Cyanobacteria and
biocrusts communities restore degraded soil: Examples of IranAtoosa Gholamhosseiniana and Adel
Sepehra,b
Dept. of Desert and Arid Zones Management, Ferdowsi University of
Mashhad (FUM), Mashhad, IRAN
Head of Research Department of Environmental Hazards Management and
Ecosystem Management, Ferdowsi University of Mashhad (FUM), Mashhad,
IRAN
adelsepehr@um.ac.irAbstractSoil is the major natural resource on which human life depends for the
production of food, feed, fiber, renewable energy and raw materials, as
well as the protection of the planet’s natural ecosystems and climate
system. Increasing soil degradation and subsequent ecosystem degradation
is a current concern in the hyper-arid areas. Soil degradation has
created many challenges for residents of arid and semi-arid regions of
Iran. The use of new technologies such as biological crusts has provided
great hope for the recovery and restoration of degraded ecosystems.
Inoculation of biological crusts, especially cyanobacteria, has had
positive results in improving soil conditions and restoring degraded
soils. In this article, has been introduced the bio-crusts communities
considering cyanobacteria species to restore degraded soils. We reported
the results of cyanobacteria applications in soil conservation in arid
environments of Iran.Key words: biological soil crusts, cyanobacteria, inoculation,
soil degradation, soil restoration1. IntroductionIndiscriminate human interference in the exploitation of nature and the
environment will have numerous consequences. The growing need of the
population for food has put a lot of pressure on the ecosystem,
especially in arid and desert areas. Soil resources especially in arid
and semi-arid regions are rapidly degraded and polluted (Oldeman et al.,
1990). Today, soil degradation in arid and semi-arid regions is
recognized as a serious and widespread problem. Soil degradation is
defined as the loss and reduction of soil yields, which in recent
decades has become a serious problem in the world and a threat to the
ability to produce agricultural products and human life (Chisholm and
Dumsday, 1987). Increasing soil degradation and subsequent ecosystem
degradation is a current concern in agriculture and the environment
(Scherr, 1999; UNEP, 1997). Soil degradation poses many challenges to
feed the world’s growing population.
In arid areas, soil degradation is referred to as desertification
(Blaikie and Brookfield, 2015). 75% of Iran’s area is covered by arid
and semi-arid areas. Human and geographical factors have led to an
increasing trend of soil degradation in Iran. Soil degradation processes
in Iran have created many challenges. Therefore, the use of effective
methods in soil conservation and restoration is essential. The use of
biological crusts is expanding as restoration of degraded soils as well
as protection against erosion and degradation. Moss, lichen and
cyanobacteria are classified as biological soil crusts (BSCs). Mosses
have organs similar to stems, leaves and rhizoids, have a relatively
high photosynthetic capacity and are similar to plants (Giuliani et al.,
2020). Cyanobacteria and algae, which usually act as pioneers in desert
soil, are low-growing plants with low photosynthesis (Chaplot, 2021).
Lichens are a collection of algal cells that are covered in epiphytic
mycelium and can withstand very dry environments (Goiris et al., 2012).
These organisms are characterized by different physiological
characteristics and require different conditions for rapid growth,
resulting in the complexity of artificial repair for each type of BSCs
(Scherr, 1999).
From the beginning of the twentieth century, the use of compounds
extracted from cyanobacteria and green algae has been considered by
farmers (Taddese, 2001). At that time, most attention was paid to the
role of cyanobacterial products in increasing the quality of products,
increasing production, reducing plant stress, and so on (Kovda, 1983).
Over time and increasing pressure on the soil, soil erosion and
destruction also increased, and this issue led to special attention to
the role of these crusts in soil conservation and restoration (Buringh,
1981).
In this study, we have tried to investigate the role and importance of
biological crusts in soil regeneration in arid and semi-arid regions of
Iran and examples of the use of these shells in Iran are given. Areas in
which a combination of factors such as wind and water erosion, soil
salinization, loss of fertility and soil quality, declining groundwater
levels, migration, poverty, etc. have led to obvious signs of
desertification.2. Soil restorationEcosystem restoration has become an important goal of environmental
protection and international policy (Zhao et al., 2013). Ecosystem
restoration means that plants, microorganisms, soil, and even higher
levels of nutrition, such as animals, are targeted for restoration
(Giraldo-Silva et al., 2019).
