The protective role of cyanobacteria on soil stability in two Aridisols in northeastern Iran

Geoderma Regional 15 (2018) e00201

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The protective role of cyanobacteria on soil stability in two Aridisols in northeastern Iran Adel Sepehr a,⁎, Mahvan Hassanzadeh a, Emilio Rodriguez-Caballero b,c a b c

Dept. of Desert and Arid Zones Management, Ferdowsi University of Mashhad, Mashhad, Iran Dept. of Desertification and Geo-Ecology, Experiemntal stations of Arid Lands (EEZA, CSIC), Carretera Sacramento s7n, Almería, Spain Departamento de Agronomía, Universidad de Almería, Carretera Sacramento s7n, Almería, Spain

a r t i c l e

i n f o

Article history: Received 15 June 2018 Received in revised form 26 November 2018 Accepted 30 November 2018

Keywords: Biological soil crust Soil stability Alluvial deposits Biocrust Aridisols Iran

a b s t r a c t Structure of cyanobacteria crusts are contained of a variety of species that having a range of attributes which contributed to their resilience and survival in arid and hyper-arid environments. Extracellular polymeric substances (EPS) produced by cyanobacteria have adhesive attributes that binds non-aggregated soil particles into a protective encrusted surface and reduces the destructive effects of wind and water erosion. In this study, we wanted to analyze the importance of soil cyanobacteria on soil stability over different landforms. To do this, we firstly was identified native and dominant cyanobacteria species, we measured different soil physicochemical properties related to soil stability and we explored the relationship between soil characteristics, stability and cyanobacteria presence. We found that cyanobacteria are able to colonize stable soils under arid conditions. However only few tolerant species were found on saline soils. Cyanobacteria promoted soil organic carbon and nitrogen. Moreover, EPS secreted by cyanobacteria increased soil water content and blind soil particle together, forming aggregates and increasing surface stability. © 2018 Published by Elsevier B.V.

1. Introduction Characterized by scarce vegetation coverage over and an exclusive diversity of landforms such as alluvial fans, clay plain, dry-lake playa, salty pans, sand dunes etc., arid and semi-arid environments comprise about one third of the global Earth's land surface (UNEP, 2011). Increased human pressure as well as inherent environmental constrains such as water scarcity and high salinity has increased soil degradation and related erosion problems in these regions (Dregne, 2002; Gamo et al., 2013). For example, in Iran, which is located in heart of Middle East and mainly characterized by arid and semi-arid climate, soil degradation and subsequent desertification process are among the main environmental problems. Soil degradation may negatively affect water resources and produce a decrease in agricultural productivity that will lead to poverty, socio-economic instabilities and a collapse of socio-ecosystems (Sarparast et al., 2018). Most bare soils and open spaces among vascular plants in arid and semiarid environments are not bare but covered by other permanent life forms such as biological soil crust or biocrusts (Weber et al., 2016). These are complex communities dominated by photoatrophic organisms such as algae, cyanobacteria, lichen, mosses in intimate association with the uppermost millimeters of the soil surface, that cover about 12% ⁎ Corresponding author. E-mail address: [email protected] (A. Sepehr).

https://doi.org/10.1016/j.geodrs.2018.e00201 2352-0094/© 2018 Published by Elsevier B.V.

of the global earth surface, fixing large amount of C and N (RodriguezCaballero et al., 2018). As consequence of their plasticity and their capacity to colonize acid or alacaline soils in extremely hot or very cold environments with low precipitation and prolonged drought periods under very high incoming solar radiation levels, cyanobacteria are the pioneer biocrust components (Pointing and Belnap, 2012). By successfully colonizing the soil surface, cyanobacteria improves soil fertility through mineral chelation, dust entrapment, and nutrient fixation, preparing soils for the establishment of more developed biocrust communities, plants and animals (Belnap et al., 2001; Mager and Thomas, 2011). Moreover, several studies revealed that by producing extracellular polymeric substances (EPS) cyanobacteria, bind soil particles together, increases aggregate stability and reduce the erosive impacts of wind and water (Eldridge and Leys, 2003; Issa et al., 2007; Rossi et al., 2017). Moreover, increased organic matter as consequence of cyanobacteria physiological activity increases water repellency and adhesion between soil particles, promoting aggregates resistance to the wetting and improving structure and stability (Whitton, 1987; Chenu et al., 2000; Issa et al., 2001; Maqubela et al., 2009). Particle size distribution and aggregates stability are dynamic soil properties that determine soil resistance to erosive forces and its capacity to provide key functions such as water infiltration (Carter et al., 1994; Ma et al., 2015). Apart of the well-known effect of soil cyanobacteria on aggregate stability, there are other important factors controlling this: i) internal factors or intrinsic soil properties (E.G. ions concentration, EC, pH,

