Abstract
Desert ecosystem is generally considered as a lifeless habitat with extreme environmental conditions although it is colonized by extremophilic microorganisms. Cyanobacteria, microalgae, and bacteria in these habitats could tolerate harsh and rapidly fluctuating environmental conditions, intense ultraviolet radiation, and lack of water, leading to cell desiccation. They possess valuable metabolites withstanding extreme environmental conditions and make them good candidates for industrial applications. Moreover, most natural microorganisms in these extreme habitats exist as consortia that provide robustness and extensive metabolic capabilities enabling them to establish important relationships in desert environments. Engineering of such consortia of cyanobacteria, microalgae, and bacteria would be functional in the sustainable development of deserts through improving soil fertility, water preservation, primary production, pollutant removal, and maintaining soil stability. Modern tools and techniques would help in constructing highly functional cyanobacterial/microalgal–bacterial consortia that are greatly useful in the establishment of vegetation in deserts as well as in biotechnological applications.
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Introduction
Desert soils have been considered economically insignificant, and the study of desert microbial diversity and their characteristics has therefore been neglected. However, since last few decades, the reduction in fertile lands because of rapid urbanization and increasing the world’s demand for food has necessitated the use of arid areas for agricultural purposes. Consequently, biological and environmental researchers are closely examining desert soils for microbiota useful for agricultural productivity of such lands (Moreno et al. 2008). The 1992 Earth Summit heard that more than 40% of the earth’s terrestrial area is in danger of desertification (Bhatnagar and Bhatnagar 2005). Deserts are characterized by extreme conditions such as high temperature, low moisture, and low availability of organic matter content, all influencing the composition of microbial communities and their activity in desert soil (Belnap et al. 2005; Saul-Tcherkas et al. 2013). Most studies suggest that deserts and desertified lands have scarce vegetation, but the surfaces of these landscapes are covered by microphytic communities such as microalgae, cyanobacteria, fungi, and bacteria in different combinations (Garcia-Pichel et al. 2001; Drees et al. 2006; Gómez-Silva et al. 2008; Sterflinger et al. 2012). Friedmann (1980) shows the microbial composition of desert soil and their physiology.
Cyanobacteria, microalgae, and bacteria have high potential to adapting extreme environments. Azua-Bustos et al. (2012) identified unrelated phototrophic microalgae of Cyanidiales and Dunaliella, and cyanobacteria such as Chroococcidiopsis from the coastal range of the Atacama Desert, and illustrated the convergent evolution of microalgae and cyanobacteria to survive in the desert environment. Dunaliella or Chroococcidiopsis have different survival mechanisms adapted to their respective habitats. On the other hand, the same mechanisms help in surviving ionic stress (caused by salt) and osmotic stress tolerance (caused by desiccation). Dunaliella biofilms colonize spider webs in deserts as a means of using condensed water for their survival. Very recently, Abinandan et al. (2018) critically examined the nature of mutualistic interactions established between microalgae and bacteria in biofilms of acid mine drainage for the removal of metals and consequent yield of biofuel from biomass.
In view of the fact that microalgae and bacteria have great potential for removing organic pollutants (Subashchandrabose et al. 2012; Subashchandrabose et al. 2017a) and toxic metals (Bahar et al. 2013) from contaminated soils, they serve as biomarkers for soil toxicity evaluation (Megharaj et al. 2011a; Subashchandrabose et al. 2015; Subashchandrabose et al. 2017b). Furthermore, these microorganisms could be used for agricultural purposes as nutrient sources (Megharaj et al. 1992). Studying interactions between cyanobacteria, microalgae, and bacteria even in desert soil is therefore useful in their biotechnological applications (Amin et al. 2015; Fuentes et al. 2016). This includes using consortia comprising cyanobacteria, microalgae, and bacteria, from desert habitats for bioremediation of oil-polluted dessert soils since higher temperatures improve both solubility and bioavailability of hydrocarbons (Margesin and Schinner 2001). In these habitats, microbial consortia are also capable of producing high-value products with a significant impact in areas like agriculture (Moreno et al. 2008) and environmental management (Margesin and Schinner 2001). However, there is no published information on the possible implications of desert microorganisms, especially consortia of cyanobacteria/microalgae and bacteria, in bioremediation of polluted environments and use of their metabolites for industrial applications. The present review provides a detailed account on the environmental and biotechnological significance of cyanobacteria/microalgae–bacteria consortia in desert soils with a critical view as to how they could be exploited in improving the vegetation of drylands as a solution for the scarcity of usable lands.
