect on vegetation and habitat on artificially stabilized desert dunes in Tengger Desert, north China. Biol. Fertil. Soils 35:147–154

    Google Scholar 

  7. Lan SB, Wu L, Zhang DL, Hu CX (2013) Assessing level of development and successional stages in biological soil crusts with biological indicators. Microb. Ecol. 66:394–403

    CAS  PubMed  Google Scholar 

  8. Lange OL, Kidron EL, Büdel B, Meyer A, Kilian E, Abeliovich A (1992) Taxonomic composition and photosynthetic characteristics of the ‘biological soil crusts’ covering sand dunes in the western Negev Desert. Funct. Ecol. 6:519–527

    Google Scholar 

  9. Lan SB, Wu L, Zhang DL, Hu CX (2012) Successional stages of biological soil crusts and their microstructure variability in Shapotou region (China). Environ. Earth Sci. 65(1):77–88

    Google Scholar 

  10. Lan SB, Zhang QY, Wu L, Liu YD, Zhang DL, Hu CX (2014) Artificially accelerating the reversal of desertification: cyanobacterial inoculation facilitates the succession of vegetation communities. Environ. Sci. Technol. 48:307–315

    CAS  PubMed  Google Scholar 

  11. Guo YR, Zhao HL, Zuo XA, Drake S, Zhao XY (2008) Biological soil crust development and its topsoil properties in the process of dune stabilization, Inner Mongolia, China. Environ. Geol. 54:653–662

    CAS  Google Scholar 

  12. Seitz S, Nebel M, Goebes P, Käppeler K, Schmidt K, Shi X, Song Z, Webber CL, Weber B, Scholten T (2017) Bryophyte-dominated biological soil crusts mitigate soil erosion in an early successional Chinese subtropical forest. Biogeosciences 14(24):5775–5788

    Google Scholar 

  13. Belnap J, Phillips SL, Troxler T (2006) Soil lichen and moss cover and species richness can be highly dynamic: the effects of invasion by the annual exotic grass Bromus tectorum, precipitation, and temperature on biological soil crusts in SE Utah. Appl. Soil Ecol. 32:63–76

    Google Scholar 

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

    Google Scholar 

  15. Ghiloufi W, Büdel B, Chaieb M (2017) Effects of biological soil crusts on a Mediterranean perennial grass (Stipa tenacissima L.). Plant Biosyst. 151:158–167

    Google Scholar 

  16. Deines L, Rosentreter R, Eldridge DJ, Serpe MD (2007) Germination and seedling establishment of two annual grasses on lichen-dominated biological soil crusts. Plant Soil 295:23–35

    CAS  Google Scholar 

  17. Zhao HL, Guo YR, Zhou RL, Drake S (2011) The effects of plantation development on biological soil crust and topsoil properties in a desert in northern China. Geoderma 160:367–372

    CAS  Google Scholar 

  18. Ghiloufi W, Chaieb M (2016) Vascular plant diversity associated with biological soil crusts: insights from Mediterranean arid ecosystem. Afr. J. Ecol. 55:252–255

    Google Scholar 

  19. Schowalter TD (2016) Decomposition and pedogenesis. In: Insect ecology (fourth edition) DOI: 10.1016/B978-0-12-803033-2.00014-5

  20. Wohlfahrt G, Fenstermaker LF, Arnone III JA (2008) Large annual net ecosystem CO2 uptake of a Mojave Desert ecosystem. Glob. Change Biol. 14(7):1475–1487

    Google Scholar 

  21. Xie J, Li Y, Zhai C, Li C, Lan Z (2009) CO2 absorption by alkaline soils and its implication to the global carbon cycle. Environ. Geol. 56:953–961

    CAS  Google Scholar 

  22. Schlesinger WH (2017) An evaluation of abiotic carbon sinks in deserts. Glob. Change Biol. 23:25–27

    Google Scholar 

  23. Dick RP, Sandor JA, Eash NS (1994) Soil enzyme activities after 1500 years of terrace agriculture in the Colca Valley, Peru. Agric. Ecosyst. Environ. 50:123–131

    CAS  Google Scholar 

  24. Karaca A, Cema CC, Turgay OC, Kizilkaya R (2011) Soil enzymes as indicator of soil quality. In: Shukla S, Varma A (eds) Soil enzymology. Springer-Verlag, Berlin, pp 119–148

