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Biosurfactants as a Biological Tool to Increase Micronutrient Availability in Soil:A Review

更新时间:2016-07-05

INTRODUCTION

Micronutrients are essential substances that are required in small amounts for human and plant health(Miller and Welch,2013).Micronutrients are also known as minor components or trace elements,but the term micronutrient is supported by the American Society of Agronomy and the Soil Science Society of America(Dubey,2011).The micronutrients include boron(B),copper(Cu),iron(Fe),chloride(Cl),manganese(Mn),molybdenum(Mo),nickel(Ni),and zinc(Zn)(H¨ansch and Mendel,2009).

Micronutrient deficiencies are a major global problem for soils/plants that affects both food production and human health.Typically,deficiencies of Fe,Mn,and Cu are less extensive than that of Zn(Imtiaz et al.,2010).In an examination of soils from several Indian states,Fe deficiency was observed to be the greatest in Haryana(26%)followed by Tamil Nadu(18%),Punjab(12%),Gujarat(8%),and Uttar Pradesh(9%)(Rajamani,2014).In addition to India,other countries such as Australia and China are also facing a soil micronutrient deficiency problem.This widespread micronutrient deficiency problem increases the challenge that worldwide agriculture is facing of adequately feeding and supplying healthy food for people of over 7 billion,a number which is expected to reach over 9 billion by 2050(FAO,2011).Such an expansion in the human population intensifies the pressure for increased food production(Baligar and Fageria,2015;Glick,2015).If the essential nutrients required for agriculture cannot be supplied in sufficient amounts,this will result in the development of widespread human malnutrition(Miller and Welch,2013).Micronutrients are used by plant physiological process in very small amounts,but are nevertheless important in plant growth and development and crop production(Shukla et al.,2014).These nutrients support biological processes such as protein synthesis,gene expression,auxin metabolism,maintenance of biological membranes,and protection against photooxidative damage,heat stress and disease.Thus,insufficient nutrients negati-vely affect crop yield,food quality,and human health(Alloway,2004;Yang et al.,2007;Das and Green,2013).The abilities of different plants to take up individual micronutrients from the soil vary,notwithstanding micronutrient concentrations in plants reflect the nutrient status of the soils where the plant are grown(Knez and Graham,2013).Successful agriculture therefore requires that soils contain sufficient levels of key micronutrients(Knez and Graham,2013).Inadequate levels of soil micronutrients have recently increased significantly in many localities due to the use of continuous cropping systems and decreased applications of organic matter(such as bioslurry and farmyard manure)in favor of chemical fertilizers,which can degrade the physical,chemical,and biological status of top soils(Fageria et al.,2003,2007).

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The presence of micronutrients in soil does not mean that plants will grow and develop well because some of the micronutrients may be tightly bound to soil particles and therefore unavailable to the plants(Knez and Graham,2013).Manufactured chemical fertilizers are typically soluble and fast acting.They contain high-analysis materials,have a high level of plant nutrients with few impurities,have a quick response in the field,and are typically highly soluble in water(Siegel et al.,1962;Silva,2000).However,manufactured fertilizers can become inactive in alkaline soil and therefore unable to be absorbed by plants(Osman,2013).In an effort to overcome this problem,many chemical solutions have been tested for the ability to decrease the binding of ionic micronutrients to soil particles and thereby enhance their availability to plants.In this regard,the solubility and disintegration energy of soil particles rely upon their surface area(Milani et al.,2015).The availability of micronutrients in soil depends on their solubility and their ability to be mobilized(Chatzistathis,2014).In this regard,there are many soil factors affecting the solubility of micronutrients and their accessibility for plants,including soil type,texture,moisture,temperature,pH,organic matter,calcium carbonate,cation exchange capacity(CEC),and structure(Schoonover and Crim,2015).

