Cyanobacterial biocrust alters soil physical properties reducing soil erosion and aerosol production

Abstract

Aerosol emission by wind erosion in the arid and semi-arid areas of the world, is of environmental and health significance. Different methods have been used to mitigate aerosol emission among which the biological methods may be the most efficient ones. Although previously investigated, more research is essential to determine how the use of exopolysaccharide (biocrust)-producing cyanobacteria may affect soil physical properties. The objective was to investigate the effects of the cyanobacteria, Microcoleus vaginatus ATHK43 (identified and registered by the NCBI accession number MW433686), on soil physical properties of a sandy soil 15, 30, 60, and 90 d after inoculation. The effects of cyanobacterial biocrust on soil properties including shear strength, soil resistance, aggregate stability (mean weight diameter (MWD) and geometric mean diameter (GMD)), and wind erosion were determined in trays using a wind tunnel. Cyanobacterial inoculation significantly increased MWD (0–1 cm depth, from 0.12 mm to 0.47 mm) and GMD (from 0.3 to 0.5 mm) after a period of 90 d. Biocrust production significantly decreased soil erosion from 55.7 kgm^− 2 to 0.3 kgm^− 2 (wind rate of 50 kmh^− 1), and from 116.42 kgm^− 2 to 0.6 kgm^− 2 (wind rate of 90 kmh^− 1) after 90 d. In conclusion, cyanobacterial biocrust can significantly improve soil physical properties in different parts of the world including the deserts, and reduce aerosol emission by mitigating the destructive effects of wind erosion on soil physical properties.

Introduction

Aerosol emission is one of the most important environmental processes significantly affecting the climatic conditions of the world including the Middle East. The main reason for dusting is global climate change resulting in rainfall reduction, and subsequent wind erosion, intensified by drought, reduction of plant growth, and the drying of rivers, lakes and wetlands [1]. Deserts are the major sources of wind erosion and aerosols emission in the arid and semi-arid areas of the world. It is accordingly essential to find environmentally friendly methods, which may control wind erosion in such areas [2–4].

Different methods have been used for controlling dusting including the chemical (mulching), mechanical (wind controller) and biological ones (planting, and the use of microbes). Although there has been less research on the use of biological methods, they have been indicated as the most efficient ones [5, 6]. Soil microbes are among the first organisms, which are able to grow in the infertile and stressed soils [7]. Research has indicated the presence of photosynthetic cyanobacteria in the deserts, which are able to resist hard conditions and enhance soil physicochemical and biological properties by: (1) producing organic products including exopolysaccharides, and (2) increasing soil carbon and nitrogen. Although there is not any plant cover in most arid and semi-arid areas of the world, the cyanobacteria (autotroph soil microbes), can cover the soil by the production of the biochemical compounds called biocrust. The cyanobacteria are resistant to drought and intense light. The biocrust are able to maintain soil moisture and increase the availability of soil nutrients [8].

The cyanobacteria, as the most important producers of biocrusts, can fix nitrogen (N), of which 70% is transferred to the soil, as the main source of N for plant growth in the arid and semi-arid areas. Due to the photosynthetic ability of cyanobacteria, they are mostly found on the soil surface, which along with other soil microbes such as fungi (microfilaments), can produce a microbial biomass and increase soil resistance to soil erosion. The microbial biomass C and N are the most available nutrients of soil organic matter for plant and microbial use [9].

The biocrusts become inactive in drought stress conditions, and lose their water. They are able to tolerate such hard conditions and become metabolically active 8–10 h after being moistened by fog, dew and high vapor pressure, resulting in the processes of photosynthesis and respiration by the present microbes [10]. The biocrusts are ecologically important because they stabilize the structure of soil, and increase soil N concentration, which enhances plant growth and decreases wind erosion [11].

The filamentous cyanobacteria produce exopolysaccharides (EPS) (biocrusts), which cover the soil surface and bind the soil particles. The production of EPS by cyanobacteria can considerably contribute to the improvement of soil structure, increase nutrients in the soil surface, and enhance soil fertility [12]. In our just published article, we indicated the use of cyanobacteria producing biocrust is a suitable method for stabilizing soil particles and decreasing soil erosion of arid and semi-arid areas [13].

With respect to the above-mentioned details, and the ability of cyanobacteria to produce EPS in the hard conditions, it has been hypothesized it is possible to use cyanobacteria in the arid and semi-arid areas for biologically controlling the processes of soil erosion and dusting. Accordingly, due to the significance of soil physical properties in enhancing the stability of soil aggregates, and subsequent reduction of soil erosion and dusting, the objective of the present research was to investigate the effects of the cyanobacteria Microcoleus vaginatus ATHK43 on soil physical properties including soil erodibility and dusting emission.

