Efficient soil microorganisms: A new dimension for sustainable agriculture and environmental development

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Agriculture, Ecosystems and Environment 140 (2011) 339–353

Contents lists available at ScienceDirect

Agriculture, Ecosystems and Environment

journa l homepage: www.e lsev ier .com/ locate /agee

eview

fficient soil microorganisms: A new dimension for sustainable agriculture andnvironmental development

ay Shankar Singh ∗, Vimal Chandra Pandey, D.P. Singhepartment of Environmental Science, Babasaheb Bhimrao Ambedkar (Central) University, Raibarelly Road, Lucknow 226025, Uttar Pradesh, India

r t i c l e i n f o

rticle history:eceived 30 August 2010eceived in revised form 20 January 2011ccepted 21 January 2011

a b s t r a c t

Sustainable agriculture is vital in today’s world as it offers the potential to meet our agricultural needs,something that conventional agriculture fails to do. This type of agriculture uses a special farming tech-nique wherein the environmental resources can be fully utilized and at the same time ensuring thatno harm was done to it. Thus the technique is environment friendly and ensures safe and healthy

vailable online 12 February 2011

eywords:gricultureiofertilizersiocontrol

agricultural products. Microbial populations are instrumental to fundamental processes that drive stabil-ity and productivity of agro-ecosystems. Several investigations addressed at improving understandingof the diversity, dynamics and importance of soil microbial communities and their beneficial and co-operative roles in agricultural productivity. However, in this review we describe only the contributionsof plant growth promoting rhizobacteria (PGPR) and cyanobacteria in safe and sustainable agriculture

yanobacteriahizobacteria

development.© 2011 Elsevier B.V. All rights reserved.

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3402. The efficient and potential soil microbes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3403. Why sustainable agriculture is so important? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3404. The contributions of soil micro-flora in sustainable agricultural production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3405. Microbial management of soil fertility for sustainable agriculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3416. Benefits of better management of the soil microbiota? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3417. Efficient soil microbes for sustainable agriculture and environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3418. Plant growth promoting rhizobacteria and agricultural productivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 341

8.1. PGPR as biological fertilizers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3428.2. PGPR in saline agricultural soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3428.3. 1-Aminocyclopropane-1-carboxylic acid (ACC) deaminase-containing PGPR protect plants from the environmental stresses. . . . . . . . . . . 3438.4. PGPR as biocontrol agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3438.5. PGPR as biological fungicides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 344

9. Contribution of cyanobacteria to agriculture and environmental sustainability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3449.1. Cyanobacteria in stability and productivity of desert soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3459.2. Reclamation of saline wastelands by cyanobateria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3469.3. Cyanobacteria as potential biocontrol agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3469.4. Soil heavy metal bioremediation by cyanobacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 347

10. Role of rhizospheric microbial interactions in environment and agricult11. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

∗ Corresponding author. Tel.: +91 522 2998718; fax: +91 522 2441888.E-mail address: jayshankar [email protected] (J.S. Singh).

167-8809/$ – see front matter © 2011 Elsevier B.V. All rights reserved.oi:10.1016/j.agee.2011.01.017

ure sustainability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 347. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 349. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 350. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 350

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40 J.S. Singh et al. / Agriculture, Ecosyste

. Introduction

According to United Nations estimates, the global human popu-ation is projected to reach 8.9 billion by 2050, with the developingountries of Asia and Africa to absorb the vast majority of thencrease (Wood, 2001). Decreasing irrigational water supplies andther environmental concerns exacerbate the challenges we faceo meet the nutritional requirements of the growing popula-ion.

The various ways in which microorganisms have been usedver the past 50 years to advance medical technology, human andnimal health, food processing, food safety and quality, geneticngineering, environmental protection, agricultural biotechnology,nd in more effective treatment of agricultural and municipalastes collectively the most impressive record. Many of these tech-ological advances would not have been possible using straight

orward chemical and physical engineering methods, or if theyere, they would not have been practically or economically

iable.Nevertheless, while microbial technologies have been applied

o various agricultural and environmental problems with con-iderable success in recent years, they have not been widelyccepted by the scientific community as it is often hard to con-istently reproduce their beneficial effects. Microorganisms areffective only when they are provided with suitable and opti-um conditions for metabolism including the available water,

xygen, pH and temperature of the ambient environment. Theypes of microbial cultures and inoculants available in the marketoday have increased rapidly owing to new technologies. Signif-cant achievements are being made in systems where technicaluidance is coordinated with the marketing of microbial products.ince microorganisms are useful in overcoming problems associ-ted with the use of chemical fertilizers and pesticides, are nowidely applied in agriculture.

Environmental pollution, by excessive soil erosion and the asso-iated transport of sediment, chemical fertilizers and pesticideso surface waters and groundwater, and ineffective treatment ofuman and animal wastes poses serious environmental and socialroblems throughout the world. Although engineers attemptedo solve such problems using established chemical and physical

ethods found that it cannot be done without deploying microbialethods and technologies.For many years, soil microbiologists and microbial ecolo-

ists differentiated soil microorganisms as ‘beneficial’ or ‘harmful’epending how they affect soil quality, crop growth and yield. Ben-ficial microorganisms are those that fix atmospheric N, decomposerganic wastes and residues, detoxify pesticides, suppress plantiseases and soil-borne pathogens, enhance nutrient cycling androduce bioactive compounds such as vitamins, hormones andnzymes that stimulate plant growth.

The recent interest in eco-friendly and sustainable agriculturalractices (Kavino et al., 2007; Saravanakumar and Samiyappan,007; Harish et al., 2009a,b). Biofertilizer and biopesticide con-aining efficient microorganisms, improve plant growth in manyays compared to synthetic fertilizers, insecticides and pes-

icides by way of enhancing crop growth and thus help inustainability of environment and crop productivity. The rhi-ospheric soils contain diverse type of efficient microbes witheneficial effects on crop productivity. The plant growth pro-oting rhizobacteria (PGPR) and cyanobacteria are rhizosphericicrobes and produce bioactive substances to promote plant

rowth and/or protect them against pathogens (Glick, 1995; Harisht al., 2009a). This communication highlighted contributions ofGPR, cyanobacteria and some beneficial microbial interactionsn the agriculture improvement and environment sustainabil-ty.

d Environment 140 (2011) 339–353

2. The efficient and potential soil microbes

Such microorganisms may comprise of mixed populations ofnaturally occurring microbes that can be applied as inoculants toincrease soil microbial diversity. Investigations have shown thatthe inoculation of efficient microbial community to the soil ecosys-tem improves soil quality, soil health, growth, yield and quality ofcrops. These microbial populations may consists of selected speciesof microorganisms including plant growth promoting rhizobacte-ria, N2-fixing cyanobacteria, plant disease suppressive bacteria andfungi, soil toxicant degrading microbes, actinomycetes and otheruseful microbes.

Efficient and potential soil microbial biota is only suitable forsustainable agriculture practices and may not the so for other alter-natives. It is an added dimension to optimizing our soil and cropmanagement practices such as crop rotation, organic amendments,conservation tillage, crop residue recycling, soil fertility restoration,maintenance of soil quality and the biocontrol of plant diseases. Ifused adequately, microbial communities can significantly benefitthe agriculture practices.

3. Why sustainable agriculture is so important?

Sustainable agriculture is a broadbased concept rather thana specific methodology. It encompasses advances in agriculturalmanagement practices and technology, and the growing recogni-tion indicates that the conventional agriculture that developed postWorld War-II, will not be able to meet the needs of the growingpopulation in the 21st Century.

Conventional agriculture is facing either reduced productionor increased costs, or both. Farming monocultures, such as wheatfields, repeated on the same land results in the depletion of top-soil, soil vitality, groundwater purity and beneficial microbe, insectlife, making the crop plants vulnerable to parasites and pathogens.An everincreasing amount of fertilizers and pesticides as well asthe energy requirements for tilling to aerate soils and increasingirrigation costs are of prime concern. While conventional methodsenabled large increases in crop yields, thus high profits only ini-tially, have failed to be considered as the ideal approach for future.

The steady increase in corporate farming based conventionalmethods in the last few decades, primarily profit driven, hasincreased the destabilization of rural communities as well asspeeded up the detrimental effects on both the farmland ecol-ogy and neighboring natural environments. Cost cutting effortshave frequently targeted farm workers; financial recompense forthe work performed, has degraded significantly compared to otherareas of human endeavor. This not only decreases their own stan-dard of living but has a flow on effect impacting the economicviability of small, rural towns.