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sodium adsorption ratio, organic matter content, clay mineral composition) and ii) external factors (E.G. climate, geomorphology, and season) (Amezketa, 1999). For example soils containing coarse aggregates are more stable than soil with fine particles (Topp et al., 1997), and many studies have shown the positive role of organic matter in formation and stability of aggregates (Tisdall and Oades, 1982; Lynch and Bragg, 1985; Boix-Fayos et al., 2001; Fullen and Booth, 2006; Zhang et al., 2008; Marques et al., 2009; Wu et al., 2013). In this research, we want to compare soil stability values between different landforms with special emphasis on the role played by biocrust forming cyanobacteria. To do this, we i) firstly was identified native and dominant cyanobacteria species within different landforms ii) then we measured different soil physicochemical properties related to soil stability, iii) ultimately the relationships between soil characteristics, stability and cyanobacteria activities were analyzed. 2. Materials and methods

Martonne, 1941), KR is a semiarid area with an average temperature of 14.2 °C and 230 mm of total annual rainfall and mainly dominated by aridisols. Within this area, two different study sites were chosen (Fig. 1). An alluvial fan area with debris flow deposits that is located in a degradation geomorphological zone with area about 19.4 ha (Site 1; 36°10′N and 58°59′E), and a clay plain area with evaporated deposits located in an aggregation geomorphological zone with area about 16.8 ha (Site 2; 35°58′N and 59°1′E). Site 1 is mainly composed by quaternary formations of fillet, schist, conglomerate and lime stone; and alluvial deposits that provided a stable and fertile surface for establishment of biocrusts including cyanobacteria, algae, lichen, and mosses. Dominant soils are Regosols with loamy texture (Table 1). Site 2 includes evaporative depositions with high salt and mainly composed by gypsum, carbonate and halite sediments. Dominant soils are clay loam with high concentration of soluble salts that limited biocrust colonization. Table 1 describes soil order and some characteristics in two studied sites.

2.1. Regional settings

2.2. Field methods and laboratory analysis

This study was conducted in Khorasan-Razavi (KR) province at northeastern of Iran. According to De Martonne classification (De

A total of 36 soil samples were acquired within the two different study sites. 12 random samples of clearly visible developed

Fig. 1. Study area location.

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expressed as percentages (modified from: USDANRCS, EFH NOTICE 210-WI-62).

Table 1 Soil order and type in the two studied sites.⁎

Order Sub_Order Principal qualifiers Supplementary qualifiers Soil Temperature Regime Soil Moisture Regime Soil Texture

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Alluvial fan

Clay plain

Aridisol Lithosol, Regosol Mollic, Calcaric Colluvio, Falvius Mesic Dry Xeric, Weak Aridic Loam

Aridisol Solonchak Natric, Salic Ochric Thermic Aridic Clay loam

⁎ The soil type of the two sites are classified in the Aridisols Order. Soil Sub_Order of site 1 is Regosolic and Lithosol located on calcareous rocks with comprise very thin soils over continuous rocks. Soil Sub_Order of site 2 is Solonchaks and it have a high concentration of soluble salts, as well as high clay content. The soil texture in site 1 was generally light to moderate and belongs to the class loam; and site 2 belongs to the class clay loam.