Materials and methods

The research area, measuring 43000 ha, is located in the northern latitude of 32^o 40’ to 32^o 42’ and the eastern longitude of 52^o 00’ to 52^o 58’ in Isfahan province (eastern part), the central Iranian flat, and is the most important source of wind erosion in the province (Figs. 1 and 2). The altitude of the region is 1528 m, with average yearly rainfall and temperature of 105.4 mm and 15.3^oC, respectively, and the average monthly humidity is 36.8%. According to the De Martonne and Emberger climatic classification, the climate of the region is dry and cold, and according to Gussen it is semi desert (Fig. 3). The average wind rate is 3.2 ms^− 1 in the west direction.

Fig. 1.

(A) The research area, (B) the collected biocrust from the research area

Fig. 2.

Annual wind rose diagram in Isfahan (eastern part, 1977–2015)

Fig. 3.

(A) The variation of rainfall, (B) the amberothermic graph, and (C) the monthly average of days with dust during 1977–2015 in Isfahan Synoptic station

The experiment, which was a complete randomized block design, was conducted in the trays with the soil from the research area, and investigated the effects of cyanobacteria producing exopolysaccharide (EPS) on soil erodibility and dusting emission. The experimental treatments consisted of control, and inoculated soil at the depths of 0–1 and 1–5 cm. The soil was sprayed with well water with the salinity (EC) of 23.52 dSm^− 1 and pH of 7.1 at 1 mmd^− 1. The treated soil was sampled at 15, 30, 60 and 90 days after inoculation, and was analysed in the lab.

Cyanobacterial inoculation

The trays of 100 × 33 × 5 cm were filled up with the soil of the 1–5 cm depth, collected from the research area. Soil physicochemical properties were determined using the standard methods (Table 1) [14]. The cyanobacteria Microcoleus vaginatus ATHK43 previously isolated from the research area, as the dominant cyanobacterial strain in the region, was identified and registered in NCBI, with the accession number of MW433686 [13]. The cyanobacterial culture was centrifuged at 4000 g for 30 min, and dH2O was used for the suspension of the biomass and its dry weight was determined. The harvested culture was dissolved in distilled water and sprayed over the soil surface at the rate of 1.6 gm^− 2 dry weight [13]. The soil surface was kept moistened daily by spraying during the 90-d period of the experiment.

Table 1.

Soil chemical and physical characteristics

EC	pH	OC	N	K 1	Na	Ca	Mg	EPS	Chl a	Sand	Loam	Clay
dS m− 1		%	%	mg.g −					mg.m− 2		%
1.03	6.85	0.26	0.035	0.207	0.443	0.852	0.248	0.061	0.18	71	19	10

EC: electrical conductivity (salinity), OC: organic carbon, EPS: exopolysaccharides, Chl a: chlorophyll a

Measurement of soil biological properties

Soil organic carbon was measured by the method of Walkley and Black [15]. For the measurement of EPS, the soil samples were first air dried and sieved and then were extracted with sulfuric acid, and centrifuged for 30 m at 3000 g. The supernatant was determined for carbohydrate concertation according to Dubois [16].

Soil physical properties

Soil resistance was measured using pocket penetrometer (Eijkelkamp Co., the Netherlands) [14]; soil texture was determined by the method of Gee and Buder [17]. Soil shear strength was also determined: the instrument was vertically placed in the soil and turned clockwise and the results were obtained on the basis of KPa (Fig. 4). Soil stability versus wind erosion was determined by the dry method [18] according to the following details. The meshes with the diameters of 2, 1, 0.425, 0.250, 0.106, and 0.05 mm representing the sieve numbers of 10, 18, 40, 60, 140, and 270, respectively, were used for the experiment according to the standards of ASTM. Fifty grams of soil sample were inserted on the sieves and were shaken for 1 min using a rotating sieve.

Fig. 4.

(A) The wind tunnel instrument, (B) and (C) Measurement of soil shear strength

Mean weight diameter (MWD)

MWD was determined according to the following formula [18].

xi: the mean diameter of the remaining aggregates on each sieve.

i: the mean diameter of the upper and bottom holes.

n: number of sieves.

wi: the ratio of the soil aggregate weights to the total soil weight following the deduction of sand and gravel weight using the following formula:

wi: the weight of remaining particles in the range of iw_(is).

w_(is): weight of sand and gravel in the range of i.

wt: soil oven-dry weight.

Geometric mean diameter (GMD)

GMD was determined using the following formula [18].

The parameters are according to the above-mentioned details.