The expansion of urban population and business and indus-trial complexes has reduced the available farmland. The locationof much of the world’s primary and best quality farmland is inareas that are steadily becoming prime real estate for top end resi-dential assets. In economic terms, farming simply cannot compete.The profits from transforming the farmland into residential sub-divisions are astronomically higher than those achievable fromfarming it by any method.

4. The contributions of soil micro-flora in sustainableagricultural production

A fundamental shift is taking place worldwide in agriculturalpractices and food production. In the past, the principal drivingforce was to increase the yield potential of food crops and their pro-ductivity. Today, the drive for productivity is increasingly combined

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ith the desire and even the demand for sustainability. Sustain-ble agriculture involves successful management of agriculturalesources to satisfy human needs while maintaining environmentaluality and conserving natural resources for future. Improvement

n agricultural sustainability requires the optimal use and manage-ent of soil fertility and its physico-chemical properties. Both rely

n soil biological process and soil biodiversity. This implies man-gement practices that enhance soil biological activity and therebyuildup long term soil productivity and crop health. Such practicesre of major concern in marginal lands to avoid degradation and inestoration of degraded lands and in regions where high externalnput agriculture is not feasible.

. Microbial management of soil fertility for sustainablegriculture

The central paradigm for the biological management of soil fer-ility is to utilize farmer’s management practices to influence soil

icrobial populations and processes in such a way as to achieveeneficial effects on soil productivity. Microbial populations androcesses influence soil fertility and structure in a variety of ways,ach of which has an ameliorating effect on the main soil-basedonstraints to productivity:

Symbionts such as PGPR and cyanobacteria, etc. increase the effi-ciency of nutrient acquisition by plants.A wide range of microbial community participates in decomposi-tion, mineralization, and nutrient availability (microbe-mediatedunusable P-availability), and therefore influence the efficiency ofnutrient cycles.Soil microbial communities mediate both the synthesis anddecomposition of soil organic matter and therefore, influencecation exchange capacity, the soil N, S, P reserve, soil acidity andtoxicity and soil water holding capacity.The burrowing and particle transport activities of soil microflora,and the aggregation of soil particles by fungi and bacteria, influ-ence soil structure and soil water regime.

. Benefits of better management of the soil microbiota?

Agriculture provides a major share of national income andxport earnings in many developing countries, while ensuring foodecurity, income and employment to a huge proportion of the popu-ation. Farmers are increasingly comlaint that declining soil fertilitys the major problem. As a result, controlling erosion and improv-ng the management of soil fertility, are now major issues on theevelopment policy agenda. Soil microorganisms contribute a wideange of essential services to the sustainability of all ecosystems,y acting as the primary driving agents of nutrient cycling, regulat-

ng the dynamics of soil organic matter, soil carbon sequestrationnd greenhouse gas emission, modifying soil physical structure andater regimes, enhancing the efficiency of nutrient acquisition by

he vegetation and enhancing plant health. These services are notnly essential to the functioning of natural ecosystems but con-titute an important resource for the sustainable management ofgricultural and environmental ecosystems.

Direct and indirect benefits of adopting microbiological man-gement of soil for sustainable agriculture production are:

Economic benefits (reduced input costs by enhancing resourceuse efficiency especially decomposition, nutrient cycling, N2-fixation, bioavailability of P, water storage and movement).Environmental protection (prevention of pollution and landdegradation especially through reducing use of agro-chemicalsand maintains soil structure and cation exchange capacity).

d Environment 140 (2011) 339–353 341

• Food security (improve yield and crop quality especially throughcontrolling pests and diseases and enhancing plant growth).

• Restoration and reclamation of wastelands (microbe mediatedremediation and rehabilititation of non-fertile waste area intofertile lands).

7. Efficient soil microbes for sustainable agriculture andenvironment

Agriculture, in a broad sense, is the activity in which the farmerattempts to integrate certain agro-ecological factors and produc-tion inputs for optimum crop and livestock production. Thus, it isreasonable to assume that farmers should be interested in ways andmeans of controlling useful soil microorganisms as the importantcomponents of the agricultural environment. Nevertheless, thisidea has often been rejected by naturalists and proponents of naturefarming and organic agriculture. The argument is that useful soilmicroorganisms will increase naturally with organic amendmentsto such soils as carbon, energy and nutrient sources. This indeedmay be true where there is the abundance of organic materials forrecycling only is in small scale farming. However, in most cases,soil microorganisms, beneficial or harmful, have often been con-trolled advantageously when crops in various agroecological zonesare grown and cultivated as crop rotations and without pesticidesuse. This explains why scientists have long been interested in theuse of potential and efficient microorganisms as soil and plant inoc-ulants to shift the microbiological equilibrium in ways that wouldenhance soil quality and the eco-friendly agriculture crops.

Low agricultural production efficiency is closely related to a poorcoordination of energy conversion which, in turn, is influenced bycrop physiological factors, the environment, and other biologicalfactors including soil microbes. The soil and rhizosphere microfloracan accelerate the growth of plants and enhance their resistanceto pathogens and harmful insects by producing bioactive metabo-lites. Such microorganisms maintain growth of plants, and thushave primary effects on both soil and crop quality. A wide range ofbenefits are possible depending on their predominance and activ-ity at any one time. However, there is a growing consensus that itis feasible to obtain maximum economic agronomic yield of highquality at higher net returns, without the use of artificial fertilizers,herbicides, insecticides and pesticides. Until recently, this was notthought to be the very likely possibility using conventional agri-cultural practices. However, it is important to recognize that thebest soil and agricultural management practices to attain a moresustainable and green agriculture will also enhance the growth,number and activities of efficient soil microflora that, in turn, canenhance the growth, yield and agriculture quality. In particular,healthy living soil with improved quality is the very foundation ofa future sustainable agriculture.

8. Plant growth promoting rhizobacteria and agriculturalproductivity

In the broadest sense, plant growth promoting rhizobacteriainclude the N2-fixing rhizobacteria that colonize the rhizosphere,providing N to plants in addition to the well characterized legumerhizobia symbioses. Regardless of the mechanism(s) of plantgrowth promotion, PGPR must colonize the rhizosphere around theroots, the rhizoplane (root surface) or the root itself (within roottissue). PGPR can affect plant growth either indirectly or directly;

indirect promotion of plant growth in affected when PGPR lessen orantagonize the deleterious effects of one or more phytopathogens;while direct route by PGPR involves either providing plants with thecompounds synthesized by the bacterium or facilitating the uptakeof certain nutrients from the environment (Glick, 1995). PGPR reg-

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Table 1Plant growth promoting rhizobacteria (PGPR) regulating various growth parameters/yields of crop/fruit plants.

PGPR Crop parameters References

Rhizobium leguminosarum Direct growth promotion of canola and lettuce Noel et al. (1996)Pseudomonas putida G 12–2 Early developments of canola seedlings Glick et al. (1997)Azospirillum brasilense and A. irakense strains Growth of wheat and maize plants Dobbelaere et al. (2002)P. fluorescens strain Growth of pearl millet Niranjan et al. (2003)P. putida strain Growth stimulation of tomato plant Gravel et al. (2007)Azotobacter and Azospirillum strains Growth and productivity of canola Yasari and Patwardhan (2007)P. alcaligenes PsA15, Bacillus polymyxa BcP26, and

Mycobacterium phlei MbP18,Enhance uptake of N, P and K by maize crop in nutrient deficientcalcisol soil

Egamberdiyeva (2007)

Pseudomonas, Azotobacter and Azospirillum strains Stimulates growth and yield of chick pea (Cicer arietinum) Rokhzadi et al. (2008)R. leguminismarum (Thal-8/SK8) and Pseudomonas sp.

strain 54RBImprove the yield and phosphorus uptake in wheat Afzal and Asghari (2008)

P. putida strains R-168 and DSM-291; Improves seed germination, seedling growth and yield of maize Nezarat and Gholami (2009)P. fluorescens strains R-98 and DSM-50090;A. brasilense DSM-1691 and A. lipoferum DSM-1690P. putida strain R-168, Seed germination, growth parameters of maize seedling in

greenhouse and also grain yield of field grown maizeGholami et al. (2009)

P. fluorescens strain R-93, P. fluorescens DSM 50090, P.

af nuta spp.

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P. fluorescens strains, CHA0 and Pf1 Increase growth, lecv.Virupakshi (Mus

lation of various growth parameters/yields of crop/fruit plants haseen listed in Table 1.