Soil restoration in degraded arid and semi-arid soils faces many
challenges due to long periods of drought and irregular rainfall
(Berdugo et al., 2020). Most arid and semi-arid regions are exposed to
large-scale human disturbances, including overgrazing, severe fire
processes, the use of chemical fertilizers to raise productivity, and
mining (Bateman and Mooz Noz-Rojas, 2019). In recent years, several new
strategies have been adopted to overcome these challenges and revitalize
these ecosystems, including the use of amendments (Luna et al., 2018) or
inoculation of soil microorganisms (Moreira-Grez et al., 2019). In
recent years, research has shown promising potential for the effects of
these organisms on restoring soil fertility and preventing water and
wind erosion (Chamizo et al., 2017, 2018; Rossi et al., 2017).
Cyanobacteria are prokaryotes that, thanks to their characteristics such
as high UV tolerance, soil salinity, drought, high temperature, etc.,
can be established in many damaged and critical environments (Adessi et
al., 2018). Cyanobacteria as the initial crust and one of the most
important microorganisms in biological crusts play an important role in
ecological, hydrological and biogeochemical processes
(Rodríguez-Caballero et al., 2018; Gholamhosseinian et al., 2020).
Cyanobacteria are the best choice for soil regeneration due to their
high resistance in poor environments, against intense UV radiation and
exopolysaccharide production, as well as rapid growth and multiplication
(Rajeev et al., 2013; Lan et al., 2015).2.1 The importance of biological crusts 2.1.1 Improving the physical and chemical properties and soil
ecosystemThe presence of unique features in biological crusts has made it
possible for them to live in harsh environments (Markou et al., 2014).
For example, algae live in different environments such as fresh water,
salt water of the sea and oceans, snow, rocks and on the surface of
plants and animals (Maestre et al., 2011). The algae Oscillatoria
Brevis, Scytonema elongates, Heterhormogonium, can withstand
temperatures up to 70 ° C, which is why they are found in abundance in
tropical and desert soils. Many algae are able to withstand sunlight and
only slow down when they are exposed to strong light conditions (Zhang
et al., 2016). Many green algae are found in a wide range of pH but have
the highest growth and yield at neutral or alkaline pH (Bilgrami and
Saha, 2004; Heidarpour et al., 2019). After death and decomposition of
these microorganisms, organic matter is added to the soil and after a
few years, it enriches the soil and makes it suitable for cultivation.
Cyanobacterial play an important role in soil physicochemical properties
(Thajuddin and Subramanian, 2005; bashtian et al., 2019; sepehr et al.,
2019; Gholamhosseinian et al., 2020) (Fig. 1).
[Fig. 1]
In recent years, inoculation of cyanobacteria into the soil due to their
vital role in the ecological cycle (Brown et al., 2019; Gholamhosseinian
et al., 2020), such as The redistribution of precipitated rainwater;
dust capture and use of airborne, interaction with vascular plants; and
enhancing the soil physical structure and stability(Fig. 2), reducing
the wind and water erosion, increasing nutrients accessibility,
increasing the roughness of the surface, so enhancing dust trapping
capacity (Fearnehough et al., 1998; Belnap and Lange, 2003; Warren et
al., 2019; Weber et al., 2016); improving the essential nutrient
concentration in plants (Belnap and Harper, 1995), enhancing nitrogen
and carbon fixation rate (Evans and Lange, 2001; Yang et al., 2014;
Madsen et al., 2016), so, increasing the mineralization and
bioavailability rate of nitrogen (Delgado-Baquerizo et al., 2013; Hu et
al., 2015); thus, biocrusts nutrient enrichment has important role in
soil fertility and nutrient bioavailability. Therefore, has become one
of the most promising biotechnology strategies to restore soil
performance in degraded arid and semi-arid areas have become (Lal, 1995;
Lutz et al., 1996; Eswaran, 1999; Muñoz -Rojas et al., 2018a). Xie et
al., (2007) found that by inoculating cyanobacteria into the soil and
conducting a 3-year study, these shells with 70% coverage in the soil
and penetration to a depth of 0.5 mm could have long-term positive
effects on soil stability. In Figure 3, you can see the difference in
the structure of soil particles in the presence and absence of crusts
(Semi-arid regions in eastern Iran).