    Google Scholar 

  25. Tate RL (1995) Soil microbiology. John Wiley, New York

    Google Scholar 

  26. Zhang W, Zhang GS, Liu GX, Dong ZB, Chen T, Zhang MX, Dyson PJ, An LZ (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

    CAS  Google Scholar 

  27. Castillo-Monroy AP, Bowker MA, Maestre FT, Rodríguez-Echeverría S, Martinez I, Barraza-Zepeda CE, Escolar C (2011) Relationships between biological soil crusts, bacterial diversity and abundance, and ecosystem functioning: insights from a semi-arid Mediterranean environment. J. Veg. Sci. 22:165–174

    Google Scholar 

  28. Bates ST, Nash TH, Sweat KG, Garcia-pichel F (2010) Fungal communities of lichen-dominated biological soil crusts: diversity, relative microbial biomass, and their relationship to disturbance and crust cover. J. Arid Environ. 74:1192–1199

    Google Scholar 

  29. Sardans J, Peñuelas J (2010) Soil enzyme activity in a Mediterranean forest after six years of drought. Soil Sci. Soc. Am. J. 74:838–851

    CAS  Google Scholar 

  30. Ghiloufi W, Quero JL, García-Gómez M, Chaieb M (2017) Potential impacts of aridity on structural and functional status of a southern Mediterranean Stipa tenacissima steppe. South Afr. J. Bot. 103:170–180

    Google Scholar 

  31. Zhang YL, Chena LJ, Chenb XH, Tanb ML, Duan ZH, Wua ZJ, Li XJ, Fanc XH (2015) Response of soil enzyme activity to long-term restoration of desertified land. Catena 133:64–70

    CAS  Google Scholar 

  32. Jia XH, Li XR, Li YS (2007) Soil organic carbon and nitrogen dynamics during the re-vegetation process in the arid desert region. Chin. J. Plant Ecol. 31:66–74. (In Chinese with English Abstract)

    Google Scholar 

  33. Boerner REJ, Decker KLM, Sutherland EK (2000) Prescribed burning effects on soil enzyme activity in a southern Ohio hardwood forest: a landscape-scale analysis. Soil Biol. Biochem. 32:899–908

    CAS  Google Scholar 

  34. Tscherko D, Rustemeier J, Richter A, Wanek W, Kandeler E (2003) Functional diversity of the soil microflora in the primary succession across two glacier forelands in the Central Alps. Eur. J. Soil Sci. 54:685–696

    Google Scholar 

  35. Yuan B, Yue D (2012) Soil microbial and enzymatic activities across a chronosequence of Chinese pine plantation development on the Loess Plateau of China. Pedosphere 22:1–12

    CAS  Google Scholar 

  36. 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

    Google Scholar 

  37. 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. 57:229–247

    PubMed  Google Scholar 

  38. Chiquoine LP, Abella SR, Bowker MA (2016) Rapidly restoring biological soil crusts and ecosystem functions in a severely disturbed desert ecosystem. Ecol. Appl. 26:1260–1272

    PubMed  Google Scholar 

  39. Chamizo S, Rodríguez-Caballero E, Cantón Y, Asensio C, Domingo F (2015) Penetration resistance of biological soil crusts and its dynamics after crust removal: relationships with runoff and soil detachment. Catena 126:164–172

    Google Scholar 

  40. Cortina J, Martín N, Maestre FT, Bautista S (2010) Disturbance of the biological soil crusts and performance of Stipa tenacissima in a semi-arid Mediterranean steppe. Plant Soil 334:311–322

    CAS  Google Scholar 

  41. Ghiloufi W, Chaieb M (2014) Effect of biological soil crusts on soil chemical properties: a study from Tunisian arid ecosystem. IJAAR 4:22–32

    Google Scholar 

  42. Bu CF, Wu SF, Zhang KK, Yang YS, Gao GX (2013) Biological soil crusts: an eco-adaptive biological conservative mechanism and implications for ecological restoration. Plant Biosyst 149:364–373

    Google Scholar 

  43. Maestre FT, Martín N, Díez B, López-Poma R, Santos F, Luque I, Cortina J (2006) Watering, fertilization, and slurry inoculation promote recovery of biological crust function in degraded soils. Microb. Ecol. 52:365–377