Among the diverse bacteria identified as PGPR, the Bacilli andseudomonads are the predominant ones (Podile and Kishore,007). PGPR exert a direct effect on plant growth by production ofhytohormones, solubilization of inorganic phosphates, increased

ron nutrition through iron-chelating siderophores and the volatileompounds that affect the plant signaling pathways. Additionally,y antibiosis, competition for space and nutrients and induction ofystemic resistance in plants against a broad-spectrum of root andoliar pathogens, PGPR reduce the populations of root pathogensnd other deleterious microorganisms in the rhizosphere, thus ben-fiting the plant growth.

.1. PGPR as biological fertilizers

A group of biofertilizers comparising beneficial rhozobacteriadentified as PGPR, are strains from genera of Pseudomonas, Azospir-llum, Azotobacter, Bacillus, Burkholdaria, Enterobacter, Rhizobium,rwinia and Flavobacterium (Rodriguez and Fraga, 1999). Free-livingGPR have shown promise as biofertilizers (Podile and Kishore,007). Many studies and surveys reported plant growth promo-ion, increased yield, uptake of N and some other elements throughGPR inoculations (Sheng and He, 2006; Glick et al., 2007). In addi-ion, treatments with PGPR enhance root growth, leading to a rootystem with large surface area and increased number of root hairsMantelin and Touraine, 2004).

In general, huge bulk artificial fertilizes is applied to replenishoil N and P with the resultant in high cost and environmen-al risk. Most of P in insoluble compounds are unavailable tolants. N2-fixing and P-solubilizing bacteria (PSB) are importantor crop plants as they increase N and P uptake and play a cru-ial role as PGPR in the biofertilization (Zahir et al., 2004; Zaidind Mohammad, 2006).Thus, the application of such microbes asnvironment friendly biofertilizer may contribute to minimize these of expensive phosphatic fertilizers. Phosphorus biofertilizers

ncrease the availability of accumulated P (by solubilization), effi-iency of biological N2-fixation and the availability of Fe, Zn, etc.,

ue to generation of plant growth promoting substances (Kuceyt al., 1989). Inoculation of N2 fixing and PSB in combination wasore effective than the single microbe in providing a more bal-

nced nutrition to agriculture crops such as sorghum, barley, blackram, soybean and wheat (Alagawadi and Gaur, 1992; Belimov

rient contents and yield of bananaAAB) plants

Kavino et al. (2010)

et al., 1995; Abdalla and Omer, 2001; Tanwar et al., 2002; Galal,2003). Reports on co-inoculation of Rhizobium and PSB on wheatare rare and especially in India, very little work has been doneon such lines. Therefore, extensive investigations to explore theeffect of single and dual inoculations of N2-fixing and P-solubilizingbacterial species on yields of various crops are required urgently.

More recent findings indicated that the treatment of arablesoils with PGPR inoculations significantly increases agronomicyields (Harish et al., 2009a,b; Yazdani et al., 2009). The PGPRstrains Pseudomonas alcaligenes PsA15, Bacillus polymyxa BcP26and Mycobacterium phlei MbP18 had the pronounced stimula-tory effects on plant growth and uptake of N, P and K by maizein nutrient-deficient calcisol soils (Egamberdiyeva, 2007). Theenhancement in various agronomic yields by PGPR was because ofthe production of growth promoting phytohormones, phosphatemobilization, production of siderophore and antibiotics, inhibitionof plant ethylene synthesis and induction of plant systemic resis-tances to pathogens (Han et al., 2004; Zahir et al., 2004; Ramazanet al., 2005; Wua et al., 2005; Zaidi and Mohammad, 2006, Turanet al., 2006; Kohler et al., 2006). Very recently, Kavino et al. (2010)reported that P. fluorescens strain, CHA0 in combination with chitinincreased growth, leaf nutrient contents and yield of banana plantsunder perennial cropping systems thus suggesting that in view ofthe environmental problems, due to excessive use and high pro-duction costs of fertilizers, PGPR may represent the potential soilmicroflora to be deployed for sustainable and eco-friendly agricul-ture.

8.2. PGPR in saline agricultural soils

Soil salinity constitutes a serious problem for vegetable as wellas other crops as salinisation suppresses plant growth, particularlyin arid and semiarid areas (Parida and Das, 2005). An alterationin physiology of plants facing salt stress adversely affects nutri-tional uptake and also crop growth. More specifically, the soil-bornepseudomonads have received paramount attention because of theircatabolic versatility, efficient root-colonising ability and capacityto produce a wide range of enzymes and metabolites that help

the plant withstand varied biotic and abiotic stresses (Vessey,2003). PGPR facilitate plant growth indirectly by reducing plantpathogens, or directly by facilitating the nutrient uptake throughphytohormone production (e.g. auxin, cytokinin and gibberellins),by enzymatic lowering of plant ethylene levels and/or by produc-

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ion of siderophores (Kohler et al., 2006). It has been demonstratedhat inoculations with AM fungi improves plant growth under salttress (Cho et al., 2006). Kohler et al. (2006) demonstrated the bene-cial effect of PGPR Pseudomonas mendocina strains on stabilizationf soil aggregate. The three PGPR isolates Pseudomonas alcaligenessA15, Bacillus polymyxa BcP26 and Mycobacterium phlei MbP18ere able to tolerate high temperatures and salt concentrations and

hus confer on them potential competitive advantage to survive inrid and saline soils such as calcisol (Egamberdiyeva, 2007).

Kohler et al. (2009) investigated the influence of inoculationith a PGPR, Pseudomonas mendocina, alone or in combination with

n AM fungus, Glomus intraradices or Glomus mosseae on growth andutrient uptake and other physiological activities of Lactuca sativaffected by salt stress. Salinity decreased lettuce growth regard-ess of the biological treatments and of the salt stress level. Thelants inoculated with P. mendocina had significantly greater shootiomass than the controls and it is suggested that inoculation withelected PGPR could better effective tool for alleviating salinitytress in salt sensitive plants.

The costs associated with amelioration of soil salinity areotentially enormous but salinity comes heavily on agriculture,iodiversity and also the environment. The contributions of PGPRo plant health and their osmotolerance mechanisms are vital. Ashe saline areas under agriculture have been on the rise every yearcross the globe, it is of serious concern (Paul and Nair, 2008). Itould be ascertained that the osmotolerance mechanisms of MSP-93 viz. de novo synthesis of osmolytes and overproduction ofalt-stress proteins effectively nullified the detrimental effects ofigh osmolarity. Pseudomonas fluorescens MSP-393 could serve ashe ideal bioinoculant for crops in saline soils (Paul and Nair, 2008).

Investigations on interaction of PGPR with other microbes andheir effect on the physiological response of crop plants under dif-erent soil salinity regimes are still in incipient stage. Inoculationsith selected PGPR and other microbes particularly, AM fungi could

erve as the potential tool for alleviating salinity stress in salt sensi-ive crops. Therefore, extensive investigations is needed in this area,nd the use of PGPR and other symbiotic microorganisms, espe-ially AM fungi, can be useful in developing strategies to facilitateustainable agriculture in saline soils.

.3. 1-Aminocyclopropane-1-carboxylic acid (ACC)eaminase-containing PGPR protect plants from thenvironmental stresses

Relatively recently, it was discovered that many plantrowth promoting bacteria (PGPB) contain the enzyme 1-minocyclopropane-1-carboxylic acid (ACC) deaminase that cleave

he ethylene precursor ACC to �-ketobutyrate and ammonia andhereby lower the ethylene levels in developing or stressed plantsSaleem et al., 2007). Bacterial strains containing ACC deaminasean, in part, at least alleviate the stress induced ethylene medi-ted negative impact on plants. Such an aspect is extensivelytudied in numerous PGPBs like Agrobacterium genomovars andzospirillum lipoferum, Alcaligenes and Bacillus, Burkholderia, Enter-bacter, Methylobacterium fujisawaense, Pseudomonas Ralstoniaolanacearum, Rhizobium, Rhodococcus, and Sinorhizobium melilotind Variovorax paradoxus (Penrose and Glick, 2001; Belimov et al.,001, 2005; Ma et al., 2003; Hontzeas et al., 2004a; Uchiumi et al.,004; Pandey et al., 2005a,b; Blaha et al., 2006; Stiens et al., 2006).he ACC deaminase metabolizes the root’s ACC into �-ketobutyratend ammonia and checks the production of ethylene which oth-

rwise inhibits plant growth through several mechanisms. Thelants treated with bacteria containing ACC-deaminase may haveelatively extensive root growth due to lowered ethylene levelsShaharoona et al., 2006) thus leading to resistance aginst varioustresses (Safronova et al., 2006).