cyanobacteria dominated biocrust at study site 1 (alluvial fan with cyanobacteria crusts-AFC), 12 random samples of soils not covered by cyanobacteria at study site 1 (alluvial fan without cyanobacteria crusts-AFN), and 12 random samples at site 2 (salty-clay plain-CPS). Cyanobacteria dominated biocrust were not found at study site 2, thus, only one class was considered at this site. Cyanobacteria dominated soils were selected as these in which cyanobacteria were clearly visible using a magnifying glass 20×. To make cyanobacteria crusts visible, the soil surfaces were sprayed with deionized water before sampling. All samples were acquired by a petri-dish with diameter of 15 cm inserted into the soil surface at a depth of 5 cm. The samples were transported to the biogeomorphology lab of Natural Resources and Environment (NRE) faculty in Ferdowsi University of Mashhad and stored at 4 °C (the icebox) during one week. Available cyanobacteria on the different samples were cultivated by the methodology proposed by Kaushik (1987). Then, we identified morphological characteristics of different species or colonies by using a microscope (magnifications 400–1000 x (Olympus CH-2)). When possible, dominant cyanobacteria species composition was identified by using a Scanning Electron Microscope (SEM) (Leo-Germany 1450VP) and light-microscope in combination with the following taxonomic references: Skinner and Entwisle (2002); Anagnostidis and Komarek (2005); Sant'Anna et al. (2011). This information was used to discuss their effect on soil stability. For the analysis of soil physicochemical characteristics and soil stability, an additional set of samples was acquired at each study site. Soil samples were taken from the upper soil surface (0–5 cm) and transported to the NRE lab of Ferdowsi University of Mashhad, airdried and sieved with a 2 mm mesh. After that, soil texture (the percentage of clay, silt, and sand) was determined using a hydrometer (ASTM 152H; Bouyoucos, 1962). Electrical conductivity (EC) and pH were measured with a soil–water suspension in the ratio of 1: 1 by EC meter and a pH meter (Jenway Inc., England); soil organic carbon (SOC) was estimated by the dichromate oxidation method (Nelson and Sommers, 1982); total nitrogen was measured by the Kjeldahl method (Bremner and Mulvaney, 1982); sodium percentage was measured by the methods described by Knudsen et al. (1982); calcium and magnesium were measured by the complexometric method (Tucker and Kurtz, 1961); calcium carbonate measured with a calcimeter Scheibler system 08.53, and soil moisture content in the surface soil (depth 0–10 cm) was calculated by weight method (oven-dry method) (Black, 1965). Additionally, we analyzed mean weight diameter of aggregates (MWD; Kemper and Roseanau, 1986), soil aggregate stability (SAS; Kemper and Koch, 1966 and Murer et al., 1993). Clay dispersion index (CDI) was also determined through the positioning of an aggregate of 4 to 5 mm diameter in a petri-dish filled with distilled water. The extent of aggregate's clay dispersion, as display by the formation of a muddy cloud around it was measured twice: 10 and 120 min after the beginning of the experiment. Dispersion index scores ranged from 0 for no cloud formation, 1 for slight cloud, 2 for moderate cloud, 3 for strong cloud, and 4 for complete cloud formation of the aggregate's clays that

2.3. Statistical analyses Cyanobacteria composition and cyanobacteria richness in the four different subsets (cyanobacteria crusts-AFC, soil under-AFC, AFN and CPS) was estimated by using, Shannon diversity and Margalef indices. Differences in soil properties and soil stability between AFC, AFN, and CPS we assessed by analysis of variance (ANOVA) and Duncan's post-hoc comparison. Moreover, we explored possible correlation between soil stability indices and soil physicochemical parameters based on the Pearson test. The analyses were performed with SPSS (ver. 20.0, IBM, US) software and all data were tested for normality assumption before data analysis (by the Kolmogorov-Smirnov test). 3. Results 3.1. Presence and absence of cyanobacteria species Site 1 presented higher cyanobacteria biodiversity and species richness than site 2 (Figs. 2 and 7; Table 2), and within this site the highest cyanobacteria biodiversity and species richness was found on biocrusted surfaces (Fig. 2; Table 2). The dominant species over these surfaces were: Leptolyngbya boryana, Leptolyngbya cf. tenerrima, Oscillatoria splendida, Oscillatoria tenuis, Microcoleus vaginatus, Phormidium tergestinum, and Nostoc commune. Some of these species such as Leptolyngbya boryana, Leptolyngbya cf. tenerrima, as well as other species of the genera Oscillatoria and Phormidium were also found in the soil under cyanobacteria dominated biocrusts, whereas species form the genra Nostoc were only found on the biocrust samples. Thought CPS site (Site 2) do not show a clear visible cyanobacteria crusts, we also found some species well adapted to salinity such as Oscillatoria splendida, Oscillatoria tenuis, Phormidium favosum and Phormidium uncinatum. However, there were only few colonies that grout only after 3–4 times the re-cultivation. 3.2. Comparison of soil characteristics in two sites: alluvial fan and clay plain There were clear differences in soil properties and stability values between different study sites (Table 3). Soil physicochemical characteristics and soil stability parameters of the three sampling sites (AFC, AFN, and CPS) are showed in Table 3. Soil moisture, clay content, EC, C/N, and SAR were significantly higher at the site 2 than at site 1, whereas CaCO3 showed the opposite pattern (Table 3). The Organic carbon content was also higher at site 2 when compared to site 1, whereas this area has lower CaCO3 and N.