Significance of desert soils
Deserts are characteristic in an annual rainfall lower than 254 mm. Consequently, biological activities in desert ecosystems rely on transitory water available. On the other hand, availability of water depends on abiotic factors such as temperature, declines in pan evaporation, geology, wind and interactions with precipitation inclusive of rainfall (Bhatnagar and Bhatnagar 2005). Based on the water availability, United Nations Convention to Combat Desertification (UNCCD) defined four dryland regions that include arid, semiarid, dry sub-humid, and hyper-arid deserts (Table 1). Generally, hyper-arid regions are biologically unproductive whereas the semiarid regions are well vegetated. Arid regions occur in between those two zones (Neilson et al., 2012). Deserts are broadly classified as hot and cold deserts, which are located in Arctic and Antarctic regions with limited rainfall and cold temperature (Ward 2016).
Most deserts are mainly located within two belts along the equator and the tropics of Cancer and Capricorn. Within the arid belt of Northern Hemisphere includes the Arabian, Iranian, Sahara, Gobi, Central Asian, and North American Southwest deserts while Southern Hemisphere includes with Kalahari, Namib, Peru, Chile, and Australian deserts. Flashing floods occur in deserts rarely by higher rainfall (> 250 mm). However, this water is not accessible to desert organisms because of non-absorption into the desert soil and surface run-off. Although some cold deserts obtain water as snow or ice, this water is also not available for vegetation (Ward 2016). Most of the studies indicate that the area of the desert would be increased because of the global warming resulting from fossil fuel combustion and industrial pollution (Brown et al. 1997; Rosenfeld 2000). Global warming results in higher evaporation in arid regions (Xu et al. 2016) and rapid loss of nitrogen from soil, thereby limiting microbial growth (Holmes et al. 1994).
Usually, deserts lack vegetative cover including higher plants. However, specialized microorganisms including cyanobacteria, microalgae, fungi, and many heterotrophic bacteria colonize few millimeters of top soil layers (Mazor et al. 1996; Garcia-Pichel et al. 2001; Nagy et al. 2005). These biological soil crusts (BSC) provide surprising capabilities for deserts to avoid desiccation and survive from extreme conditions such as high temperatures, low nutrient levels, high summer UV radiation, physical instability caused by strong winds, high pH, and high salinity (Bowker et al. 2005; Belnap et al. 2007; Chamizo et al. 2013). These organisms are essential in enhancing soil fertility and stability (Abed et al. 2010; Wierzchos et al. 2015; Ward 2016). Majority of deserts have spatial variations of their soil types and shifted habitats with unique vegetative forms creating through the dune systems and high salinity (Abed et al. 2015). Nutrient such as nitrogen limitation in the soil causes less vegetation in most deserts (Hadley and Szarek 1981; Gallardo and Schlesinger 1992). Most limiting nutrient in the Australian deserts is phosphorus, while Africa’s Namib and Kalahari deserts have lower nitrogen, phosphorus, and potassium content (Grimm et al. 1981; Robinson 2001).
Soil type in the deserts could be varying according to the region or climatic conditions and affects for microbial composition. The sand deserts are not generally accounting for 15–20% of the total number of deserts (Robinson 2001). Deserts mainly with minerals and low organic matter contain saline soil (Goudie and Middleton 2006). Furthermore, Fierer and Jackson (2006) demonstrate that soil in tropical forests with acidic pH has lesser bacterial taxa compared to the desert with neutral pH. Denaturing gradient gel electrophoresis (DGGE) analysis showed that Atacama Desert has a microbial composition, which can grow in hypersaline habitats (de los Ríos et al. 2010). The imperfectly developed wide range of unidentified bacteria and fungi exists in the hyper-arid polar desert (Pointing et al. 2009). All these studies illustrate unique and extraordinary microbial diversity related to desert soil.