Chelates or chemically synthesized surfactants are typically used in soil washing;they are often a chemical complex that is lipid in nature in which the metals are held so tightly that it is easily taken up by plant roots(Sahoo,2007).Unfortunately,chemically synthesized surfactants/chelators are often toxic,and many are able to persist in the environment for a long time(Jessop et al.,2015).On the other hand,there are many naturally occurring chelating/complexion/solubilizing agents that are produced by living organisms(plants and microbes),e.g.,biosurfactant,a multifunctional microbial metabolite,and have been described as green surfactants owing to the perception of them being environmentally friendly and biodegradable(Sinha et al.,2008).Biosurfactants have the potential to enhance metal bioavailability in soils(Mulligan et al.,2001),and compared to synthetic surfactants,they can have higher foaming,higher selectivity,and higher specific activity at elevated temperatures,pH,and salinity(Desai and Banat,1997;Makkar and Cameotra,1997;Brennan and Shelley,1999).At the critical micelle concentration(CMC),biosurfactants decrease the surface tension,increase the solubility and mobility of ionic metals,and enhance the micronutrient availability in soil(Pacwa-P′lociniczak et al.,2011).There are very few published reports on the use of biosurfactants in agriculture,and therefore more detailed study is required to evaluate their potential.This review examines the role,application,and effects of biosurfactants on micronutrient solubility,availability,and uptake in plants and their potential to resolve the problems of micronutrient deficiency in soil.

SOURCES OF MICRONUTRIENTS IN SOIL

Methods of providing micronutrients to plants typically include the use of organic matters such as grass clippings,tree leaves,and green manure(Welch et al.,1991;Sekhon,2003)(http∶//www.ncagr.gov).However,a more complete list of sources is as follows.

Natural sources

Geologic parent material or rock outcroppings(Morales,1974),volcanoes(Seaward and Richardson,1989),and forest and prairie fires are natural sources of micronutrients in soil.The micronutrients in the soil and their availability to plants are determined by the minerals contained in the original parent material and by the weathering processes that have taken place over the years(Wuana and Okieimen,2011).

Agricultural sources

Manures are a common source of micronutrients in soil(Wuana and Okieimen,2011).Incorporation of the following amendments enhance the macro/micronutrient supplement contents in soil∶compost,crop residues,silage juice,ruined remains of crops and plants,wash water,beddings,spent mushroom media,spent soilless media,and spent supplement solutions(https∶//www.bcac.bc.ca)(Zu et al.,2005).

Industrial sources

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Domestic effluents

Effluents from domestic waste/municipal sewage treatment plants often contain high levels of nutrients that potentially could be used for plant growth(Table I).Agricultural processing of effluents could provide water and nutrients for crop production(Chambers et al.,2002);the nutrient-enriched sewage effluent could substantially reduce the use of chemical fertilizers(Wang and Tao,1998;Ladwani et al.,2012).Sewage effluent,in addition to being a source of irrigation water,is a potential source of micronutrients for plants;consequently effluent application can increase the concentration of micro-and macronutrients in soil(Asgharipour and Reza Azizmoghaddam,2012).

DEFICIENCY STATUS OF MICRONUTRIENTS IN SOIL AND ITS IMPACTS

It is estimated that the more than 3 billion people worldwide suffer from nutrient deficiency(Monreal et al.,2015).Deficiencies of micronutrients in soil and plant are a global nutritional problem and are prevalent in many countries(Cakmak,2002;Imtiaz et al.,2010).Iron deficiency generally occurs in citrus orchards and sugarcane plants grown on calcareous soils,and Mn deficiency is generally observed in plantation crops such as cardamom and tobacco.These deficiencies occur due to specific soil and climatic conditions existing at the time of crop growth,substantially affecting the crop yield.

Despite adequate soil preparation,watering,and mulching,if plants fail to grow or multiply,it can be a sign of multiple nutrient deficiencies in soil/plant.Jyothi(2014)compile the data for survey and analysis of more than 250000 soil samples in 20 Indian states(Table II).Micronutrient deficiencies in humans result in anemia,decrease immunity,decrease resistance to infection,impede growth and development of the nervous system,and increase susceptibility to other diseases which slow the growth of children(Swaminathan et al.,2013).

It is well known that micronutrient deficiencies in agriculture soil affect the growth of plants and the nutrient levels of crops.Micronutrients related to agriculture not only are essential for crops,but also affect livestock(Knez and Graham,2013).Micronutrient deficiencies in agricultural soils have become a major constraint to the soil efficiency,stability,and sustainability(Bell and Dell,2008;Kumar and Babel,2011).The percentages of agricultural soils suffering nutrient deficiencies have been estimated at 49%for Zn,31%for B,15%for Mo,14%for Cu,10%for Mn,and 3%for Fe(Cakmak,2002;Alloway,2004;Graham,2008).In this regard,nearly 50%of the world’s cultivated area supports suboptimal growth because of the lack of plantavailable Zn in the soil.Calcareous soils or high-pH soils are prone to Zn sequestration,while sandy or other coarse soils are prone to Zn leaching(Adams and Sun,1971;Marschner,2011).These basic soil characteristics have been found throughout India in Bihar(calcareous soils),Andhra Pradesh(Vertisols),Tamil Nadu(Inceptisols),Karnataka(Al fisols),Maharashtra(Lateritic soils),and Haryana(Aridisols),where low crop yields have also been observed(Subba Rao et al.,1996).High pH reduces the solubility and mobility of Zn in soils by stimulating its absorption to soil constituents and limiting its diffusion to plant roots(Sherene,2010).