Fig. 2. Margalef and Shannon indices values of cyanobacteria crust form Site 1, soil underlying cyanobacteria crust from Site 1, non-crusted surfaces from Site 1 and Site 2.

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Table 2 Number of Cyanobacteria species found in samples of alluvial fan (site 1) and salty-clay plain (site 2). Detailed picture of the different cyanobacteria species are shown in Fig. 7. Cyanobacteria species

Anabaena sp. Aterocapsa cf. belizensis Gloeocapsa magma Leptolyngbya boryana Leptolyngbya cf. tenerrima Leptolyngbya sp. Microcoleus vaginatus Nostoc commune Nostoc desertorum Nostoc indistinguendum Nostoc membranaceum Oscillatoria annae Oscillatoria irrigua Oscillatoria splendida Oscillatoria tenuis Phormidium chalybeum Phormidium favosum Phormidium tergestinum Phormidium uncinatum Pseudanabaena sp. Tolypothrix sp.

Alluvial deposits (site 1)

Clay plain (site 2)

Crust (0–0.01 cm)

Under Crust (0.01 cm–5 cm)

Non Crust (0–5 cm)

Non Crust (0–5 cm)

0 3 5 12 9 3 7 7 5 3 2 4 6 9 9 6 3 7 6 6 3

1 0 0 9 9 0 5 0 0 0 0 9 3 0 3 0 0 0 6 4 3

5 0 0 4 3 0 1 0 0 0 0 6 0 0 0 0 0 0 1 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 3 6 0 3 0 4 0 0

There were also significant differences between sampling sites in the three different soil stability indices between the studies surface. From the different surfaces CPS has the highest value of CDI, where as MWD and SAS levels were significantly higher at Site 1. Soils covered by biocrust and non-crusted surfaces on site 1 also showed contrasting stability values, being SAS and MWD higher on areas covered by biocrusts. Fragment size distribution of soil aggregates size also varied between the different study sites and between crusted and non-crusted surfaces (Fig. 3). Cyanobacteria crusts showed the highest fraction of coarser soil aggregates (N2 mm) with a mean value of MWD = 0.99 mm, whereas AFN showed higher content of fine soil aggregates (b0.045 mm, and lower values of MWD = 0.48 mm). This parameter indicates that cyanobacteria can create larger soil aggregates by binding the smaller particles with polysaccharides (Fig. 4), because the soil texture of both regions is very similar. These results are corroborated by SEM images, which clearly showed that exopolysaccharides produced by cyanobacteria bling soil particles together forming larger soil aggregates that increases soil stability (Fig. 4). Site 2 showed the smallest aggregate size of the three studied surfaces (MWD = 0.06 mm; Fig. 4). These differences in soil stability and aggregate formation also affected soil structure. As shown in Fig. 5-1 and 5-2, soil not covered by cyanobacteria had massive and platy structure with very low porosity, whereas cyanobacteria dominated soils (Fig. 6-3, 6-4) were characterized by granular structure with high porosity.