Cyanobacteria and microalgae in desert soils
Compared to other biological species, microalgae and cyanobacteria are highly adaptive to specific environments due to their ability to survive at high temperatures, low water potential, and radiation. Also, their ability to grow as autotrophs, heterotrophs, or mixotrophs makes them as good colonizers on different ecosystems such as deserts (Subashchandrabose et al. 2013). Cyanobacteria are mainly contributing to biological crusts in deserts encouraging soil fertility regarding nitrogen and carbon fixation. The requirement of the small wet period for their metabolic functions makes them good candidates for desert soil (Belnap 2003b). Most cold deserts in Colorado Plateau are dominated by cyanobacteria, Microcoleus vaginatus, resulting in nitrogen fixation (Belnap 1996; Belnap 2003a).
Earlier, the scientists said that desert crusts represent a limited number of microalgae because their results mainly relied on light microscopic observations (Metting 1981). However, recent researches on different stages of zoospores and gametes along with the features on crust structure and functions show a wide range of desert algae (Lewis and Flechtner 2002; Lewis and Flechtner 2004). Phycologists use accurate methods such as nuclear 18S rDNA genes and plasmid-borne ribulose bisphosphate carboxylase gene to identify and develop systematic relationships of desert algae (Cardon et al. 2008). Redfield et al. (2002) demonstrate cyanobacterial composition and their relative abundance of different soil crusts present in Colorado Plateau arid desert using terminal restriction fragment analysis (TRF) following 16S rDNA sequence. Most frequent algal species in Baja California and Mexico deserts are Nostoc commune and Schizothrix calcicola (cyanobacteria), Myrmecia astigmatica (chlorophyte), and diatoms such as Hantzschia amphioxys, H. amphioxys f. capitata, Luticola cohnii, L. mutica, and Pinnularia borealis var. scalaris, and novel strains of Cylindrocystis brebissonii var. deserti var. nov., Elakatothrix obtusata sp. nov., and Fasckulochloris mexicana sp. nov. belonging to 32 genera (Flechtner et al. 1998). Lewis and Lewis (2005) demonstrate five classes of desert algae originating from freshwater ancestor using phylogenetic analysis based on 18S rDNA. Thus far, more than 400 species of microalgae have been identified from deserts throughout the world.
Some cyanobacteria exhibit specific changes in their morphology and physiology while surviving in desert habitats. For example, Nostoc commune var. flagelliforme, popularly known as a Chinese food delicacy (Gao 1998), has specific geometry in its colony and different protein pattern which makes the cyanobacterium a good survivor under desiccation. Such cyanobacteria excrete a novel protein WspA that hydrolyses the backbone of exopolysaccharides (EPS) and enhances expandability of cell wall, thereby helping in strengthening cell wall by incorporating and binding EPS molecules for the overall survival under desiccation (Liu et al. 2017). In desert environments, photosynthesis efficiency in cyanobacteria is reduced, and assimilation process limited due to decreased water availability. Therefore, the rate of nitrogen fixation under these conditions is very low in order to conserve energy because dinitrogenase utilizes more energy (Scherer and Zhong 1991). Interestingly, nitrogenase activity increases with the availability of water and starts declining after some time because the enzyme is more sensitive to temperature at this stage of wetting (Gao 1998). Some strains of cyanobacteria such as N. flagelliforme also develop biological soil crusts using sand particles to control desertification (Chen et al. 2011).
Biochemical components of these cyanobacteria such as secondary carotenoid complexes also change due to harsh conditions such as excessive light, nutritional stress, oxidative stress, and UV radiations (Zakar et al. 2016). Carotenoid composition and content vary with the depth of desert layers for harvesting light conditions and surviving from above conditions (Vítek et al. 2017). These stress tolerance mechanisms in desert microorganisms produce industrially valuable products which take attention of biotechnologists (Poong et al. 2018). Thus, the valuable metabolites produced by several cyanobacteria support desert microorganisms to survive and make them serve as soil improvers and produce industrially important components (Table 2).