Some synthetic surfactants,e.g.,linear alkylbenzene sulphonates(LAS)and alkylphenol ethoxylates(APE),are known to exhibit estrogen-like properties,possibly linked to a decreasing male sperm count and carcinogenic effects(Scott and Jones,2000;Edwards et al.,2003).While there is little serious risk to the environment from the commonly used anionic synthetic surfactants,cationic synthetic surfactants are known to be more toxic,and at present there is a lack of data on the degradation of cationic synthetic surfactants and their fate in the environment(Scott and Jones,2000;McGuire and Compton,2002;Mungray and Kumar,2009).Anionic synthetic surfactants(SDS)may change the structure of DNA or polypeptide chains as well as the surface charge of molecules in living organisms through binding to bioactive macromolecules such as peptides,enzymes,and DNA(Cserh´ati et al.,2002;Ivankovi´c and Hrenovi´c,2010).These changes can cause modifications in biological functions to occur(Cserh´ati et al.,2002).Cationic synthetic surfactants mainly target the cytoplasmic membrane on any microorganism present in the soil quaternary ammonium compound(QAC)which acts to disorganize the inner membrane through their long alkyl chains(McDonnell and Russell,1999).Synthetic surfactants in the nonionic category directly bind to different protein and phospholipid membranes and hence have antimicrobial activity.This binding increases the permeability of membrane and vesicle,resulting in loss of low-mass molecules(Contreras et al.,2006)and ultimately in cell death through the loss of ions and amino acids(Cserh´ati,1995).Nonionic and cationic synthetic surfactants adsorb to soil and sediment to a greater extent than anionic synthetic surfactants.Most surfactants in soil can be degraded by some species of microorganisms;however,anaerobic conditions might make them more persistent(Scott and Jones,2000;Ying,2006).Mungray and Kumar(2008)reported that synthetic surfactants enter the environment through discharge of sewage effluents into surface waters and through application of sewage sludge on land(Mungray and Kumar,2008,2009).High concentrations of synthetic surfactants and their byproducts are often very toxic,and they can also alter the composition of soil biota.Environmental risks posed by synthetic surfactants and their degradation byproducts can be assessed in terms of toxicity based on the comparison of the predicted environmental concentration and the predicted no-effect concentration.Nevertheless,more toxicity data are needed for terrestrial risk assessment of synthetic surfactants and their degradation products(Ying,2006;Cirelli et al.,2008).Many synthetic surfactants pose significant environmental risks due to their harmful chemical compounds and their incomplete degradation in water and soil.Synthetic surfactants are reported to cause long-term adverse effects,while bio-based products are more likely to degrade easily and therefore not pollute the environment(Ying,2006).

Deficiency effects on plants

The deficiency of any single micronutrient in soil can constrain plant growth and reduce yield,notwithstanding the sufficient availability of other essential micro-and macronutrients(Hodges,1996).All nutrients have specific and essential functions in plant metabolism(Maathuis and Diatloff,2013).Micronutrient deficiencies in soil tend to be harder to reliably detect than macronutrient deficiencies,but they enhan-ce the strong development of crops,delivering higher yields and harvest quality.An adequate supply of micronutrients also increases hereditary potential of plants.More specifically,sufficiency or deficiency of micronutrients has a significant effect on root and shoot growth,seed viability,and food quality.Their toxicity or insufficiency can bring about hindered development,low yield,and even plant death.

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Deficiency effects on food supply

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Impacts of micronutrient deficiency in human

Malnutrition in human develops when micronutrients are not supplied through food in sufficient amounts(Miller and Welch,2013).Worldwide,more than two billion people suffer from one or more micronutrient deficiencies(Popkin et al.,2012).In developing countries,micronutrient deficiencies in human are now a massive and rapidly growing health problem,especially among poor people,affecting around 40%of the world population(Buyckx,1993;Ramalingaswami,1995).Welch(2002)pointed out that the Zn,Fe,Cu,and iodine(I)deficiencies in plant and animal can cause growth retardation,delayed skeletal and sexual maturity,dermatitis,diarrhea,alopecia,and defects in immune function with a resulting increase in susceptibility to infection.Iron deficiency can cause nutritional anaemia,problem pregnancies,stunted growth,and lowered resistance to infections(Welch,2002).