3.3. Investigation of relationship between soil stability indices and soil physicochemical properties Correlation analysis demonstrated that soil stability was mainly drive by soil physicochemical properties. As we can see on Fig. 4, SAS index were directly correlated with soil moisture (0.785) and nitrogen (0.628), while it decreases as CaCO3 (−0.574), pH (−0.515) and silt percentage (−0.437) increases. MWD also showed a strong positive correlation with soil moisture (0.87) and nitrogen (0.632), but also increases as SOC (0.467) and clay content did (0.451) and decreases at larger pH values (EPS produced by cyanobacteria tramp clay particles forming larger soil aggregates). The CDI index showed the opposite pattern, with increasing values as CaCO3 (0.554), pH increased (0.532), soil moisture (−0.702) and nitrogen (−0.683) increased. 4. Discussion 4.1. Failure to form cyanobacteria crust in the clay plain area Cyanobacteria are well adapted to high weather-induced stress but they are very sensitive to small changes in environmental conditions and anthropogenic disturbances, which may lead to a biocrust coverage loss, and the replacement of well-developed communities by early stages of succession that are less resistant to erosive forces (Evans and

Table 3 Average ± standard deviation values of the different soil physicochemical properties and soil stability indices within the three sampling units (alluvial fan with cyanobacteria crusts-AFC, alluvial fan without cyanobacteria crusts-AFN, salty-clay plain-CPS), different letters indicate significant differences between sampling units according to the Duncan post-hoc test.

Soil physicochemical properties

Soil stability parameters

Elements

AFC

AFN

CPS

Soil moisture (%) Sand (%) Silt (%) Clay (%) SOC (%) CaCO3 (%) N (mg/kg) pH EC (ds/m) SAR C/N CDI (%) SAS (%) MWD (mm)

2.69 ± 0.29 b 44.83 ± 1.54 a 33.37 ± 2.5 c 21.78 ± 1.78 b 0.51 ± 0.1 b 21.01 ± 1.09 ab 807.39 ± 122.03 a 8.12 ± 0.04 b 0.37 ± 0.09 b 1.18 ± 0.04 b 6.35 ± 1.36 b 18.07 ± 4.97 c 10.34 ± 1.51 a 0.99 ± 0.05 a

1.57 ± 0.05 c 43.95 ± 2.19 a 35.39 ± 2.1 b 20.64 ± 0.3 b 0.346 ± 0.15 c 21.56 ± 1.89 a 490.03 ± 121.23 b 8.33 ± 0.11 a 0.37 ± 0.12 b 1.25 ± 0.15 b 7.60 ± 3.11 b 33.89 ± 4.75 b 4.18 ± 1.68 b 0.48 ± 0.1 b

5.26 ± 0.9 a 18.66 ± 4.28 b 40.48 ± 0.75 a 40.84 ± 4.04 a 0.66 ± 0.1 a 19.86 ± 0.99 b 418.41 ± 110.52 b 7.99 ± 0.27 b 36.61 ± 21.48 a 79.48 ± 37.62 a 11.83 ± 1.96 a 53.63 ± 4.66 a 3.22 ± 3.17 b 0.06 ± 0.01 c

Note: Within a given soil properties, different superscripts indicate a significant among the three classes (Mean ± Std. Deviation), respectively, at p b .05.

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microbial communities than expected by the high humidity and organic carbon content (Yu and Steinberger, 2012). Environmental disturbances (Garcia et al., 2015), and other stress factors such as wind erosion, also represent an obstacle for cyanobacteria colonization and biocrust formation. For all these reasons, thought SOC levels are very high, this site showed the lowest stability values of the different surfaces analyzed in this study (Table 3). This corroborated that, in a similar way as observed on other regions (Bowker et al., 2016), environmental conditions in site 2 act as abiotic filter for cyanobacteria biocrust colonization, and demonstrated that cyanobacteria dominated biocrusts are one of the most important stabilizing agents in drylands soils (Bowker et al., 2016).

4.2. The role of cyanobacteria in the formation of soil aggregates and soil stability

Fig. 3. Fragment size distributions of soil aggregates obtained by the MWD method in the three sampling units (alluvial fan with cyanobacteria crusts-AFC, alluvial fan without cyanobacteria crusts-AFN, salty-clay plain-CPS).