The erodibility of surface soil

The erodibility of surface soil was determined by wind tunnel (produced by Isfahan Islamic Azad University), with an open circuit and a fan prepared for the desert. The fluctuations of wind rate on the soil surface were measured by the van Karman formula:

V1 and V2 are the wind rates in the initial and secondary heights, respectively; H1 and H2 are the wind initial and secondary height. Soil erosion with the average rate of wind including 13.9 and 25 ms^− 1 for a 20 cm-height in a five-minute period was investigated.

Statistical analysis

The data were subjected to analysis of variance using SAS and means were compared by least significant difference (LSD) at P ≤ 0.05.

Results

Analysis of variance

According to the analysis of variance, bacterial inoculation, days after inoculation and their interactions significantly affected soil shear strength, soil resistance, wind erosion at 50 and 90 kmh^− 1, MWD and GMD (P ≤ 0.01) (Table 2).

Table 2.

Analysis of variance indicating the effects of bacteria on soil physical properties

		Mean squares
	df	SSS	SR	WE50	WE90	MWD	GMD
Trt	1	139.876 **	5583.769 **	13935.879 **	75115.416 **	0.372 **	0.052 **
Rep	8	0.322	37.528	18.656	98.037	0.002	0.001
Day	3	7.218 **	593.863 **	502.329 **	3451.913 **	0.043 **	0.014 **
Trt ×Day	3	6.593 **	472.431 **	514.190 **	3359.056 **	0.035 **	0.007 **
Day×Rep	12	0.219 ns	19.482 ns	19.240 ns	83.659 ns	0.002 ns	0.002 ns
Error	12	0.227	13.590	14.176	38.980	0.003	0.001
R-Square		0.986	0.983	0.990	0.995	0.952	0.928

*P < 0.05; **P < 0.01; n.s., not significant (P > 0.05)

SSS: soil shear resistance, SR: soil resistance, WE50, and WE90: wind erosion at 50 and 90 km. h^− 1, respectively, MWD: mean weight diameter, GMD: geometric mean diameter

Exopolysaccharide (EPS)

Bacterial inoculation significantly increased (P ≤ 0.01) soil EPS in the depth of 0–1 cm. In the initial sample, EPS was equal to 0.061 mgg^− 1, which increased to 0.59 mgg^− 1 after 90 d. However, in the depth of 1–5 cm it was 0.036 mgg^− 1 (data not shown).

Soil physical properties

Soil shear strength significantly increased after a 90-d period at P ≤ 0.01 from 0.3 KPa in control to 5.7 KPa in the inoculated treatment (Fig. 5a). Bacterial inoculation significantly increased soil resistance from 1.5 KPa in control to 41 KPa after 90 d (Fig. 5b). The GMD of soil aggregates significantly increased from 0.3 mm in control to 0.5 mm after 90 day of bacterial inoculation (Fig. 5c). Similarly, bacterial inoculation significantly increased MWD of soil aggregates from 0.12 mm to 0.47 mm (Table 3; Fig. 5d).

Fig. 5.

Soil properties including: (A) shear resistance, (B) soil resistance, (C) GMD, (D) MWD, (E) wind erosion 50, and (F) wind erosion 90 affected by bacterial biocrust and time

Table 3.

Soil stability on the basis of MWD [19]

Stability class	MWD (mm)
Highly unstable	0.4
Unstable	0.4–0.8
Relatively stable	0.8–1.3
Stable	1.3-2.0
Highly stable	> 2.0

Wind erosion

Bacterial inoculation significantly decreased wind erosion (wind rate = 50 km. h^− 1) from 55.7 kgm^− 2 in control to 0.3 kg. m^− 2 after 90 d (Fig. 5E); similarly, for the wind rate of 90 kmh^− 1, bacterial inoculation significantly decreased wind erosion from 116. 42 kgm^− 2 to 0.6 kgm^− 2 (Fig. 5F).

Discussion

M. vaginatus is a cyanobacterial strain commonly found in Iranian deserts. Soil inoculation with this strain boosted its capacity to form biocrust, consequently improving soil physical properties. According to the results the EPS produced by cyanobacteria, M. vaginatus ATHK43, significantly improved soil physical properties, by the production of biocrusts. Fattahi el [20]. similarly found inoculation of soil by the two species of cyanobacteria including M. vaginatus and Nostoc punctiforme considerably improved soil physical properties and decreased wind erosion. Kheirfam and Asadzadeh [21] also found that cyanobacteria are able to significantly decrease wind erosion by the production of biocrust, exopolysaccharides and filaments. According to Hashim et al. [22] cyanobacteria are able to decrease wind erosion by enhancing soil erodibility factors. Water is one of the most important parameters for bacterial growth and activities, however, in water deficient conditions the cyanobacterial population becomes resistant to the stress [23, 24].