Bacteria in desert soils
Bacterial population in desserts could vary throughout the world from < 10 to 1.6 × 107 in deserts of Atacama and Nevada, respectively. Gram-positive bacteria are more prominent, and their population does not decline considerably even in summer. Prominent bacteria of deserts include coryneforms such as Cystobacter, Archangium, Myxococcus, and Sorangium, and other forms like Bacillus, Acinetobacter, Micrococcus, and Proteus (Bhatnagar and Bhatnagar 2005). DGGE profile of the bacterial population in an Atacama Desert is dominated by phyla of Gemmatimonadetes and Planctomycetes (Drees et al. 2006). Real-time quantitative PCR demonstrates the high abundance of Deinococcus and Rubrobacter performing tolerance against radiation and desiccation in hyper-arid polar desert in Antarctica (McMurdo Dry Valley) (Pointing et al. 2009). These desert bacteria have tolerance against gamma and UV radiations. For instance, the strength of ionization radiation affects bacterial community growing in non-arid and arid soil from Louisiana forest and Sonoran desert respectively. Bacteria dominated by Deinococcus, Geodermatophilus, and Hymenobacter from arid soil survive at 30 kGy whereas none of the bacteria from non-arid soil survives at the dosage greater than 13 kGy (Rainey et al. 2005). Thermostable enzymes are contributing their survival under harmful conditions. A novel esterase was found from Escherichia coli isolated from Antarctic desert soil, and it tolerates high pH including an optimum activity at 9.0 and broader temperature range of 7–54 °C including an optimum temperature of 40 °C (Heath et al. 2009). Thus, desert bacteria could be an excellent source of valuable enzymes and metabolites for industrial applications such as melanin using for sunscreens (Gabani and Singh 2013).
Consortia of cyanobacteria, microalgae, and bacteria in desert soil crusts
The association between cyanobacteria and microalgae with other aerobic or anaerobic microorganisms that exist as microbial flocks in a community is known as a consortium (Mouget et al. 1995; Munoz and Guieysse 2006; Megharaj et al. 2011b; Subashchandrabose et al. 2011). This interaction could be either mutualism or parasitism (Martin et al. 2014; Fuentes et al. 2016). Under mutualism, the relationship between microalgae and bacteria facilitates the exchange of micronutrients such as vitamin B12 (Croft et al. 2005) as well as macronutrients like organic carbon, phosphorous, and nitrogen (Teplitski and Rajamani 2011; Cho et al. 2015). For instance, Chlamydomonas reinhardtii uses vitamin B12 supplied by heterotrophic bacteria for the exchange of photosynthate of alga (Croft et al. 2005; Kazamia et al. 2012). Bacteria enhance algal growth by excreting various hormones that change the bioactivities of both partners (Teplitski and Rajamani 2011). In the parasitism, some heterotrophic bacteria secrete chitinases, glucosidases, cellulases, and other enzymes to degrade algae within the consortium acquiring nutrients (Fergola et al. 2007; Kim et al. 2007; Xue et al. 2018). Some bacteria produce NH2OH along the conversion of ammonium into nitrite, which inhibits the growth of Chlorella sp. (Baumgarten et al. 1999).
Sediment particles of ice in deserts such as McMurdo Dry Valleys in Antarctica act as a source of inorganic and organic nutrients for the enrichment of cyanobacterial/microalgal−bacterial consortia with enhanced photosynthesis, N2 fixation, and organic matter decomposition. Microautoradiographs illustrates that heterotrophic bacteria metabolize organic substrates when they closely associated with cyanobacteria such as Phormidium, Chamaesiphon, and Nostoc. Cyanobacteria fix carbon and nitrogen while heterotrophs recycled CO2 back to photoautotrophs (Priscu et al. 1998). Hypolithic microbial consortia associated with nitrogen fixers including cyanobacteria and proteobacteria play a vital role in the nutrient cycling of Antarctic desert soils. PCR amplification of metagenomic DNA using primers for nifH, polF, and polR shows major nitrogen fixers belonging to Nostocales, which contains heterocysts and proteobacteria including Azotobacter vinelandii (Cowan et al. 2011).