d Environment 140 (2011) 339–353 343

ACC deaminase containing PGPBs when bound to the seed coator root of a developing seedlings, act as a sink for ACC, ensuring thatplant ethylene levels do not get elevated to a point that impairs rootgrowth (Jacobson et al., 1994; Glick, 1995; Glick et al., 1998, 1999).In addition, by lowering ethylene levels, ACC deaminase containingPGPBs protect plants from the deleterious effects of numerous envi-ronmental stresses, including flooding (Grichko and Glick, 2001),metals (Burd et al., 2000; Nie et al., 2002), drought (Mayak et al.,2004a) and salts (Mayak et al., 2004b). The importance of ACCdeaminase in the bacterium Enterobacter cloacae UW4 regardingplant growth promotion, has been demonstrated (Li et al., 2000).Hontzeas et al. (2004b) reported that ACC deaminase containingPGPB Enterobacter cloacae UW4 induces root elongation and pro-liferations in canola (Brassica rapa) largely by lowering ethylenelevels. While it is clear that ACC deaminase containing PGPR pro-mote growth of a variety of plants under various environmentalstresses, the precise nature of the changes in plant gene expres-sion by the bacterium, remains to be elucidated. Utilization of PGPRcontaining ACC deaminase activity in promoting plant growth anddevelopment both under stress and normal conditions and geneticmanipulation of cultivars with genes expressing this enzyme, hasattracted attentions of many (Sergeeva et al., 2006). Therefore, fur-ther developments in this area are extremely important possibly viavarious biotechnological approaches for agriculture sustainability.

8.4. PGPR as biocontrol agents

The PGPR is a group of rhizosphere colonizing bacteria that pro-duces substances to increase the growth of plants and/or protectthem against diseases (Harish et al., 2009a). PGPR may protectplants against pathogens by direct antagonistic interactions withthe pathogen, as well as through induction of host resistance.PGPR that indirectly enhance plant growth via suppression of phy-topathogens do so by a variety of mechanisms. These include, theability to produce siderophores to chelate iron, making it unavail-able to pathogens, to synthesize anti-fungal metabolites such asantibiotics, fungal cell wall lysing enzymes, or hydrogen cyanidethat suppress the growth of fungal pathogens, to successfully com-pete with pathogens for nutrients or specific niches on the rootand to induce systemic resistance (Glick et al., 1995; Bloembergand Lugtenberg, 2001; Persello Cartieaux et al., 2003). The PGPR asbiocontrol agents against various plant diseases has been presentedTable 2.

The ability of PGPRs as biocontrol agents against various plantdiseases has been listed in Table 3. Among the various PGPRsidentified, Pseudomonas fluorescens is one of the most extensivelystudied rhizobacteria, because of its antagonistic actions againstseveral plant pathogens (Kavino et al., 2007; Saravanakumar andSamiyappan, 2007; Harish et al., 2009a). The biocontrol dependson a wide variety of traits, such as the production by the bio-control strain of various antibiotic compounds, iron chelatorsand exoenzymes such as proteases, lipases, chitinases, and glu-canases as well as the competitive root colonization (ChinAWoenget al., 2000; Lugtenberg et al., 2001). The biocontrol efficacy andPGPR fluorescent pseudomonads is further increased by mixingtwo or more strains of Pseudomonas spp. (Singh et al., 1999;Saravanakumar et al., 2009) or mixing with chitin or other sub-stances (Radjacommare et al., 2002). Pseudomonas fluorescensMSP-393 has been proved as biocontrol agent for many of the cropsgrown in saline agricultural soils (Paul and Nair, 2008).

Banana bunchy top virus (BBTV) is one of the deadly viruses

that severely affect the yield of banana (Musa spp.) crop in WesternGhats, Tamil Nadu, India (Kavino et al., 2010). Kavino et al. (2008)demonstrated that application of P. fluorescens strain CHA0 + chitinbio-formulations, significantly reduced the BBTV incidence in hillbanana varity under greenhouse and field conditions. Chitinases

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Table 2Plant growth promoting rhizobacteria (PGPR) as biocontrol agents against various plant diseases.

PGPR Experimental sites Disease References

Bacillus pumilus strain SE34, Kluyvera cryocrescensstrain IN114, B. amyloliquefaciens strain IN937a,and B. subtilus strain IN937b.

Greenhouse experiment Cucumber MosaicCucumovirus (CMV) of tomato(Lycopersicon esculentum)

Zehnder et al. (2000)

B. amyloliquefaciens 937a, B. subtilis 937b, and B.pumilus SE34

Field condition Tomato mottle virus Murphy et al. (2000)

B. pumilus strain INR7 Field study Bacterial wilt disease incucumber (Cucumis sativus)

Zehnder et al. (2001)

Pseudomonas fluorescens based bio-formulation Rice field Sheath blight disease and leaffolder insect in rice (Oryzasativa)

Radjacommare et al. (2002)

B. pumilus strain SE34 Laboratory condition Blue mold disease of tobacco(Nicotiana)

Zhang et al. (2002)

B. subtilis strain GBO3, B. pumilus strain INR7 and B.pumilus strain T4

Greenhouse and fieldconditions

Downy mildew in pearl millet(Pennisetum glaucum)

Niranjan et al. (2003)

B. subtilis strain IN937a – CMV in cucumber Jetiyanon et al. (2003)B. cereus strains B101R, B212R, and A068R Greenhouse bioassays Foliar diseases of tomato Silva et al. (2004)Bacillus strains BB11 and FH17 Greenhouse experiment Blight of bell pepper (Capsicum

annuum)Jiang et al. (2006)

Pseudomonas fluorescens Saline field condition Saline resistance in groundnut(Arachis hypogea)

Saravanakumar andSamiyappan (2007)

Burkholderia strains MBf21 and MBf15 In vitro and In vivo Maize (Zea mays) rot Hernandez Rodriguez et al.,2008 (2008)

B. subtilis ME488 – Soil borne pathogen ofcucumber and pepper (Piper)

Chung et al. (2008)

P. fluorescens strain CHA0 + chitin bio-formulations Banana under greenhouse andfield conditions

Significantly reduce theBanana Bunchy Top Virus(BBTV) incidence

Kavino et al. (2008)

Bacillus sp., and Azospirillum strains SPS2, WBPS1 and Greenhouse study Rice blast Naureen Zakira et al. (2009)

imcC(

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Z2–7Fluorescent Pseudomonas spp. Rice field

Bacillus strain Greenhouse condition

nduced by PGPR play an important role in PGPR-mediated insectanagement by hydrolyzing chitin as this constitutes a structural

omponent of the gut linings of insects (Harish et al., 2009b).hitinases also degrade fungal cell walls and cause cell lysisRadjacommare et al., 2004).

.5. PGPR as biological fungicides

PGPR and bacterial endophytes play a vital role in the man-gement of various fungal diseases. But one of the major hurdlesxperienced with biocontrol agents is the lack of appropriate deliv-ry system. Mathiyazhagan et al. (2004) reported that Bacillusubtilis (BSCBE4), Pseudomonas chlororaphis (PA23), endophytic P.uorescens (ENPF1) inhibited the growth of stem blight pathogenorynespora casiicola. According to them, the combined applicationf BSCBE4 and ENPF1 through seedling dip and foliar spray offered

aximum control of stem blight both in vitro and in vivo. Simi-

arly, seed treatment and soil application of P. fluorescens reducedoot rot of black gram by Macrophomina phaseolina (Jayashreet al., 2000; Shanmugam et al., 2001) and panama wilt of bananaRaguchander et al., 1997). Seed and foliar application of P. fluo-

able 3hanges in physico-chemical characteristics of saline soil due to application ofyanobacterial inoculum (Nostoc calcicola).

Physico-chemicalsoil properties

Uninoculatedcyanobacterialgrowth condition

Inoculatedcyanobacterialgrowth condition

pH 10.40 5.0–8.80Organic-C (%) 0.12 0.59–0.66Total-N (%) 0.02 0.17–0.18Total-P (%) 0.03 0.03–0.3C/N ratio 6.00 3.28–4.00Na+ (ppm) 0.78 0.60

odified from Pandey et al. (2005a,b).