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TABLE II Extents of deficiencies of nutrients in soil for crop production(source:Jyothi,2014)

Nutrient Extent of deficiency%N 26–63 P 38–42 K 13–37 S 35–40 Zn 49 Fe 13 B 33

ACCESSIBILITY OF PLANTS TO MICRONUTRIENTS

The physical and chemical properties of soils such as soil texture,pH,CEC,anion exchange capacity(AEC),and moisture contents are closely related to the mobility of nutrients in soil,which increases the availability of these nutrients to plants.Micronutrient deficiencies occur not only because of insufficient amounts present in soil,but also may occur due to poor solubility,which may be affected by soil organic matter content,pH,adsorptive surface,texture,and nutrient interactions(Ayele et al.,2013).Sustainable productivity of an agroecosystem is determined by soils and their physical,chemical,and biological properties.The sustainability of soils depends on their capacity to supply required nutrients to the developing plants;micronutrient deficiencies in soils decrease plant strength,productivity,and(for perennials)future sustainability(Bell and Dell,2008).Increasing or decreasing the range of soil pH affects the micronutrient availability to plants and is considered to be a major factor for nutrient deficiency.Soils of high pH ranges(6.5)may have limited nutrient availability to plants,therefore requiring fertilizer amendment(Poh et al.,2009).Solution theory holds that any ion in soil solution is available to plants if their roots are capable of absorbing it(Alloway,2004);ions must pass into solution and move to plant roots by diffusion or mass flow of water before being absorbed through symplastic,apoplastic,and foliar ion pools(Foster,1990;Silva,2000).Market research shows that over 90%of farmers know that they have a problem with nutrients in soil being unavailable to plants(Hodges,1996;Aref,2012).Therefore,farmers generally add phosphorus and Zn fertilizers to agricultural soils to increase crop productivity(L´opez-Rayo et al.,2012;Rawashdeh and Sala,2013).On the other hand,these two elements are often tied up with other compounds and become less available to plants,which results in losses of farmers.Chelation/solubilization enhances the accessibi-lity of supplements in both manure and in soils(Alley et al.,2010;Malik et al.,2012).In this way,the surfactant is the most vital part of any chelating compounds.The word surfactant means surface-active compound.Surfactants unbind trace metals from the soil surface,and chelating agents surround the trace metal ions and keep them in solution.A method of sequestering micronutrients and providing them to a plant comprises applying an effective amount of a plant fertilizer comprising a surfactant composition to an area of the plant or soil/substrate surrounding the plant(Bansiwal et al.,2006)and subsequent formation of coordinate bonds with the micronutrients.The surfactant then transports the micronutrients across plant membranes and releases the micronutrients for use by the plant(McLaughlin et al.,2012).Bansiwal et al.(2006)reported surfactant-modified zeolite as a carrier for fertilizer and for the slow release of phosphate.Zeolite was modified by the addition of hexadecyltrimethylammonium bromide,a cationic surfactant,to modify its surface to increase its capacity to retain anions(e.g.,

GENERAL DESCRIPTION OF SURFACTANTS

Biosurfactants,through their accumulation at the immiscible fluid interfaces can reduce surface tension,increasing the surface area of such compounds with di-fferent degrees of polarity and allowing increased mobility,bioavailability,and biodegradation(Banat et al.,2000).Biosurfactants can be effectively used to solubilize,mobilize,and increase the availability of micronutrients and trace metals in deficient soil(Maier et al.,2001;Sheng et al.,2008).Cationic,anionic,and nonionic surfactants contain both hydrophobic and hydrophilic portions,making them ideal for solubilization of hydrophobic compounds(Georgiou et al.,1992;Makkar and Cameotra,2002).Different types of biosurfactants,low-and high-molecular-mass biosurfactants,have different physical characteristics.For example,low-molecular-mass biosurfactants lower the surface and interfacial tension and are effective in solubilizing metals in water and soil,as well as reducing repulsive forces between two non-similar phases.On the other hand,high-molecular-mass biosurfactants are able to reduce repulsive forces between two immiscible compounds through higher emulsification activity,making it easier for them to mix(Calvo et al.,2009;Sober´on-Ch´avez and Maier,2011).