Hypolithic communities including culturable bacteria like Bacillus sp., Streptomyces sp., and a cyanobacterium, Chroococcidiopsis sp., are in Atacama Desert experiencing an annual rainfall < 5 mm per year (Gómez-Silva et al. 2008). It suggests that microbial consortia with cyanobacteria have longer survival under the sunlight of 16–300 kJ m−2 in Atacama Desert since cyanobacterial species produce exopolysaccharides (EPS) that provide residence for other cyanobacteria and bacteria besides protecting bacteria from desiccation. These EPS enhance stabilization of sediments and cohesion of the mat which provides surface and growth substrate for the consortium and assists detoxification by binding to potential toxins and heavy metals (Decho 1990). Longer exposure to desiccation induces production of scytonemin, a stable and passive sunscreen in Chroococcidiopsis sp. used for its survival in desert soil (Mazor et al. 1996; Gómez-Silva et al. 2008; Abed et al. 2010).
Consortia of heterotrophic bacteria with microalgae contribute to the production of water-stable aggregates needing for nitrogen cycle, water retention, primary production, mineralization, and soil stability (Evans and Johansen 1999). Furthermore, this biological interaction could be used for mitigation of climatic changes, stabilizing desert soil from wind and water erosion, and fertilizing arid soils. Certain aerobic heterotrophic bacteria exhibit hydrocarbon degradation while cyanobacteria in the consortia provide oxygen to oil degraders for oxidative degradation of hydrocarbon (Abed and Köster 2005). Desert soils with hydrocarbon-degrading rhizospheric consortia enhance the plant growth and these organisms support for bioremediation of oil-polluted area (Radwan et al. 1998). Activity of nitrogen-fixing bacteria in Tengger Desert in China enhances soil fertility and algal diversity including Chlamydomonas sp., Chlorococcum humicola, and Chlorella valgaris which increases soil texture, nutrient availability, and organic matter content in the desert, thus providing favorable environment for establishing desert soil and propagating cryptogams that supports restoration of biodiversity in deserts (Li et al. 2003).
In Atacama Desert, endolithic microbial communities exhibit higher water availability due to less exposure to harmful UV and photosynthetic active radiation (PAR) through gypsum rocks containing sepiolite inclusions. However, intensive PAR enhances colonization of cyanobacteria and microalgae in the cryptoendolithic environment resulting in the production of carotenoids within the topmost algal layer. Simultaneously, hypoendolithic cyanobacteria produce scytonemin pigment as a defense mechanism against damages of photoinhibition and photooxidation, which could use for drugs preventing skin from UV damages. This could apply for sunscreen due to its broad absorption spectrum of UV radiations (Gabani and Singh 2013). Orange-colored algal cells produced larger quantities of carotenoids just below the gypsum to provide protection to green algae from intense solar radiation and allow them to grow in little deeper layers until maturation. Meanwhile, scytonemin in the hypoendolithic environment protect colonized cyanobacteria beneath the green microalgal cell layer (Wierzchos et al. 2015).
Ecological significance of consortia in soil crusts on desert plants
The presence of consortia dominated by cyanobacteria enhances uptake of essential nutrients. They increase the nitrogen content of soil while enhancing the plant uptake of Na, Cu, Zn, and K (Harper and Belnap 2001). In contrast, they cause negative impacts on the uptake of P and Fe by the associated seed plants as depicted in Fig. 1. The dense growth of these microorganisms on the soil surfaces is most influencing on essential elements for short-lived herbs, which are rooted on soil surface instead of deeply rooted herbs. The rhizosphere bacteria of desert plants such as Opuntia cholla, Stenocereus thurberi, and Pachycereus pringlei fix atmospheric nitrogen and produce organic acids which reduce pH of the soil and rock medium for enhancing bacterial growth and consequently dissolving insoluble phosphates, limestone, and rocks. The desert bacteria are thus able to discharge minerals such as Mg, K, Cu, Fe, and Zn from the rocks and subsequently help the growth of plants and other microorganisms. These results indicate that rhizosphere bacteria on cacti root support chemical weathering in hot and subtropical deserts and enhance the growth of desert plants (Puente et al. 2008).