Rice Sheath rot (Sarocladiumoryzae)

Saravanakumar et al. (2009)

Blight of squash Zhang et al. (2010)

rescens reduced sheath blight of rice (Nandakumar et al., 2001).Manjula and Podile (2001) demonstrated that the formulationsof plant growth promoting B. subtilis AF 1 in peat supplementedwith chitin or chitin-containing materials had better control ofAspergillus niger and Fusarium udum than AF 1 alone in groundnutand pigeon pea, respectively. Strains of Burkholderia cepacia havebeen shown to have biocontrol characteristics against Fusarium spp.(Bevivino et al., 1998).

9. Contribution of cyanobacteria to agriculture andenvironmental sustainability

Due to evolutionary antiquity of cyanobacteria, they are widelyadapted to survive against various extreme environments such asdrought, salinity, low to high temperatures, etc. During phylogeny,cyanobacteria have been exposed to a variety of stresses, the mainbeing water and salt stress. Cyanobacteria are traditionally bestadapted to drought and desiccation probably through the presenceof modified vegetative cells (spores or akinetes) that are resistantto desiccation.

Cyanobacteria represent a continually renewable biomasssource that releases to the environment soluble organic substancesas extracellular products also known as secondary metabolites,which can be mineralized by the microflora and are thus beneficialto agricultural crops. These substances may be the growth promot-ers and/or inhibitors for other organisms, including soil microflora(Zulpa et al., 2003). Reports available about cyanobacteria as bio-control agents show that these organisms are effective against plantpathogens (Yuen et al., 1994). However, observations on the effects

of cyanobacteria and their metabolites on other plant pathogensunder field conditions are scarce.

Cyanobacteria occurring in chronically contaminated environ-ments (with salts, heavy metals, pesticides and other potentialtoxicants) have tendency to take up and accumulate the toxicants

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J.S. Singh et al. / Agriculture, Ecosyste

ntracellularly. The pollutant level in cyanobacterial cells can evene used as the pollution indicator. Since cyanobacteria are therincipal primary producers of diverse type of ecosystems, toler-nce of such organisms to diverse extreme environments (salinity,rought, contaminated soils, etc.) is relevant from an ecologicaliew point. However, little is known about the mechanisms per-itting cyanobacterial adaptations to such extreme conditions.ore investigation is needed to make sound predictions about the

ole of such microbes in restoration of wastelands for sustainablegriculture development. Use of successful indigenous strains ofyanobacteria as the potential biofertilizer not only improves thehysico-chemical and biological properties of the soil but also helps

n promoting yield of various agricultural crops such as rice, wheatnd pearl millet under saline, drought and contaminated agroe-osystems. Regular application of cyanobacterial strains adaptedo various extreme environments seems promising for wasteland

anagement and improvement of soil stability, nutrient status,oil microbial activities, nutrient mineralization and crop growthn ecologically sustainable manner.

Cyanobacterial biofertilizers mobilize nutritionally importantlements such as P from a non-usable to a usable form throughiological processes (Hegde et al., 1999). Cyanobacteria play an

mportant role in various chemical transformations of soils andhus, influence the bioavailability of major nutrients like P to plants.yanobacteria and PSB have been used as biofertilizer to increaserop production (Singh et al., 1997; Earanna and Govindan, 2002).n recent years, biofertilizers have emerged as promising compo-ents of the integrated nutrient supply system in Indian agriculture.he cyanobacterial ability to mobilize insoluble forms of inorganic-is evident from the finding of Kleiner and Harper (1977) who

eported more extractable P in soils with cyanobacterial coverhan in nearby soils without cover. Synergistic effects of efficientoil microbes and cyanobacteria, the excretion of organic acidso increase P availability and the decrease of sulphide injury byncreased O2 content has also been reported (Ordog, 1999).

The success of biotechnology tools mainly depends upon howuch it costs and how simple it can be during operation and uti-

ization. One of the biotechnological applications resulting fromhe development of a cyanobacterial biofertilizer technology is theroduction and distribution of cyanobacterial biofertilizers to farm-rs. Plastic bottles, polyethylene and polypropylene sachets haveeen used for distribution of liquid cyanobacterial cultures insteadf the expensive glass containers (Suresh et al., 1992). The basicdvantage of this technology is that after obtaining the soil basedtarter cyanobacterial culture, farmers can generate the biofertil-zer on their own with least extra additional inputs. Unfortunately,he outdoor cyanobacterial production technique is not so pop-lar among the farming community. Cyanobacterial biofertilizertilization is also limited due to lack of basic knowledge regard-

ng the factors involved in the success and failure of establishmentf inoculated cyanobacterial species. Detail field investigationsegarding development of efficient high quality cyanobacterial soilnocula and their application in specific regions such as saline androught-proven regions are also needed. This biofertilizer tech-ique is still limited in use and therefore, it is important to introduceyanobacterial application under field conditions for sustainablegriculture.

.1. Cyanobacteria in stability and productivity of desert soils

Dryland soils in desert and semi-arid regions suffer from major

onstraints like poor physical properties, low fertility and watereficiency (Nisha et al., 2007). Organic matter content of drylandoils is chemically and biologically less stable, and tends to decreaseery rapidly in arid regions thus leading to poor organic matterontents. Poor soil structure usually associated with low organic

d Environment 140 (2011) 339–353 345

carbon, compaction, salinity and sodicity results in reduced aera-tion and rates of water infiltration, hence more soil erodability, andthe reduced number and biodiversity of micro-flora ultimately hasthe adverse impact on plant growth and productivity.

Cyanobacterial application to the organically poor semi-aridsoil played a significant role in improving the status of carbon,nitrogen and other nutrients in the soil (Nisha et al., 2007). Highorganic-C in treated soils might be attributed to autotrophic natureof the cyanobacteria, which synthesize and add organic matter tosoil. Diazotrophic cyanobacteria which are photoautotrophic andN2-fixing improve crop production by acting as natural biofertil-izers through increase in both C and N status of soils. Biogenicsoil crusts comprising mainly cyanobacteria seem to increase soilfertility by incorporating organic matter in soil (Belnap et al.,2001). In recent years, there are several studies to show thatcyanobacterial crusts play a significant role in arid and semi-aridecosystems through C and N inputs along with several micronu-trients to improve hydrology and soil stability (Orlovsky et al.,2004). Cyanobacterial inoculations in disturbed soils have beenreported to restore the population of carbon and nitrogen cyclemicroorganisms (Acea et al., 2003). Several studies reported thatcyanobacteria produce extracellular polymeric substances (EPS)that help them to overcome conditions of water stress and alsobind soil particles (Mazor et al., 1996). Cyanobacterial sheathsand EPS also play a major role in water retention due to theirhygroscopic nature (Decho, 1990). Thus the soil microflora con-tributes to increased water holding capacity of soils (Verrecchiaet al., 1995). It has also been reported that cyanobacteria, as car-bon and nitrogen fixers, can contribute to the improvement ofsoil nutrient status in arid soils (Jeffries et al., 1992; Lange et al.,1994). Flaibani et al. (1989) reported that exopolysaccharides fromcyanobacteria also contribute to reclaimation and improvement ofdesert soils.Cyanobacteria seem to exert a mechanical effect on soilparticles by the superficial network of the trichomes/filaments aswell as enmeshing with soil particles at depth (Nisha et al., 2007).Some native cyanobacterial strains have been reported to play animportant role in improving soil aggregation, water holding capac-ity and soil aeration in paddy and several other agriculture fields(Rogers and Burns, 1994; DeCaire et al., 1997; Hegde et al., 1999).A number of studies demonstrated that cyanobacteria play a verycrucial role in bioamelioration of soils and enhancing crop yieldnot only aggregation initiation but also through protection of soilporosity due to reduction of the damaging effect of water addition(Marathe, 1972; Falchini et al., 1996). The diazotrophic cyanobac-teria contribute substantially to the fertility of the soil especiallyunder tropical paddy field conditions. However, most of these stud-ies have been carried out on paddy, and there is scanty informationregarding the possible role of bioameliorant cyanobacteria in rela-tion to other crops in semi-arid areas where paddy cannot begrown due to constraints of water availability. The native strainsof cyanobacteria in semi-arid soils showed remarkable potentialfor improving structural stability, nutrient status and productivityof the soil due to their inherent tolerance capacity under lim-ited soil moisture condition (Manchanda and Kaushik, 2000; Nishaet al., 2007). ‘Cyanocover’ produced organic matter, which increasedsoil organic C as well as water-stable soil aggregates (MalamIssaet al., 2001). Better soil aggregation in cyanobacterial bio-fertilizertreated soils may be attributed to polysaccharides produced by theblue green algae (Ahmed et al., 2000). Increase in total sugar contentin soils having a cyanobacterial mat has been found to correspondto the enhanced soil aggregation process. The cyanobacterial con-

sortium used as biofertilizer also produces abundant EPS about25% of their total biomass (Nisha et al., 2007). Algal biomass andactivity in soil crust are concentrated in the upper soil layers andEPS have gluing effect on soil particles leading to accelerates soilaggregation.