Surfactants can be categorized into synthetic surfactants and biosurfactants.Synthetic surfactants are manually chemically synthesized,and biosurfactants are biologically synthesized.

Fig.1 Surfactant/biosurfactant monomers corresponding to their ionic properties,nonionic(1),anionic(2),cationic(3),and zwitterionic gemini(4)surfactants(a),and different types of micelle formations by aggregation of biosurfactant monomers,reverse(1),normal(2),mixed(3),and liposomic(4)micelles(b).

Synthetic surfactants and their environmental hazards

Synthetic surfactants are classified into three types∶anionic(the polar group is usually either sulphate,sulphonate,or carboxylate),cationic(the polar group is a quaternary ammonium ion),and nonionic(the polar group is polyoxyethylene,sucrose,or polypeptide).The hydrophobic chains of these three types of synthetic surfactants include olefins,alkylphenols,paraffins,and alcohols(Volkering et al.,1997).The most common synthetic surfactants which are used in trace metal/micronutrient solubilization in soils are sodium dodecyl sulfate(SDS)(Romanell et al.,2004;Shin,2004;Sun et al.,2011),Triton X-100(TX100)(Shin,2004;Chang et al.,2005),cetyltrimethylammonium bromide(CTAB)(Sun et al.,2011),Tween-80(TW80)(Sun et al.,2011;Dong et al.,2013),and sodium N-lauroyl ethylenediamine triacetate(LED3A)(Chang et al.,2005;Qiao et al.,2016).Table III shows the different ionic properties of some synthetic surfactants.

Unfortunately,synthetic surfactants may have a negative impact on the environment during their lifecycle.Typically,production,formulation,use phase,and discharge phase are counted as parts of their life-cycle.In the first two phases(production and formulation),the amounts of chemicals released or emitted into the environment(Mungray and Kumar,2008,2009)may bioaccumulate,and their production processes and byproducts can be environmentally hazardous(Banat et al.,2000).

TABLE III Ionic properties of some synthetic surfactants

a)Surfactants that are composed of two hydrophilic and two hydrophobic groups(Molinaro et al.,2002).

Synthetic surfactant Ionic property Reference Tween-80Nonionic Dhote et al.(2013)Sodium dodecyl sulphate(SDS) Anionic Xia et al.(2009)Cetyltrimethylammonium bromide(CTAB) Cationic Mohammad et al.(2003)Triton X-100 Nonionic Zhang et al.(2014)Zwitterionic geminia) Dipolar ionic Malik et al.(2011)

Systematic survey and analysis of more than 2.5 million soil samples in 20 Indian states by the All India Coordinated Research Project indicates a deficiency to the extent of 49%for Zn and 33%for B,with 13%,7%,and 4%of the samples rating low in Fe,Mo,and Mn,respectively(Shukla et al.,2015).These data reveal nutrient deficiencies in many soils,the seriousness and extent of which varies over agro-ecological zones,soil types,and,most importantly,management practices,crop yields,and cropping systems.Micronutrient deficiencies in soil affect different living systems as described in detail below.

Biosurfactants

The increasing demand for environmentally friendly products and favourable regulatory outlook from developed countries are some of the driving factors in the market of mannosylerythritol lipid.This biodegradable natural surfactant obtained from microbes can be an attractive alternative to synthetic surfactants in micronutrient-deficient soil(Pacwa-P′locinicz et al.,2011;Ehrhardt et al.,2015;Mnif and Ghribi,2016).Therefore,there is a need to identify and evaluate chelators/solubilizers with potentially good micronutrient-solubilizing efficiency and environmental compatibility,i.e.,biosurfactants.There are three different types of biosurfactants(Fig.2)∶i)glycolipids(glucose+lipid),e.g.,rhamnolipid and sophorolipid,ii)lipopeptides(protein+lipid),e.g.,surfactin and mycosubtilin,and iii)phospholipids(phosphate+lipid),e.g.,sphingomyelin and lecithin.