Increased roughness, albedo and trapping of airborne particles are other
well-known features of these crusts (Chamizo et al., 2016;
Gholamhosseinian et al., 2020). Adessi et al, (2018) in an experiment
showed that by removing the exopolysaccharides of cyanobacteria from the
soil, the water holding capacity was reduced by up to 80%.
[Fig.2]
[Fig. 3]2.1.2 vegetation establishment, seed germination These microorganisms can lead to optimal plant growth (Condon and Pyke,
2018; Havrilla et al., 2019); These shells may act as armor-like
barriers to seed, but if seeds can be successfully created, the presence
of biological shells can increase seedling growth rate (Ferrenberg et
al. 2018; Slate et al., 2019). Research has shown the positive effect of
cyanobacteria on germination and grain growth of wheat and rice
(Muñoz-Rojas et al., 2018).
In addition, the use of cyanobacteria on the seeds can be a useful tool
for inoculation into the soil after germination (O’Callaghan, 2016).
Soaking the seeds in cyanobacterial suspension in addition to rapid seed
germination and better seedling growth provides favorable conditions for
inoculation of cyanobacteria into the soil (Gupta and Lata, 1964;
Mahmood et al., 2016). The ability of cyanobacteria as a biological
initiator to regenerate soil in an arid region of Western Australia was
investigated, and the results showed that cyanobacteria due to their
high protein content have positive effects on native plant growth and
improved soil substrate characteristics (Flemming and Wingender, 2010).
Cyanobacteria can be used as biological controllers against fungi and
bacteria harmful to plants (Sing et al., 2016) and also capable of
producing plant growth regulating hormones (PGR) (Venkataraman, 1981)
and gibberellin (Shen-Rui and Shen, 1997) and organic acids (Hellebust,
1974). Studies have shown that the use of cyanobacterial extract
increases plant growth (Offer et al., 1992) and controls fungal damping
disease (Caire et al., 1976). The use of cyanobacteria is recommended to
increase seed germination as a biological fertilizer and to increase the
growth of many plants (Strick et al., 1997). Due to these
characteristics, their high dispersion and establishment in any
environment, cyanobacteria can be used as a potential tool for soil
repair in arid areas (Rossi et al., 2017).2.1.3 Application of EPS production in improving soil properties
and soil stabilityOne of the reasons for the importance of cyanobacteria in the
restoration of degraded soils is the synthesis of Extracellular
polymeric substances (EPS), which are called the most vital chemicals
produced by these microorganisms. These polysaccharides play an
important and vital role in improving soil physicochemical parameters
(Weber et al., 2016). These polysaccharides form a protective layer
around the cells called the capsule (De Philippis and Vincenzini, 1998);
that protects the cell under drought stress (Costa et al., 2018).
Studies have shown that another important role of the EPS matrix is the
aggregation capacity of soil particles, which improves soil structure
and soil fertility (Boonchai et al., 2014).
These polymers can improve soil quality, health, fertility and structure
(Hwang et al., 2004; Escribano et al., 2009). EPS is produced to protect
the cell under environmental stresses such as salinity, pH changes,
drought, temperature changes, etc. (Wingender et al., 1999). It also
protects the cyanobacteria from the negative effects of heavy metals and
antimicrobial chemicals by creating a layer around them, as a result, it
allows cyanobacteria to survive in very harsh conditions where other
microorganisms are unable to survive. EPSs are important for improving
soil quality because they trap nutrients and make the environment
suitable for chemical reactions. As EPS increases the ability of soil
particles to accumulate, it can increase soil nutrients.3. Examples of research experiences and use of biological crusts
(considering cyanobacteria) in IranThe location of Iran in the arid region and the increasing
desertification process in this country has multiplied the importance of
soil protection and soil restoration. Decreased soil quality and health,
increased dust storms, reduced crops, increased migration, poverty,
unemployment, etc. are all consequences of increasing soil degradation
and desertification. In this section, we have tried to give examples
about the use of biological crusts, especially cyanobacteria in arid and
desert areas of Iran, as an effective solution to solve the mentioned
problems.