Soil cyanobacterial production of EPS enhances soil physicochemical and biological proprieties by increasing: (1) the bacterial resistance to biotic and abiotic stresses including drought, protozoa, and radiation [25], (2) the cohesion of soil particles by the production of biofilms, and (3) soil fertility [26, 27]. Soil shear strength significantly increased by cyanobacterial inoculation, which is due to the presence of higher organic C including EPS in the biocrusts strongly binding soil particles. The filaments of cyanobacteria may also improve the structure of the soil by binding the soil particles. In biocrust the increase of silt and clay, and the decrease of sand increases soil shear strength. The dominant particle of the experimental soil was sand, which cannot result in the formation of crust. Additionally, the biocrust produced by the bacterial population is much more resistant and can strongly bind the soil particles [28, 29].

The measurement of soil resistance is a fast and good method to determine the conditions for plant growth; the compaction of soil is accordingly measured by the use of the same method [14]. The critical rate of soil resistance for plant growth is 2000 KPa, above which plants would not be able to grow. So, according to our results, the produced biocrust is suitable for plant growth and can also control wind erosion [9].

The tested cyanobacteria can form biocrusts on the soil’s surface by trapping soil particles through the production of sticky EPS and their filaments [13]. The morphology of cyanobacteria controls the trapping of soil particles, and the morphology of biocrust control the accumulation of dust, and a higher surface roughness results in a higher dust accumulation [21, 30]. This indicates the important role of biocrust in the deposition of dust particles by dust trapping, accumulation and subsequent stabilization [31]. Cyanobacteria can trap particles by: (1) the network of cyanobacterial filaments, and (2) their tubular EPS, or (3) randomly attachment on the surface of cyanobacterial colonies. Such type of trapping was also observed by the researchers in the north of Iran [32]. Therefore, enhancing the soil trapping efficiency of cyanobacteria may require further investigation.

The erosion by the wind rates of 50 and 90 kmh^− 1 were completely stopped by the bacterial inoculation, which is due to the improved structure of soil by the bacterial EPS, filaments and other organic sources. In the soil with less than 2% of organic C, the stability of soil aggregates is compromised and as a result such types of soils are vulnerable to erosion. The cohesion of soil particles by EPS is due to the binding of hydroxyl, carboxyl and amine functional groups to the clay particles [29].

In the desert areas and due to the low rate of precipitation and subsequently little soil leaching, cyanobacteria might favour soil stability by forming biocrusts, which can even serve as a microenvironment for other organisms of the soil microbiota [33]. In water bodies, the formation of blooms due to anthropogenic pollution represent a urgent problem for human health and maintenance of ecological balance [34]. Although mutualistic interactions between cyanobacteria and other soil microbes have been reported in the literature, competition and other detrimental ecological interactions require further scientific investigation [35].

Conclusion

The identified and tested cyanobacteria, Microcoleus vaginatus ATHK43, was able to decrease wind erosion by enhancing soil physical properties including soil shear strength, soil resistance, and aggregate stability including mean weight diameter and geometric mean diameter. This occurred since cyanobacteria produce exopolysaccharides (EPS) capable of binding soil particles. The resulting biocrust enhances soil resistance and alleviate the unfavorable effects of wind erosion and the subsequent aerosols emission. According to the results, after a considerable period of time after inoculation, cyanobacteria produced significantly higher EPS, and enhanced soil physical properties. There is an acclimation period for cyanobacteria to properly grow in the soil environment for N fixation and biomass production as the main sources of carbon and nitrogen. The use of cyanobacterium M. vaginatus ATHK43 is advised for enhancing soil physical properties, because it mitigated wind erosion and dusting emission. However, more research is essential to indicate the optimum conditions, which may enhance the efficiency of cyanobacteria for producing EPS and reducing soil erosion and dusting emission. The future research prospects that arise from this study may investigate the tested cyanobacteria for stimulating plant growth, which can be used for enhancing soil stability and reforestation projects in arid sites similar to deserts. The presence of cyanobacteria in the soil can create a microenvironment that can host a diverse microbial community, improving nutrient cycling and producing specialized metabolites of interest. Enhancing soil trapping efficiency through cyanobacterial biocrusts also require further investigation by testing other strains and soil types.

Author contribution

AK conducted the experiments, collected and analysed data, AT supervised the research, and wrote the first draft, MH co-supervised the research.

Funding

There was not any funding for the present research.

Data availability

All avaible data have been presented in the manuscript.

Declarations

Conflict of interest

The authors declare they do not have any conflict of interest.