Johansen, 1999; Warren, 2014; Belnap et al., 2018). The different study sites analyzed by us represent different landforms that provided contrasting habitat for cyanobacteria establishment and biocrust development. Study site 1 is mainly composed by alluvial deposits formed during debris flow processes that represent a stable habitat for cyanobacteria and biocrust colonization, which are clearly visible, on different stages of development on the topsoil at different stages of development. Whereas hyper conditions as well as salt accumulation, abundance of sodium, calcium, magnesium ions and high SAR and EC levels that characterize site 2 (Table 3), prevents the establishment of vegetation and impede the formation of visible surface biocrust, however some grow resistant cyanobacteria species after several recultivation (Table 2 whit species found: Oscillatoria splendida, Oscillatoria tenuis, Phormidium favosum, Phormidium uncinatum). As nitrogen fixation in most drylands soils is mainly derived by biocrust forming organisms and related bacterial populations (Evans and Lange, 2003; Belnap, 2003), this resulted in reduced amount of fixed N (Kidron, 2016), which together to high C inputs from dust and windy deposits raises the C/N ratio to levels of 11.8 (Table 3). Moreover, high salinity levels as well as the absence of a visible cyanobacteria dominated biocrust at site 2 could lead to lower values of the functional diversity of

Fig. 4. Pearson correlation coefficient between soil stability indices and soil physicochemical properties: soil moisture (SM), silt fraction (Silt), clay fraction (Clay), organic matter content (SOC), calcium carbonate content (CaCO3), Nitrogen (N), and Ph. ** and * indicate significant correlation p b .01 and p b .05, respectively.

As previously reported in other regions biocrusted surfaces from in Khorasan-Razavi province (Iran) were compositionally distinct topsoil microbiomes with higher richness of most cyanobacteria species such as Leptolyngbya boryana, Leptolyngbya cf. tenerrima, Oscillatoria splendida, Oscillatoria tenuis, Microcoleus vaginatus, Nostoc sp, Phormidium tergestinum and Tolypothrix sp. (Table 2); these identified species confirm the results of Williams et al. (2017) in biocrusts were compositionally distinct topsoil microbiomes. Most of these species fix C and N controlling biogeochemical cycles (Elbert et al., 2012), and improving soil fertility in most arid environments (Jeffries et al., 1992; Lange et al., 1994; Mayland and McIntosh, 1966). This is corroborated by results obtained at site 1. As shown in Table 3 organic carbon content has increased up to 1.5 times and Nitrogen content was doubled when soil was colonized by cyanobacteria, which resulted in a reduction of the C/N ratio and may produce changes in soil nutrient stoichiometry, with important implications for plant productivity (Delgado-Baquerizo et al., 2013). These differences were exacerbated when biocrust from site 1 where compared with bare areas form site 2 (clay plain area), where in the lowest levels of cyanobacteria diversity and abundance, as well as the lowest values in soil nutrient concentrations were observed. These results confirm the studies of Hamza and Anderson (2005); Rao et al. (2012), and Williams and Eldridge (2011) that fount a negative effect of environmental stress on cyanobacterial communities. Also soil compaction caused reduced nutrient recycling and mineralization, and limited the activity and biodiversity of soil microorganisms (Table 4). Biocrusts species also secrete EPS (Decho, 1990; Belnap and Gardner, 1993; Hu et al., 2003), which increase soil water retention capacity due to the hygroscopic properties of polysaccharides (Decho, 1990; Rossi et al., 2017). This explains the higher soil water content values observed on cyanobacteria dominated areas (AFC) than on soils without biocrust presence (Table 3). EPS and cyanobacteria filaments also act as binding agent for soil particles (Lynch and Bragg, 1985; Issa et al., 2007; Rossi et al., 2017). By doing that, they trap fine particles forming stable aggregates (Fig. 5) that lead to the development of an organic-bridge between contiguous soil particles that represent a strong armored surface (Fig. 54) as showed by Rossi et al. (2017). This is the main reason why bio crusted surfaces from site 1 showed higher stability values, larger MWD and SAS than non-bio crusted soils from same place, whereas clay dispersion of non-crusted soils is twice this found on areas colonized by cyanobacteria biocrust (Fig. 3). These results are consistent with results obtained by Issa et al. (2007) who found the increase in aggregate stability is presumably related to the effect of cyanobacteria and EPS. Generally, the SAS and MWD do not show large spatial variability stability indices are on the front of the physicochemical properties changes in the same side, and the increase of these two indices and the decrease of the CDI index in the sample site with cyanobacteria crust indicate the increase of soil stability by cyanobacteria. Nevertheless, content of SAR and EC show a significant amount comparing with other two sites. Therefore, EC and SAR are increased in the surface without cyano-crusts, versus nitrogen and organic matter indicated high