Sepehr et al., (2019) With a study in a semi-arid region located in
eastern Iran examined the importance of EPS in soil stability. The
results of this study showed that the genera Microcoleus sp,scillatoria sp, Leptolyngbya sp and Phormidium sp are
among the dominant species in arid regions of Iran and among these two
species Oscillatoria splendida and Oscillatoria tenuis had
the highest tolerance to soil salinity. The EPS secreted by these
cyanobacteria increases the stability of the aggregates and reduces the
dispersion at the soil surface. Hassanzadeh Bashtian et al., (2019) by
examining the relationship between soil parameters and the development
of biological crusts showed that crusts have an effective role in
increasing organic carbon, nitrogen, calcium carbonate and reducing
salinity and sodium in soil. Gholamhosseinian et al (2020) also reached
this conclusion by studying the biological crusts in the semi-arid
region of Iran; The presence of crusts in the soil helps to improve the
chemical and physical conditions of the soil and also increases the
diversity of soil minerals by affecting the geochemical processes of the
soil and the deposition of dust.
Due to the known roles of cyanobacteria, soil inoculation with
cyanobacteria has been proposed as a sustainable technology to improve
soil quality and control and regenerate degraded soils in arid and
semi-arid regions (Rossi et al. 2017). Cyanobacteria are able to retain
more water in the soil and store moisture by secreting
exopolysaccharides, in lichens and mosses, this role is played by
filaments (Fig. 4).
[Fig. 4]
The study of biological communities in these saline soils south of the
Caspian Sea showed that these biological crusts have positive effects on
increasing soil quality. These effects include increasing nitrogen,
phosphorus, copper and iron and decreasing pH, sodium, sodium adsorption
ratio and percentage of exchangeable sodium compared to crustless soils
(Jafari et al., 2004; Kakeh et al., 2018; Bashtian et al., 2019). Also,
the presence of these biological crusts leads to increased infiltration
and soil moisture (Kakeh et al., 2018).
Deposition of non-rainfall water in arid and semi-arid regions is of
great importance. Maintaining moisture is very important for the
survival of vegetation and maintaining water balance in these areas. In
the desert areas of Iran, the lack of vegetation leads to a decrease in
moisture and water loss through evaporation and transpiration, as well
as runoff. Therefore, the role of biological shells to solve this
problem is of particular importance.270 samples containing cyanobacteria
were tested under artificial rainmaker compared to the control sample.
Samples with cyanobacterial crust had higher permeability and less
runoff production and also reduced soil salinity (Kakeh et al., 2020).
In addition to soil surface, these crusts also affect soil properties,
so they play an important role in conservation, restoration and
rehabilitation soils in arid and semi-arid regions.
Dust storms are a common phenomenon in desert areas. In recent years,
the intensity and frequency of these storms have increased sharply in
Iran (Cao et al., 2015). The problems of sandstorms in Iran cause a lot
of damage to agricultural products every year and create problems such
as migration and poverty (Khusfi et al., 2020). Inoculation of
cyanobacteria can be an effective solution to this problem. In
northwestern Iran, two species of Nostoc sp. andOscillatoria sp. were obtained from the dry bed of the river.
After inoculating cyanobacteria, sandy soils were tested in a wind
tunnel at a speed of 72 km / h. The presence of cyanobacterial filaments
among the sand particles caused the particles to coalesce and reduced
wind erosion by 96.6% (Kheirfam and Asadzadeh, 2020). A study was
conducted to evaluate the success of cyanobacterial inoculation in
reducing runoff in a large-scale degraded land with natural rainfall in
northwestern Iran. The results showed that inoculation of two species ofNostoc sp. and Oscillatoria sp in soil reduced 57-32% of
runoff (Fig 5). Also, roughness and stability index did not show
positive results (Sadeghi et al., 2020). A study in northern Iran showed
that inoculation of cyanobacteria into degraded soils after 60 days
showed a significant difference in chemical parameters such as carbon
and nitrogen (Kheirfam et al.,
2017). Biological crusts and sediments were collected from the loess
plateau of Northern Iran. Cyanobacterial diversity and grain
stabilization were studied by light and scanning electron microscopy.
The results reported in this study confirm the integral role of
cyanobacteria in the formation of loess. EPS layers and cyanobacterial
filaments enclosing fine and coarse soil particles, respectively. This
is the first step in loess formation (Dulić et al., 2017). The formation
of loess prevents the dispersion of clay particles.