Cyanobacteria first colonize and stabilize topmost layers of soil, and form biological soil crusts with bacteria and microalgae stabilizing the topsoil. Therefore, cyanobacterial amendments to soils can effectively control the desertification process by increasing nutrient availability and promoting growth of vegetation. Lan et al. (2014) used cyanobacteria, Microcoleus vaginatus and Scytonema javanicum , as an inoculum, for soil stabilization because they produce exopolysaccharides that help in the aggregation of soil particles and formation of biological crusts which leads to soil stability. These cyanobacterial soil crusts, in turn, increase soil carbon content and nitrogen thereby provide necessary nutrients for vascular plants.
The fine roots of plants penetrate the desert soil and hold together by mucilage to provide a “rhizosheath.” Bacteria such as Bacillus polymyxa, Ancalomicrobium sp., and Hyphomicrobium sp. are associated with desert rhizosheaths and stimulate water retention and plant uptake of nutrients (Watt et al. 1994). Thus, desert soil crusts dominated by heterotrophic bacteria, microalgae, and cyanobacteria play a major role in the biogeochemistry of arid zone. They also contribute organic carbon for plant growth (Belnap et al. 2003; Bashan and de-Bashan 2010), fix atmospheric nitrogen (Malam Issa et al. 2001; Pointing and Belnap 2012), and promote survival of vascular plant seedlings (Godinez-Alvarez et al. 2012). Consortia of Chlorella sp. and Azotobacter sp. that are isolated in desert rhizosphere were used as a biostimulator and biofertilizer for enhancing germination and growth of rice plants (Zayadan et al. 2014). Bacteria, Acinetobacter rhizosphaerae, isolated from the cold desert in Himalaya have high phosphorus solubilization and indole acetic acid (IAA) production supporting for plant growth (Gulati et al. 2009). This IAA supports the growth of resident microorganisms including microalgae within rhizosphere and non-rhizosphere and root elongation of plants (Vassilev et al. 2012; Amin et al. 2015). These microalgae subsequently serve as a source of carbon for plant growth (Trejo et al. 2012). Therefore, these organisms play the major role in the vegetation of deserts, and subsequently, they can be used for agricultural purposes. The presence of consortia of photosynthetic organisms and bacteria on the desert surface or within the soil supports water retention, reduction of soil erosion, soil stability maintenance, and nutrient availability enhancement for plants (Subashchandrabose et al. 2013).
Industrial potential of enzymes from desert microalgae, cyanobacteria, and bacteria
Desert soil is a good source for exploration of thermostable enzymes for biotechnological applications because desert isolates of microalgae, cyanobacteria, and bacteria have great potential in degrading materials rich in carbohydrates (Herbert 1992; Varshney et al. 2015). Biological crusts formed in desert soils predominantly by Nostoc spp. and Microcoleus spp. were shown to have increased enzymatic activities compared to those of bare lands. For instance, the activities of invertase, cellulases, and proteases in the desert soil layers were 21.70 μmol glucose g−1 h−1, 0.13 μmol glucose g−1 h−1, and 21.12 μmol NH3 g−1 h−1, respectively, and the corresponding enzyme activities in barren soils were 0.08 μmol glucose g−1 h−1, 0.03 μmol glucose g−1 h−1, and 0.03 μmol NH3 g−1 h−1, respectively (Miralles et al. 2012). Interestingly, cyanobacteria showed increased degradation of low molecular weight substrates compared to high molecular weight substrates. Indeed, such an activity supports cyanobacteria for their survival under conditions of desiccation and developing symbiosis, leading to increased soil nutrient availability for vegetation (Miralles et al. 2012).