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46 J.S. Singh et al. / Agriculture, Ecosyste

EPS produced by the cyanobacteria also seem to promote thectivity of soil microflora as indicated by high soil enzymatic activ-ties. Such microbial flora, in turn, may produce more EPS, thusurther amplifying the effect. Cyanobacteria thus play a very impor-ant role in fixing C and N in soil, and have been considered verymportant for desert ecosystem. Removal of cyanobacteria fromhe arid sites reduces productivity and increases erosion by expos-ng unprotected subsurface soils to wind and water (Belnap andillette, 1997). Several workers reported that formation of algalrust by Microcoleus vaginatus and M. chthonoplastes in extremelyry climates, make significant contributions in stability of soilsCampbell, 1979; Belnap and Harper, 1995).

The above observations indicate that the application of droughtesistant indigenous strains of cyanobacterial biofertilizers at aelatively higher dose as mentioned in most of the experimentsot only improves the physico-chemical and biological propertiesf the soil but also helps in promoting crop yield under droughtnd water-limited agriculture. Applications of such cyanobacte-ial members are predicted to be very crucial for enhancing soiluality, soil nutrient status, soil microflora, nutrient mineralizationnd crop growth in desert and semi-arid soils in the ecologicallyustainable manner. The understanding of the biology of droughtesistant cyanobacteria may be useful in sustainable agriculturalnd particularity in drought crops. It is evident from the aboveoints that indigenous strains of cyanobacteria from semi-aridnvironment could be effective under a stress soil moisture-stressegime. The remarkable tolerance of cyanobacterial strains tosmotic stress can makes them successful in agriculture of aridnd semi-arid soils where scarcity of water is imminent. Further,he cyanobacterial strains, adapted to high osmotic stress condi-ions can be the suitable strategy to enhance crop productivity andeclamation of such wastelands for sustainable agriculture.

.2. Reclamation of saline wastelands by cyanobateria

Soil salinization is predicted to result in 30% loss of fertile agri-ulture lands globally within the next 25 years, and up to 50% byhe year 2050. The water-logged situation for long periods leads tooil salinization. In countries like China and India, the situation cane worst given to the increasing demand for rice as a staple food byhe indiscriminate increasing population. Diverse cyanobacterial

embers are assumed of special significance in saline soils habi-ats. Due to the morphological and genomic diversity cyanobacteriare adapted to survive in saline environments.

The remediation and rehabilitation of saline soils what are alsoxtensively distributed in India, is urgently required in order toonvert these huge wastelands to fertile lands. Physico-chemicalethods such as pyrite and sulfur or excessive irrigation usually

pplicable in the reclamation of alkaline soils, are not so effectiven the removal of soluble salts and exchangeable Na+ from the soilystem (Pandey et al., 2005a,b). Cyanobacteria can be used to reha-ilitate and reclaim the saline soils as they form a thick stratum onhe soil surface during the favourable months of rainy and wintereasons (Pandey et al., 2005a,b; Srivastava et al., 2009). The metabo-ite synthesized by cyanobacteria when incorporated in the soil,

ay help to conserve organic C, organic N, and organic P as well asoisture, and convert Na+ clay complexes to Ca2+ clay complexes

nd enhance soil properties (Singh and Singh, 1989; Venkataraman,993; Vaishampayan et al., 2001). Organic matter and N added byyanobacteria may bind the soil particles, and thus improve soilermeability, aeration and fertility. Application of mixed cyanobac-

erial inocula to saline soils showed a significant decrease in pHhile the increase in total soil N, P and organic-C (Table 3). The

rganic metabolites produced by cyanobacteria and their releasen the soil systems can be mineralized. Some degraded metabolitesan accumulate and enhance the soil organic-N content, and may

d Environment 140 (2011) 339–353

consequently maintain the soil fertility and stability year after year(Kaushik and Misra, 1989; Ladha and Reddy, 1995).Whitton andPotts (2000) demonstrated that extracellular substances producedby cyanobacteria improve the physico-chemical structures of salinesoils. The efficiency of cyanobacteria in increasing crop yields mayalso depends on the soil type. Several field experiments conductedon different types of soils showed that cyanobacteria supplementedwith 25–35% urea N were more effective for rice crop in acid, salineand red soils, than in calcareous and neutral soils (Rogers and Burns,1994). Cyanobacteria play a major role in improving soil environ-ment in addition to N2-fixation with their capacity to reclaim soilsalinity thus leading to improves organic matter content and waterholding capacity of soils and also reduced soil erosion.

Nitrogen (N) is the macronutrient required in high amounts byplants, and its availability in soils may change substantially at rel-atively short time intervals (Cameron and Haynes, 1986). For rapidgrowth of all plants, nitrogen is probably the most common limit-ing factor in saline soils. Hence, an adequate supply of N in salineagriculture field is also very important. The long-term field exper-iments showed that the use of only chemical fertilizers cannot bean efficient option to maintain and enrich the fertility of such prob-lematic soils. However, some reports indicated that use of pyritewith cyanobacteria can be the very effective corrective measuresin reclamation and enrichment of saline soils (Singh et al., 2010).Diazotrophic cyanobacteria are the dominant microflora in riceagriculture, and are presently used as a supplement to chemicalN fertilizers for rice cultivation in rice-growing countries, includ-ing India. This technology suffers from serious drawback as its useat the farm level, is not gaining universal acceptance due to somemajor problems. In order to significantly improve the efficient useof cyanobacteria as an N-based biofertilizer for rice cultivation,studies have been carried out in different dimensions both in thelaboratory and in the field (Hashem, 2001a). Cyanobacterial strainswere isolated, identified and quantified from a wide range of dis-tinctively different types of soils, viz. acid, calcareous, saline, redand neutral soils. The strains isolated were tested for their N2-fixingcapacity and growth under various stress conditions prevailing inthe rice field, e.g. pH, combined N, pesticides, salinity and nutri-ent availability in order to select suitable strains to be used asbiofertilizer. The field trials showed that cyanobacterial biofertiliz-ers may reclaim acidic and saline soils, improve the fertility statusand may supplement 25–35% N for use in rice cultivation in thesesoils. These biofertilizers may be thus recommended for enrich-ing the soil productivity of nutrient poor saline soils (Hashem,2001b). Further, the role of cyanobacteria as biofertilizers in sus-tainable agriculture recorded special significance, particularly inthe present context of high cost of chemical fertilizers (Kannaiyan,2002).

Based on the above information, it may be deduced that theapplication of biofertilizers like cyanobacteria can be a potentialagent to provide essential nutrient and organic matter to salinesoils. Although the fundamental investigations related to the affectof salinity stress and the effect of different metals on growth andphotosynthesis in cyanobacteria and field related studies on nitro-gen fixation in rice agriculture are well documented (Apte et al.,1987; Nayak et al., 2004), their application as remediating agents, isvery scare. Thus there exists an urgent need to develop the efficientand potential alkalophilic and saline tolerant cyanobacterial strainsthat can be applied as technology for reclamation and restorationfor huge unused saline waste-lands usable for sustainable agricul-ture purposes.

9.3. Cyanobacteria as potential biocontrol agents

Information about the cyanobacteria as biocontrol agents ismostly based on observations in the laboratory, and very few

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Table 4Strains of cyanobacterium Nostoc muscorum exhibiting the antagonistic effects.

Cyanobacteria Plant disease Pathogenic microorganisms References

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Nostoc muscorum strain Damping offN. muscorum strain Wood blue stainN. muscorum strain 79a White mold of lettuce (Lactuca sativa)

emonstrations have been conducted under field condition. Inodern agriculture practices, the conventional control methods

f plant diseases have not been found quite efficient due to sur-ival of the reproductive structures of pathogens in the soil. At theame time, fungicides and other artificial chemical agents inhibithe growth and development of crop plants (Nyporko et al., 2002).owever, two contact fungicides, iprodione and vinclozolin, haveeen reported with effective and successful results (Westerdijk,000). Various antagonistic microorganisms have been identi-ed for almost every life cycle stage of several plant pathogenicicrobes, and cyanobacteria it is here that are as the efficient antag-

nistic agents against several pathogenic microbes (Yuen et al.,994).