Many pests cause a lot of damage to Iranian farms every year. The use of
chemical pesticides also has its disadvantages and leads to chemical
contamination in the soil and endangers the health of the soil. The use
of cyanobacteria as a killer of bacteria and pathogenic fungi is a
completely harmless process and is also useful for improving the quality
and health of the soil. In order to find the potential of cyanobacteria
for the production of antibacterial and antifungal compounds in rice
fields in northern Iran, 150 strains of cyanobacteria fromHapalosiphon sp, Fischerella sp, Stigonema sp, Nostoc spwere isolated and studied. The results of this experiment showed that
the genera Hapalosiphon sp, Fischerella sp, Stigonema sp have the
greatest effect on antifungal and bacterial activities as well as
reducing lead in the environment (Ghasemi et al., 2003). The combination
of Tjipanazoles obtained from Tolypothrix tjipanensis also showed
significant fungicidal effects against wheat blight, rice blast and leaf
rust (Borowitzka, 1995). Another study of 76 species of cyanobacteria
found that 17 species, generally from the four families Nostocaceae,
Stigonemataceae, scillatoriaceae and Chroococcaceae, had antibacterial
effects (soltani et al., 2005).
The use of chemical fertilizers to increase yields may be effective at
first, but over time it leads to pollution and degradation of soil and
the environment. In recent decades, the use of cyanobacteria to increase
seed germination rate, seedling establishment and increase crop growth
has been widely used. Shriatmadari et al., (2013) in order to
investigate the effect of blue-green algae on crop growth, the dominantAnabaena sp. and Nostoc sp. were identified and isolated
from paddy soils. After 40 days of inoculating the algae extract into
the potting soil, the parameters of root length, fresh and dry weight of
the plant, number of leaves and plant height were measured. Liquid
chromatography confirmed the production of plant growth stimulants such
as phytohormones and the results showed a significant difference
compared to the control.
[Fig. 5]4. ConclusionThe interaction between biocrusts and soil is very important and good
awareness from that help to better manage soil specially in arid and
semi-arid areas. New techniques for soil restoration in arid area are of
particular importance. Successes in inoculating cyanobacteria in the
soil could provide a new perspective on ecosystem restoration in Iran.
Numerous studies for inoculation of cyanobacteria as an artificial
induction strategy in the fight against desertification and
rehabilitation of degraded soils (Evans et al., 1999).
Given the properties of biological crusts, especially cyanobacteria, the
idea of adding them to the raw material to increase soil stability and
reduce losses due to water and wind erosion seems to be useful. Research
into BSC inoculation, especially the use of cyanobacteria, has made
great strides so far. cyanobacteria have successfully been inoculated in
soils under laboratory conditions (Issa et al., 2007;
Mu~noz-Rojas et al., 2018b) and in local field settings
(Chen et al., 2006; Wang et al., 2017). For countries located in very
hyper-arid, such as Iran Like Iran, using these biological crusts for
soil restoration can be considered a very useful and efficient
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Fig. 1 Fig.
2Fig. 3Fig. 4Fig.
5Caption of Figures:Figure 1. The schematic shows that many ecosystem processes are
affected by the presence of biological crustsFigure 2. In Figures A, B, and D, you can see that the presence
of crusts has led to the accumulation and strength of the soil. The
pictures c and e also show the interconnection of soil particles in the
presence of lichensFigure 3. Above images show an arid region in eastern Iran
including a surface without biological crust cover (a) and at the right
side a surface with biological crusts (b). Images of c and d show the
electron microscope (SEM) of these surfaces which involves coarse
particles in image c with little coherence and presence of
polysaccharide and cyanobacterial filaments surround the conducting
particles in image d.Figure 4. (a) cyanobacterial colonies on the soil surface
before rain and (b) cyanobacteria during rainfall by water absorption
have formed a protective layer on the soil surface and (c) microscopic
image of soil particles surrounded by cyanobacteria and (d) Formation of
fine soil structures by cyanobacterial filaments. (Kheirfam et al. 2020)Figure 5. Electron microscope images a) Cyanobacterial
filaments extracted from soil b) - Soil particles among polysaccharide
filaments c) Polysaccharide filaments of cyanobacteria (red circle) hold
soil particles together d) Close view of a polysaccharide filaments. The
red arrow indicates fine soil particles