Of the total bacteria isolated from a hot desert environment, the percent occurrence for amylolytic, proteolytic, and cellulolytic bacteria was 70.83, 50.41, and 5.41, respectively (Aanniz et al. 2015). These enzymes help in decomposing limited organic matter available in desert soils and increase nutrient uptake by seed plants. Moreover, the thermostability of the enzymes in desert isolates has greater industrial applications in starch industry (Prakash and Jaiswal 2010), production of food additives (Demirjian et al. 2001), and synthesis of pharmaceutical intermediates (Niehaus et al. 1999). Nithya et al. (2017) reported thermostable α-amylase activity in an actinobacterium, Streptomyces fragilis DA7-7, isolated from desert soil samples from Saudi Arabia. They demonstrated the potential of the enzyme in starch liquefaction and pharmaceutical and food industries, and as an additive in detergent production, since it has tolerance to high temperatures, pH, salt, and detergents. Although microalgae, cyanobacteria, and bacteria present in desert soils are rich sources of thermostable enzymes, very limited investigations explored their potential as such studies require development of high-throughput screening based on advanced omics tools and mass culturing of these organisms present in desert consortia (Varshney et al. 2015).
Engineering consortia of cyanobacteria/microalgae and bacteria for desert soils
Using cyanobacterial/microalgal−bacterial consortia as a sustainable engineered system to restore desert ecosystems for agricultural purposes has become a growing trend in the recent past. Alginate beads with different shapes and arrangements are used in various industries as suitable carriers of inoculants. Chlorella vulgaris and Azospirillum brasilense (PGPB) within rhizosphere co-immobilize on small alginate beads to build-up the close relationship and it shows considerable growth and proliferation of microalgae (Gonzalez-Bashan et al. 2000). Light microscopic observations reveal colonization of the microalga at the periphery of the beads because of high oxygen concentration while the bacteria colonized throughout the whole bead. A. brasilense produce phytohormones such as indole-3-acetic acid (IAA) increasing the growth of the microalga C. vulgaris. The alginate beads with co-cultures compared to those containing sole organisms increased soil quality along with root and shoot development resulting in higher organic matter content and microbial activity in desert soils as represented in Fig. 2. They also showed an increase in soil microbial carbon by the co-cultures in the beads within 60 days (Table 3) as when compared with the individual microorganisms immobilized in beads (Trejo et al. 2012).
Sears and Prithiviraj (2012) suggest cyanobacteria-based consortial inoculant called TerraDerm for fertilizing the desert soil. In the preparation of a particular consortium, the selected microorganisms are initially mass cultured in a liquid medium using both light and sugar-fed photobioreactors. The cultivated microorganisms strain using capillary belt arrangement onto a thin damp mat without damaging the living biomass. These damp mats are composed of the following: antioxidants such as beta carotene, xeriprotectants as layers to avoid cell damage of microorganisms by desiccation, micronutrients and sugars for initial establishment of non-photosynthetic organisms, quartz and clay to support granulation of mats and to avoid cell damage, unique gene sequence for tracing the growth and proliferation, and vascular plant seeds for germination and survival in harmony with cyanobacteria and other microorganisms. The wet mat is then dried into thin granules using low-temperature belt without harming microorganisms. Finally, processed granules of consortia feed into the fluidized bed bioreactors. Cost-effective agricultural aircrafts use for the distribution of these inoculants in the desert region improving the soil fertility and stability against soil erosion.
Increasing the indigenous microbial consortia supports efficient hydrocarbon degradation and vegetation of desert soil. Wang et al. (2009) demonstrate improving microbial consortia within desert through isolated cyanobacterial strains, Microcoleus vaginatus Gom and Scytonema javanicum Born et Flah from algal soil crusts from a desert area of Inner Mongolia. Liquid medium inoculating with both organisms was placed in a greenhouse and subsequently transferred to a tank and into previously setup moving dunes with sand barriers and erecting straw checkerboards. M. vaginatus and S. javanicum were mixed in a ratio of 10:1 and sprayed uniformly over the sand surface. The automated sprinkler system is watering for 15–18 days until the cyanobacterial consortia emerged. This soil medium can be introduced to desert soil facilitating vegetation and establishing stable soil.