    PubMed  Google Scholar 

  44. Belnap J (1993) Recovery rates of cryptobiotic crusts: inoculant use and assessment methods. Gt. Basin Nat. 53:89–95

    Google Scholar 

  45. Bu CF, Wu S, Yang YS, Zheng M (2014) Identification of factors influencing the restoration of cyanobacteria-dominated biological soil crusts. PLoS One 9(3):e90049

    PubMed  PubMed Central  Google Scholar 

  46. Acosta-Martínez V, Cruz L, Sotomayor-Ramίrez D, Pérez-Alegrίa L (2007) Enzyme activities as affected by soil properties and land use in a tropical watershed. Appl. Soil Ecol. 35:35–45

    Google Scholar 

  47. Hill TCJ, DeMott PJ, Tobo Y, Fröhlich-Nowoisky J, Moffett BF, Franc GD, Kreidenweis SM (2016) Sources of organic ice nucleating particles in soils. Atmos. Chem. Phys. 16(11):7195–7211

    CAS  Google Scholar 

  48. Schulte EE, Hopkins BG (1996) Estimation of soil organic matter by weight loss-on-ignition. p. 21–31. In F.R. Magdoff et al. (ed.) Soil organic matter: analysis and interpretation. SSSA Spec. Publ. 46. SSSA, Madison, WI

  49. Baldrian P, Valaškova V (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol. Rev. 32:501–521

    CAS  PubMed  Google Scholar 

  50. Kilcawley KN, Wilkinson MG, Fox PF (2002) Determination of key enzyme activities in commercial peptidase and lipase preparations from microbial or animal sources. Enzym. Microb. Technol. 31:310–320

    CAS  Google Scholar 

  51. Seidl V (2008) Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions. Fungal Biol. Rev. 22:36–42

    Google Scholar 

  52. Schneider K, Turrion MB, Grierson PF, Gallardo JF (2001) Phosphatase activity, microbial phosphorus, and fine root growth in forest soils in the Sierra de Gata, western central Spain. Biol. Fertil. Soils 34:151–155

    CAS  Google Scholar 

  53. Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol. Biochem. 42:391–404

    CAS  Google Scholar 

  54. Brockett BFT, Prescott CE, Grayston SJ (2012) Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol. Biochem. 44:9–20

    CAS  Google Scholar 

  55. Sinsabaugh RL, Saiya-Cork K, Long T, Osgood MP, Neher DA, Zakd DR, Norby RJ (2003) Soil microbial activity in a Liquidambar plantation unresponsive to CO2-driven increases in primary production. Appl. Soil Ecol. 24:263–271

    Google Scholar 

  56. Belnap J, Prasse R, Harper KT (2001) Influence of biological soil crusts on soil environments and vascular plants. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer-Verlag, Berlin, pp 281–300

    Google Scholar 

  57. Rossi F, Potrafk RM, Garcia Pichel F, De Philippis R (2012) The role of the exopolysaccharides in enhancing hydraulic conductivity of biological soil crusts. Soil Biol. Biochem. 46:33–40

    CAS  Google Scholar 

  58. Chamizo S, Cantón Y, Rodríguez-Caballero E, Domingo F, Escudero A (2012) Runoff at contrasting scales in a semiarid ecosystem: a complex balance between biological soil crust features and rainfall characteristics. J. Hydrol. 452–453:130–138

    Google Scholar 

  59. Gao S, Ye X, Chu Y, Dong M (2010) Effects of biological soil crusts on profile distribution of soil water, organic carbon and total nitrogen in Mu Us Sandland, China. J. Plant Ecol. 3:279–284

    Google Scholar 

  60. Qiu Y, Fu B, Wang J, Chen L (2001) Spatial variability of soil moisture content and its relation to environmental indices in a semi-arid gully catchment of the Loess Plateau, China. J. Arid Environ. 49:723–750

    Google Scholar 

  61. Rovira P, Vallejo VR (2002) Mineralization of carbon and nitrogen from plant debris, as affected by debris size and depth of burial. Soil Biol. Biochem. 34:327–339