Several researches suggest that some members of cyanobacte-ia could also be used as bio-control agents against plant pathogenso obtain higher yield and good health of crop plants in agri-ulture (Zulpa et al., 2003; Biondi et al., 2004; Tassara et al.,008). Some strains of cyanobacteria (Nostoc muscorum) show-

ng the antagonistic affects against plant pathogens have beenresented in Table 4. Among cyanobacteria N. muscorum haseen shown to exert antifungal activity on soil fungi (Rhizotocniaolanii), and especially those producing damping off (DeCaire et al.,990). N. muscorum also inhibits the growth of other pathogenicungi causing the disease wood blue stain (Zulpa et al., 2003).eMule et al. (1991) demonstrated that methanol extracts andxtracellular products from another axenic strain of N. musco-um inhibited growth of Sclerotinia sclerotiorum. Tassara et al.2008) demonstrated that the bioactive compounds synthesizedy N. muscorum are the useful biological control agent for let-uce white mold caused by S. sclerotiorum and this treatment cane used for other crops having similar infection pattern. NostocTCC 53789, a known cryptophycin producer, is a source of nat-ral pesticides against the fungi such as S. sclerotiorum, insects,ematodes with cytotoxic effects (Biondi et al., 2004). Cyanobac-eria have been reported as the potential source of biologicallyctive secondary metabolites with cytotoxic, antifungal, antibac-erial or antiviral activities (Teuscher et al., 1992). However, thenvestigations about the use of these microbes as potent bio-ontrol agents and their role in control of several plant diseasesor sustainable agriculture in field conditions are still awaited inetail.

.4. Soil heavy metal bioremediation by cyanobacteria

Several chemicals are released into the soil ecosystem eithers a method of disposal or as a consequence of the technology ofheir utilization. In particular, the application of pesticides, many ofhich are toxic or contain toxic contaminants, is central to the high

ields in modern agriculture. With the advances in biotechnology,ioremediation has become one of the major developing researchrea of environmental restoration, utilizing microorganisms toeduce the concentration/toxicity of various chemical pollutantsuch as heavy metals, dyes pesticides, etc. Biological treatment

specially using cyanobacteria, for treatment of water bodies hasainfold advantages over conventional methods, as cyanobacte-

ia are cosmopolitan in environment and known to accumulateigh levels of metal/pollutant; therefore, the process involved iselatively cheap and environment friendly.

Rhizotocnia solanii DeCaire et al. (1990)Pathogenic fungi Zulpa et al. (2003)Sclerotinia sclerotiorum Tassara et al. (2008)

Biodegradation is increasingly being considered as a less expen-sive alternative to physical and chemical means of pollutantdetoxification. Pathways of biodegradation have been character-ized for a number of heterotrophic microorganisms, mostly soilisolates, some of which have been used for remediation of soil,water and other polluted sites. Because cyanobacteria are pho-toautotrophic and some also fix atmospheric nitrogen, their use fordecontamination of polluted soil systems can be a very effectivetool for sustainable and green agriculture.

Cyanobacterial strains that combine aerobic metabolism intheir vegetative cells with anaerobic metabolism in the differ-entiated cells (heterocysts), are widespread in many ecosystems,including polluted soils (Sorkhoh et al., 1992). The viability andmetabolic activity of these cyanobacteria, unlike those of het-erotrophic microorganisms, are not subject to reduction by thedecrease in concentrations of pollutants that they may break down.Cyanobacteria have been shown to degrade both naturally occur-ring aromatic hydrocarbons (Cerniglia et al., 1980) and xenobiotics(Narro et al., 1992). Kuritz and Wolk (1995) demonstrated that twofilamentous cyanobacteria (Anabaena sp., strain PCC 7120 and Nos-toc ellipsosporum) had the ability to degrade a highly chlorinatedaliphatic pesticide, lindane (g-hexachlorocyclohexane), the resultsevidenced that this ability can be enhanced by genetic engineer-ing, and provided qualitative evidence that these two strains canbe genetically engineered to degrade even chlorinated pollutant, 4-chlorobenzoate. Kuritz and Wolk (1995) for the first time reportedthat cyanobacteria can be genetically engineered to enhance theirdegradation ability of organic pollutants. Current systems forintroducing organisms for bioremediation of polluted areas arerestricted to the implementation of biodegradative microorgan-isms from soil; in general, agriculture soils contaminated withsynthetic chemicals remain largely untreated by remediation pro-grams. On the basis of previous investigations, it may be proposedthat the use of cyanobacteria can be considered for low cost,low maintenance remediation of pollutants in agriculture soils.It appears likely other biodegradative operons responsible forpollutant degradation can also be introduced and expressed incyanobacteria and the modified cyanobacteria will prove useful forbiodegradative applications in decontamination for green and safeagriculture.

Major metal pollutants which are commonly found in soil sys-tems are Cu, Zn, Ni, Co, Pb, Cr, Cd, etc. (Kaushik et al., 1999). Amongthe photoautotrophs, cyanobacteria are relatively more tolerantto heavy metals (Fiore and Trevors, 1994). The uptake of metalions (Cu, Pb, Zn, Ni, Cd, Cr, etc.) has been reported in some of theefficient cyanobacteria are: Spirulina platensis, Oscillatoria anguis-tissima, Microcystis sp., Synechococcus sp. (Verma and Singh, 1995;Rai et al., 1998; Pradhan and Rai, 2000; Yee et al., 2004). Some effi-cient cyanobacteria reported for the remediation of heavy metalspolluted soils has been presented in Table 5.

10. Role of rhizospheric microbial interactions inenvironment and agriculture sustainability

Because of current public concerns about the sideeffects ofagrochemicals, there is an increasing interest in improving theunderstanding of microbial interaction activities among rhizo-spheric microbes and how these can be efficiently used for the

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348 J.S. Singh et al. / Agriculture, Ecosystems an

Table 5Cyanobacteria reported for the remediation of heavy metals from soil systems.

Cyanobacteria Toxicants References

Spirulina platensis Cu, Pb, Zn, Ni, Cdand Cr

Greene et al. (1987)

Nostoc calcicola Cu Verma and Singh (1990)Microcystis sp. Ni and Cd Rai et al. (1998)Oscillatoria anguistissima, Cu, Pb, Zn, Ni, Cd

and CrAhuja et al. (1999)

Microcystis aeruginosa f.flosaquae strain C3–40

Cd, Cu, Pb, Mnand Zn

Parker et al. (2000)

Synechococcus sp. Cu, Pb, Ni and Cd Yee et al. (2004)Limnothrix planctonica,

Synechococcusleopoldiensis andPhormidium limnetica

Hg Lefebvre et al. (2007)

Nostoc calcicola and Cr Anjana et al. (2007)

beasa(otb

a(

of PGPR cultures and pure chemicals, these authors first reported

Fe

Chroococus sp.Lyngbya and Gloeocapsa. Cr Kiran et al. (2008)

enefit of agriculture and environment (Barea et al., 2004; Lucyt al., 2004). In soil ecosystems, beneficial microbial interactionsre responsible in the regulation of key environmental phenomena,uch as the mineralization of complex organic matters into simplervailable N, and the regulation of plant growth and productivityBarea et al., 2004). A conceptual theme showing the future rolef PGPR, cyanobacteria and rhizospheric microbial interactions inhe development of sustainable agricultural and environmental has

een demonstrated in Fig. 1.

Many studies indicate that soil microbial communities inter-ct with plant roots and soil constituents at the root soil interfaceGlick, 1995; Bowen and Rovira, 1999; Barea et al., 2002). The great

ig. 1. A conceptual theme exhibiting the role of PGPR, cyanobacteria and microbial innvironment.

d Environment 140 (2011) 339–353

array of root microbe interactions forms a dynamic environmentknown as the rhizosphere where microbial communities also inter-act. The differing physical, chemical, and biological properties of therhizospheric soil, compared with those of the root free bulk soil,are responsible for changes in microbial diversity and for increasednumbers and activity of microbes in the rhizosphere micro envi-ronment (Kennedy, 1998).

Certain microbial interaction activities can be exploited as alow-input biotechnology, and form a basis for a strategy to helpsustainable, environmentally friendly practices fundamental to thestability and productivity of both agricultural systems and naturalecosystems (Kennedy and Smith, 1995). Although it is acknowl-edged that diverse soil micro-flora and micro-fauna affect plantgrowth and aboveground food webs (Bonkowski, 2004; Scheu et al.,2005).