Zambrano et al. (2016) introduced a simple lab-scale photobioreactor to obtain cyanobacterial/microalgal−bacterial consortia. These bioreactors are made of glass, and either side is covered by steel. All the contents including biomass of algae and bacteria and dissolved substrates of ammonium and nitrate are stirred uniformly at 350 rpm and temperature under 23 °C. The reactors are supplied with oxygen and carbon dioxide and placed under fluorescent light. The dominant bacteria and microalgae are genus Rhodobacter and Scenedesmus, respectively. While constructing such models for developing consortia for deserts with high light irradiation, light attenuation (light gradient from top to bottom) must be considered since these light intensities could affect the algal growth under real situations. Also, culture conditions such as medium temperature, species and inoculum densities of bacteria and algae, and the quantity of incident light to be provided are the major criteria for engineering the consortia, and it should include advanced approaches for controlling their physical and chemical environmental conditions.
Genetically engineering of algae and bacteria consortia with favorable characteristics such as stability, robustness, and scalability would be supportive for applying them into desert vegetation (Goers et al. 2014; Ramanan et al. 2016). However, in vitro studies would be required before they are applied into deserts. Microfluidic devices fabricated with accurate micron-scale environments could be used for studying their interactions, development, communication, and establishment such as biofilm formation of these synthetic co-cultures (Hong et al. 2012). Usually, microorganisms in natural environments cooperatively live with different types of organisms that perform very complex functions. Therefore, synthetic biologists engineer clonal communities containing unique characters like cellular memory, cell division, differentiation, and adaptation presenting in complex multicellular forms. This would be supportive for various biotechnological applications and study how new functions within artificial or natural consortia useful in cellular signaling and communication pathways between diverse organisms that help to construct the consortia for the extreme environmental conditions in the deserts (Brune and Bayer 2012). A better understanding of associations such as competition and the cooperation of both algae and bacteria for different types of nutrients available in ecosystems would be the significant factors for engineering of consortia for a particular environment such as deserts. Furthermore, engineering of the consortium would be achievable in view of the existing biotechnological tools, for instance, metabolic profiling and functional genomics (Subashchandrabose et al. 2011).
Conclusions
Desert soils are characteristic of having harsh and rapidly fluctuating environmental circumstances, intense ultraviolet radiation, and lack of water, and are colonized by extremophilic microorganisms that include cyanobacteria, microalgae, and bacteria. Most of these naturally occurring microorganisms in the extreme habitats exist as consortia by developing extensive metabolic capabilities. Cyanobacterial/microalgal−bacterial consortia have superior performance compared to individual organisms, and engineering of such consortia would be very useful in water retention, mineralization and maintaining the stability of desert soils, primary production, and establishment of vegetation on desert surfaces, as well as in biotechnological applications such as pollutant removal from contaminated deserts and production of industrially important enzymes. Currently, there are growing trends towards the use of genetically modified microbial populations in synthetic biology for designing and studying efficient consortia with ecological functions for desert restoration. By studying the relationships such as adaptations of desert cyanobacteria, microalgae, and bacteria within a consortium would support for engineering beneficial, comprehensive, and controllable cyanobacterial/microalgal−bacterial consortia for the desert ecosystem.
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IP acknowledges the University of Newcastle for UNRS and UNIPRS scholarships, and SRS acknowledges the University of Newcastle for ECR HDR scholarship.
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Perera, I., Subashchandrabose, S.R., Venkateswarlu, K. et al. Consortia of cyanobacteria/microalgae and bacteria in desert soils: an underexplored microbiota. Appl Microbiol Biotechnol 102, 7351–7363 (2018). https://doi.org/10.1007/s00253-018-9192-1
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DOI: https://doi.org/10.1007/s00253-018-9192-1