    CAS  Google Scholar 

  62. Roth CH (1985) Infiltrabilität von Latosolo-Roxo-Böden in Nordparaná, Brasilien, in Feldversuchen zur Erosionskontrolle mit verschiedenen Bodenbearbeitungs-systemen und Rotationen. Göttinger Bodenkundliche Berichte 83:1–104 [Infiltrability of Oxisols in Northern Paraná, Brazil, in erosion control plots with different tillage systems and crop rotations; in German]

    Google Scholar 

  63. Franzluebbers AJ (2000) Water infiltration and soil structure related to organic matter and its stratification with depth. Soil Tillage Res. 66:197–205

    Google Scholar 

  64. Housman D, Powers H, Collins A, Belnap J (2006) Carbon and nitrogen fixation differ between successional stages of biological soil crusts in the Colorado Plateau and Chuhuahuan Desert. J. Arid Environ. 66:620–634

    Google Scholar 

  65. Grote E, Belnap J, Housman D, Sparks J (2010) Carbon exchange in biological soil crust communities under differential temperatures and soil water contents: implications for global change. Glob. Chang. Biol. 16:2763–2774

    Google Scholar 

  66. FAO (2005) The importance of soil organic matter: key to drought-resistant soil and sustained food and production. http://www.fao.org/3/a-a0100e.pdf

  67. Belnap J, Gardner JS (1993) Soil microstructure in soils of the Colorado Plateau: the role of the cyanobacterium Microcoleus vaginatus. Great Basin Nat. 53:40–47

    Google Scholar 

  68. García-Pichel F, Belnap J (1996) Microenvironments and microscale productivity of cyanobacterial desert crusts. J. Phycol. 32:774–782

    Google Scholar 

  69. Zhang BC, Zhou XB, Zhang YM (2015) Responses of microbial activities and soil physical-chemical properties to the successional process of biological soil crusts in the Gurbantunggut Desert, Xinjiang. J. Arid. Land 7(1):101–109

    Google Scholar 

  70. Rivera-Aguilar V, Godínez-Alvarez H, Moreno-Torres R, Rodríguez-Zaragoza S (2009) Soil physico-chemical properties affecting the distribution of biological soil crusts along an environmental transect at Zapotitlán drylands, Mexico. J. Arid Environ. 73:1023–1028

    Google Scholar 

  71. Pushkareva E, Pessi IS, Wilmotte A, Elster J (2015) Cyanobacterial community composition in Arctic soil crusts at different stages of development. FEMS Microbiol. Ecol. 91(12):fiv143

    PubMed  PubMed Central  Google Scholar 

  72. Concostrina-Zubiri L, Huber-Sannwald E, Martínez I, Flores JF, Escudero A (2013) Biological soil crusts greatly contribute to small-scale soil heterogeneity along a grazing gradient. Soil Biol. Biochem. 64:28–36

    CAS  Google Scholar 

  73. Darby BJ, Neher DA, Belnap J (2007) Soil nematode communities are ecologically more mature beneath late- than early-successional stage biological soil crusts. Appl. Soil Ecol. 35:203–212

    Google Scholar 

  74. Geisseler D, Horwath W, Scow K (2011) Soil moisture and plant residue addition interact in their effect on extracellular enzyme activity. Pedobiologia 54:71–78

    Google Scholar 

  75. Miralles I, Domingo F, Garcia-Campos E, Trasar-Cepeda C (2012) Biological and microbial activity in biological soil crusts from the Tabernas desert, a sub-arid zone in SE Spain. Soil Biol. Biochem. 55:113–121

    CAS  Google Scholar 

  76. Chamizo S, Cantón Y, Lázaro R, Domingo F (2013) The role of biological soil crusts in soil moisture dynamics in two semiarid ecosystems with contrasting soil textures. J. Hydrol. 489:74–84

    Google Scholar 

  77. Sardans J, Peñuelas J, Ogaya R (2005) Drought decreases soil enzyme activity in a Mediterranean Quercus ilex L. forest. Soil Biol. Biochem. 37:455–461

    CAS  Google Scholar 

  78. Cannone N, Wagner D, Hubberten HW, Guglielmin M (2008) Biotic and abiotic factors influencing soil properties across a latitudinal gradient in Victoria Land, Antarctica. Geoderma 144(1–2):50–65