As PGPR and rhizobia occupy the same micro-habitats in the rhi-zosphere, they must interact during root colonization. In legumes,PGPR can improve nodulation and N2-fixation (Andrade et al., 1998;LucasGarcia et al., 2004). Field studies (Dashti et al., 1998; Baiet al., 2003), particularly those using 15N-based techniques (Dashtiet al., 1998) reinforce such beneficial interaction effects betweenmicrobial communities. PGPR enhance nodule formation impli-cates their production of plant hormones among the co-inoculationadvantages. Few Pseudomonas strains, but not all, enhanced nod-ule number and reduction of acetylene by B. japonicum in soybeanplants (Chebotar et al., 2001). Using both cell free supernatants

that plant growth regulating substances produced by PGPR affectedN2-fixation and root nodulation. These observations were furtherextended by Manero et al. (2003). The possibility that metabolitesother than phytohormones, such as siderophores, phytoalexins,

teractions in soil ecosystem for the development of sustainable agriculture and

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J.S. Singh et al. / Agriculture, Ecosystems and Environment 140 (2011) 339–353 349

Table 6Plant growth promoting rhizobacteria (PGPR) and associated plant interactions involved in the remediation of different pollutants.

PGPR Plants Sites Pollutants References

Pseudomonas fluorescens 2–79 Wheat Pot experiments Trichloroethylene(TCE)

Yee et al. (1998)

Kluyvera ascorbata SUD165,SUD165/26

Indian mustard (Brassica juncea),Canola (Brassica napus) and Tomato(Lycopersicon esculentum)

Pot experiments Ni, Pb and Zn Burd et al. (2000)

Brevundimonas sp., KR013, P.fluorescens CR3, Pseudomonassp., KR017, Rhizobiumleguminosarum NZP561

None Culture media Cd Robinson et al. (2001)

Mesorhizobium huakuii B3 Astragalus sinicus Hydroponics Cd Sriprang et al. (2003)P. putida Flav1–1, P. putida PML2 Arabidopsis Pot experiments Polychlorinated

biphenyls (PCBs)Narasimhan et al.(2003)

Azospirillum brasilense Cd,Enterobacter cloacae CAL 2, P.putidab UW3

Tall fescue (Festuca arundinacea) Pot experiments Polycyclic aromatichydrocarbons (PAHs)

Huang et al. (2004b)

P. putida UW3, A. brasilense Cd and Tall fescue (Festuca arundinacea), Pot experiment PAHs Huang et al. (2004a)E. cloacae CAL2 Kentucky bluegrass (Poa pratensis)

and Wild rye (Elymus canadensis)E. cloacae CAL2, E. cloacae UW4 Tall fescue (Festuca arundinacea) Pot experiments Total petroleum

hydrocarbons (TPHs)Huang et al. (2005)

P. fluorescens F113 Alfalfa Pot experiments PCBs Villacieros et al. (2005)A. lipoferum strains, A. brasilense

strainsWheat Pot experiments Crude oil Muratova et al. (2005)

P. chlororaphis L1391 (pOV17) andP. putida 53a (pOV17)

Mustard Microcosms Naphthalene Anokhina et al. (2006)

Pseudomonas sp., A4, Bacillus sp. 32 Indian mustard Pot experiments Cr Rajkumar et al. (2006)Bacillus subtilis SJ–101 Brassica juncea Pot experiments Ni Zaidi et al. (2006)Azotobacter chroococcum HKN–5, B.

megaterium HKP–1, B.mucilaginosus HKK–1

Brassica juncea Pot experiments Pb and Zn Wu et al. (2006)

P. putida UW4,HS–2 Transgenic canola (Brassica napus) Field study Ni Farwell et al. (2007)Bradyrhizobium sp., (vigna) RM8 Green gram (Vigna radiate) in vitro conditions Ni and Zn Wani et al. (2007)Pseudomonas sp., M6, P. jessenii

M15Castor bean (Ricinus communis) Pot experiments Ni, Cu and Zn Rajkumar and Freitas

(2008b)Pseudomonas sp., 29C, Bacillus sp.

4CIndian mustard Greenhouse condition Ni Rajkumar and Freitas

(2008a)Psychrobacter sp., SRA2, SRA1 and

B. cereus SRA10Brassica juncea and B. oxyrrhina Pot experiments Ni Ma et al. (2009a)

A. chroococcum HKN–5 and B.megaterium HKP–1

None Solution Pb and Cd Wu et al. (2009)

B. pumilus ES4, B. pumilus RIZO1,and A. brasilense Cd

Atriplex lentiformis Greenhouseexperiments

Phytostabilizing minetailings

DeBashan et al. (2010)

Bradyrhizobium sp., Pseudomonas Lupinus luteus in situ Phytostabilisation of Dary et al. (2010)

Po

a2at

1

iepcdqp

ptoaeNd

sp. and Ochrobactrum cytisi

Achromobacter xylosoxidans Ax10 Brassica juncea

nd flavonoids, might enhance nodule formation (LucasGarcia et al.,004), but this hypothesis has not been verified. Some PGPRs andssociated plant interactions, effective in the remediation of variousoxicants from different sites are given in Table 6.

1. Conclusions

An ideal agricultural system is sustainable if maintains andmproves human health, benefits producers and consumers bothconomically and spiritually, protects the environment, androduces enough food for an increasing world population. Indis-riminate population growth, land degradation and increasing foodemand, sustaining agricultural production through improved soiluality management is critical to the issue of food security andoverty alleviation in most, if not all, developing countries.

The high cost of chemical nitrogenous fertilizers and the lowurchasing power of most of the farmers restrict its optimal usehus hampering crop production. Besides, a substantial amount

f the urea N is lost through different mechanisms includingmmonia voatilization, denitrification and leaching losses, causingnvironmental pollution problems. The utitilization of biological2-fixation technology can decrease the use of urea N, prevent theepletion of soil organic matter and reduce environmental pol-

heavy metal pollutedsoils

t experiments Cu Ma et al. (2009b)

lution to a considerable extent. Different bio-fertilizers systemsthat include PGPR and cyanobacteria are in use on a limited scaleparticularly in rice agroecosystems. Before largescale extension ofmicrobial biofertilizers systems at the farm level, further researchis needed to determine their N supplement potentials.

Worldwide, considerable research progress has been achievedin the area of bacterial and cyanobacterial biofertilizer technology.It has also been demonstrated and proven that this technologycan be the very effective and potential means for enriching soilfertility and enhancing rice agriculture yield. However, the tech-nology needs further improvement for its better exploitation undersustainable agriculture development programs. Cyanobacteria andPGPR are excellent model systems that can provide the biotech-nologist with novel genetic constituents and bioactive chemicalswith multifact use in agriculture and environmental sustainabil-ity. Current and future progress in our understanding of PGPRand cyanobacteial diversity, colonization ability, mechanisms ofinteractions, formulation and application could facilitate their

development as the reliable components in management of sus-tainable agricultural systems.

PGPR and cyanobacteria offer an environmentally sustainableapproach to increase crop production and health. The use of molec-ular techniques has enhanced our capacity to understand and

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A

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50 J.S. Singh et al. / Agriculture, Ecosyste

anage the rhizosphere ecosystems, and may lead to new prod-cts with improved effectiveness. Genetic enhancement of PGPRtrains with enhanced colonization and effectiveness, may involveddition of one or more traits associated with plant growth promo-ion. Genetic manipulation of host crops for root-associated traits tonhance establishment and proliferation of beneficial microorgan-sms is being pursued. Health and safety testing are also requiredo address such issues as the non-target effects on other organismsncluding toxigenicity, allergenicity and pathogenicity, persistencen the environment and potential for horizontal gene transfer.

cknowledgements

Authors are very thankful to Professor S.P. Singh, Centre ofdvanced Study in Botany, Banaras Hindu University, Varanasi foris help in revision and editing the manuscript. The authors thankhe Head, Department of Environmental Science, Babasaheb Bhim-ao Ambedkar (Central) University, Lucknow-226025 for providingnfrastructural facilities. This work was possible through grantsiven to Dr. Jay Shankar Singh as Senior Research Associate [Sci-ntist’s Pool Scheme; CSIR sanction No. 13 (8243-A)/Pool/2008]y Council of Scientific and Industrial Research, Human Resourceevelopment Group, Government of India, New Delhi. Vimalhandra Pandey is thankful to University Grants Commission, Gov-rnment of India, New Delhi for financial support.

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