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Fig. 5. SEM images showing cyanobacteria binding effect. Pictures 1 and 2: soil surface without cyanobacteria in site 2. Picture 3: Large batches cyanobacteria that contain a number of cyanobacteria strings in a pod. Picture 4: extracellular polymeric substances (EPS) secreted by cyanobacteria. Picture 5: mark a complicated network of cyanobacteria that surrounding soil particles. Picture 6: cyanobacteria filaments play the role of connecting soil particles.

amounts in the surfaces with visible cyanobacteria. These results confirm the first hypothesis. 5. Conclusions We found that cyanobacteria species including Leptolyngbya boryana, Leptolyngbya cf. tenerrima, Oscillatoria splendida, Oscillatoria tenuis, Microcoleus vaginatus, Nostoc commune and Phormidium

tergestinum are able to colonize soils from arid and semi-arid areas in Iran. However, high salinity levels found on site 2, as well as perturbation and extreme wind erosion, act as abiotic filters for cyanobacteria colonization which showed very low biodiversity and richness values in comparison with Site 1. At this site only very salt tolerant species such as Oscillatoria splendida and Oscillatoria tenuis are able to survive. EPS secreted by cyanobacteria blind soil particle together, forming aggregates, increasing surface stability, and reducing clay dispersion.

Fig. 6. Soil building (pictures have been prepared using stereomicroscope): pictures 1 and 2 are taken from site 2 - CPS: soil without cyanobacteria; pictures 3 and 4 are from site 1 - AFN: soil without cyanobacteria; pictures 5 and 6 from site 1 - AFC: soil with cyanobacteria.

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Fig. 7. Cyanobacteria species identified in soil surface samples (0-5 cm) at the two different sites.

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Fig. 7 (continued).

Table 4 Results of the independent sample test (T_test) evaluating differences in Soil physicochemical properties and Soil stability parameters between sampling units (alluvial fan with cyanobacteria crusts-AFC, alluvial fan without cyanobacteria crusts-AFN, salty-clay plain-CPS). Elements

Soil physicochemical properties

Soil stability parameters

Soil moisture (%) Sand (%) Silt (%) Clay (%) SOC (%) CaCO3 (%) N (mg/kg) pH EC (ds/m) SAR C/N CDI (%) SAS (%) MWD (mm)

Levene's test for equality of variances

t-test for equality of means

F

Sig.

t

df

Sig. (2_tailed)

11.946 1.924 0.474 6.301 3.043 7.674 0 28.982 2.172 16.849 11.145 0.381 0.47 4.686

0.002 0.179 0.498 0.02 0.095 0.011 0.999 0 0.155 0 0.003 0.543 0.5 0.042

12.819 1.135 −2.137 2.184 3.077 −0.875 6.391 −5.882 0.081 −1.445 −1.267 −7.958 9.405 15.53

11.744 22 22 11.633 22 17.637 22 13.646 22 12.779 15.044 22 22 15.167

0 0.268 0.044 0.05 0.006 0.393 0 0 0.936 0.172 0.225 0 0 0

Mean difference

Std. error difference

1.122 0.879 −2.018 1.139 0.163 −0.553 317.358 −0.207 0.003 −0.066 −1.244 −15.8168 6.154762 0.510394

0.087 0.774 0.944 0.521 0.053 0.632 49.657 0.035 0.043 0.045 0.982 1.987637 0.654382 0.032865

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