    CAS  Google Scholar 

  79. Fontaine S, Marotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition. Soil Biol. Biochem. 35:837–843

    CAS  Google Scholar 

  80. Lal R, Kimble JM, Follett RF, Stewart BA (1998) Soil processes and the carbon cycle. CRC Press, Florida, p 609

    Google Scholar 

  81. Buschiazzo DE, Estelrich HD, Aimar SB, Viglizzo E, Babinec FJ (2004) Soil texture and tree coverage influence on organic matter. J. Range Manag. 57:511–516

    Google Scholar 

  82. Cenini V, Fornara D, Mcmullan G, Ternan N, Carolan R, Crawley MG, Clement JC, Lavorel S (2016) Linkages between extracellular enzyme activities and the carbon and nitrogen content of grassland soils. Soil Biol. Biochem. 96:198–206

    CAS  Google Scholar 

  83. Trasar-Cepeda C, Leiros MC, Gil-Sotres F (2008) Hydrolytic enzyme activities in agricultural and forest soils. Some implications for their use as indicators of soil quality. Soil Biol. Biochem. 40:2146–2155

    CAS  Google Scholar 

  84. Acosta-Martínez V, Klose S, Zobeck TM (2003) Enzyme activities in semiarid soils under conservation reserve program, native rangeland, and cropland. J. Plant Nutr. Soil Sci. 166:699–707

    Google Scholar 

  85. Adetunji AT, Lewu FB, Mulidzi R, Ncube B (2017) The biological activities of β-glucosidase, phosphatase and urease as soil quality indicators: a review. J. Soil Sci. Plant Nutr. 17:794–807

    Google Scholar 

  86. Olander L, Vitousek P (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochem 49:175–191

    CAS  Google Scholar 

  87. Quiquampoix H (2000) Mechanisms of protein adsorption on surfaces and consequences for extracellular enzyme activity in soil. In: Bollag JM, Stotzky G (eds) Soil biochemistry. Marcel Dekker, New York, pp 171–206

    Google Scholar 

  88. Gianfreda L, Bollag MJ (1996) Influence of natural and anthropogenic factors on enzyme activity in soil. In: Stotzky G, Bollag JM (eds) Soil biochemistry, vol 9. Marcel Dekker, New York, pp 123–193

    Google Scholar 

  89. Bindu MV, Harikumar VS (2016) Soil contamination and remediation effects on the structure and activity of soil microbial communities. Science 242 p

  90. Knelman JE, Graham EB, Ferrenberg S, Lecoeuvre A, Labrado A, Darcy JL, Nemergut DR, Schmidt SK (2017) Rapid shifts in soil nutrients and decomposition enzyme activity in early succession following forest fire. Forests 8(9):347. https://doi.org/10.3390/f8090347

    Article  Google Scholar 

  91. Yang X, Wei K, Chen Z, Chen L (2016) Soil phosphorus composition and phosphatase activities along altitudes of alpine tundra in Changbai Mountains, China. Chin. Geogr. Sci. 26:90–98

    Google Scholar 

  92. Turner BL (2010) Variation in pH optima of hydrolytic enzyme activities in tropical rain forest soils. Appl. Environ. Microbiol. 76:6485–6493

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Arrieta JM, Herndl GJ (2001) Assessing the diversity of marine bacterial β-glucosidases by capillary electrophoresis zymography. Appl. Environ. Microbiol. 67:4896–4900

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Cao Y, Green PG, Holden PA (2008) Microbial community composition and denitrifying enzyme activities in salt marsh sediments. Appl. Environ. Microbiol. 74(24):7585–7595

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Nottingham AT, Turner BL, Whitaker J, Ostle N, Bardgett RD, McNamara NP, Salinas N, Meir P (2016) Temperature sensitivity of soil enzymes along an elevation gradient in the Peruvian Andes. Biogeochemistry 127(2):217–230

    CAS  Google Scholar 

  96. Qiu Y, Zhang J (1999) Quantitative analysis to the gradients in space and time of natural plant communities in Bashuigou of the Guandi Mountain. Chin. J. App. Environ. Biol. 5:113–120 (In Chinese)

    Google Scholar 

  97. Toberman H, Laiho R, Evans CD, Artz RRE, Fenner N, Strakova P, Freeman C (2010) Long-term drainage for forestry inhibits extracellular phenol oxidase activity in Finnish boreal mire peat. Eur. J. Soil Sci. 61:950–957

    Google Scholar 

  98. Pind A, Freeman C, Lock MA (1994) Enzymic degradation of phenolic materials in peatlands—measurement of phenol oxidase activity. Plant Soil 159:227–231

    CAS  Google Scholar 

  99. Freeman C, Ostle N, Kang H (2001) An enzymic ‘latch’ on a global carbon store. A shortage of oxygen locks up carbon in peatlands by restraining a single enzyme. Nature 409:149

    CAS  PubMed  Google Scholar 

  100. Sedia EG, Ehrenfeld JG (2003) Lichens and mosses promote alternate stable plant communities in the New Jersey Pinelands. Oikos 100:447–458

    Google Scholar 

  101. Saenz MT, Garcia MD, Rowe JG (2006) Antimicrobial activity and phytochemical studies of some lichens from south of Spain. Fitoterapia 77:156–159

    CAS  PubMed  Google Scholar 

  102. Shrestha G, St. Clair LL (2013) Lichens: a promising source of antibiotic and anticancer drugs. Phytochem. Rev. 12:229–244

    CAS  Google Scholar 

  103. Martίnez I, Escudero A, Maestre FT, de la Cruz A, Guerrero C, Rubio A (2006) Small-scale patterns of abundance of mosses and lichens forming biological soil crusts in two semi-arid gypsum environments. Aust. J. Bot. 54:339–348

    Google Scholar 

  104. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Wolińska A, Bennicelli R (2010) Dehydrogenase activity response to soil reoxidation process described as varied condition of water potential, air porosity and oxygen availability. Pol. J. Environ. Stud. 19:651–657

    Google Scholar 

  106. You Y, Wang J, Huang X, Tang Z, Liu S, Sun OJ (2014) Relating microbial community structure to functioning in forest soil organic carbon transformation and turnover. Ecol. Evol. 4:633–647

    PubMed  PubMed Central  Google Scholar 

  107. Kivlin SN, Treseder KK (2014) Soil extracellular enzyme activities correspond with abiotic factors more than fungal community composition. Biogeochem 117:23–37

    CAS  Google Scholar 

  108. Ladlie JS, Meggitt WF, Penner D (1976) Effect of soil pH on microbial degradation, adsorption, and mobility of metribuzin. Weed Sci. 24:477–481

    CAS  Google Scholar 

  109. Singh H, Reddy MS (2011) Effect of inoculation with phosphate solubilizing fungus on growth and nutrient uptake of wheat and maize plants fertilized with rock phosphate in alkaline soils. Eur. J. Soil Biol. 47:30–34

    CAS  Google Scholar 

  110. Li J, Okin GS, Alvarez L, Epstein H (2007) Quantitative effects of vegetation cover on wind erosion and soil nutrient loss in a desert grassland of southern New Mexico, USA. Biogeochem 85:317–332

    Google Scholar 

  111. Whitford WG (2002) Ecology of desert ecosystems. Academy, New York, p 151

    Google Scholar 

  112. Belnap J, Eldridge D (2001) Disturbance and recovery of biological soil crusts. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer-Verlag, Berlin, pp 363–383

    Google Scholar 

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Acknowledgements

W. Ghiloufi was supported by a fellowship from the National Research Foundation of Korea funded by the Ministry of Science, ICT and Future Planning (2016R1D1A1A02937049). H. Kang is grateful to the ERC (20110030040) and SGER (2016R1D1A1A02937049) funded by the National Research Foundation of Korea, and fund from the Korea Forest Service (2017096A001719BB01). The authors thank colleagues who helped with the lab work.

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  1. Unit of Research Plant Biodiversity and Ecosystems in Arid Environments, University of Sfax, Sfax, Tunisia

    Wahida Ghiloufi & Mohamed Chaieb

  2. School of Civil and Environmental Engineering, Yonsei University, Seoul, 03722, South Korea

    Juyoung Seo, Jinhyun Kim & Hojeong Kang

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  1. Wahida Ghiloufi
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Ghiloufi, W., Seo, J., Kim, J. et al. Effects of Biological Soil Crusts on Enzyme Activities and Microbial Community in Soils of an Arid Ecosystem. Microb Ecol 77, 201–216 (2019). https://doi.org/10.1007/s00248-018-1219-8

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  • DOI: https://doi.org/10.1007/s00248-018-1219-8

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