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Biosurfactants are amphiphilic molecules that are produced by some plants,but mostly by microorganisms(bacteria,fungi,and yeasts).They are exuded into the extracellular space and act as surface-active agents that reduce surface and interfacial tension between individual molecules at the surface and interface,respectively(Ivshina et al.,1998;Hwang et al.,2009).Some are produced as fermentation byproducts(Kitamoto et al.,2009).They accumulate at the interface between two immiscible liquids(e.g.,oil and water),between a liquid and a solid(e.g.,soil and oil)or between two solids(e.g.,soil and metal).Biosurfactants then reduce the surface and interfacial repulsive forces between the two dissimilar phases and allow these two phases to become miscible.Interest in biosurfactants emanates from their potential for wide applicability and their advantages over synthetic surfactants(Desai and Banat,1997;Banat et al.,2000;Rodrigues et al.,2006;Singh et al.,2007).A large number of different microorganisms can produce surface-active compounds that vary in their chemical properties as well as molecular size(Table IV).

Biosurfactants can be monomeric or polymeric and particulate compounds.The most promising and effective biosurfactants at the present time are surfactin,a lipopeptide from Bacillus subtilis,rhamnolipid,a glycolipid from Pseudomonas aeruginosa,and sophorolipid,a glycolipid from Torulopsis bombicola(Mulligan et al.,2001).Several reviews on microbially produced surfactants have focused on their types and commercial potentials(Banat et al.,2000),their natural roles(Ron and Rosenberg,2002),their applications in sustainable development(Mulligan,2005),their use in the production of inexpensive compounds(Haba et al.,2000;Dubey and Juwarkar,2001;Nitschke et al.,2007),and their use in medical applications(Singh and Cameotra,2004;Rodrigues et al.,2006).Although microbes can grow anywhere on a very wide variety of substrates,the yield of biosurfactants depends on nutritional and physical conditions provided(Haba et al.,2000;Dubey and Juwarkar,2001;Singh and Cameotra,2004;Rodrigues et al.,2006;Nitschke et al.,2007).

Fig.2 Chemical structures of some common biosurfactants,rhamnolipid and sophorolipid(glycolipid),surfactin and mycosubtilin(lipopeptide),and sphingomyelin and lecithin(phospholipid)(Salihu et al.,2009).

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BIOSURFACTANT PROPERTIES

Chemical properties of synthetic surfactants can be similar to those of biosurfactants with regard to foaming ability,emulsification,lubricity,surface tension reduction,solubilization,etc.However,biosurfactants,produced by microorganisms,are biodegradable and less toxic compared to many synthetic surfactants(Desai and Banat,1997;Mnif and Ghribi,2016).They also have better foaming properties and higher selectivity(Edwards et al.,2003;Mulligan,2005).

Biosurfactants are considered as very promising biotechnological products.The use of biosurfactants instead of synthetic surfactants in many applications allows for high levels of specificity as well as efficiency.Biosurfactants are good wetting agents and emulsifiers,having several advantages over synthetic surfactants including effectiveness over a wide range of temperature,pH,and salinity(Kosaric,1992;Das et al.,2008;Pacwa-P′lociniczak et al.,2011)and synthesis under user-friendly conditions(e.g.,low temperature and pressure).Biosurfactants are described by properties including critical micelle concentration(CMC),hydrophilic-lipophilic equalization(HLE),chemical structure,and charge and also properties from their biological source(Van Hamme et al.,2006).Some useful properties of biosurfactants are described as follows.

Critical micelle concentration

Critical micelle concentration is the concentration at which all of the molecules in a surfactant will exist as micelles(even in very small quantities).Formation of micelles needs a very low concentration in water,and for the potential application,these micelles are needed in a very low amount,i.e.,the CMC(Barros et al.,2007;Kumar and Lal,2014;Ehrhardt et al.,2015).Capacity to form micelles from monomers(estimated colloidal clusters)in any liquid solution because of the presence of hydrophilic and hydrophobic groups in a monomer molecule in a concentrated form is also a basic characteristic of biosurfactants(Rangel-Yagui et al.,2005;Ying,2006).Subsequently,the CMC is the most critical parameter for any biosurfactant in terms of its capability for solubilization of hydrophobic pollutants in contaminated soil.The wide use of biosurfactants in different industrial fields(cosmetic,medicinal,environmental agriculture,laundry,etc.)is due to their tendency in various media to form micelles.

As described previously,soil micronutrient de ficiencies can lead to lower crop yields(Rehm and Schmitt,2002;PAIS,2012).During the past decade,micronutrient status has been ascertained primarily for Zn and to a lesser extent for B and Mo(Narwal et al.,2013;Bailey et al.,2015).Deficiency of Zn is widespread in Asia(Turkey,India,China,and Indonesia),sub-Saharan Africa,and the northwestern region of South America(Cakmak,2002;PAIS,2012)(https∶//www.iatp.org).Modern,highly productive,pathogen-resistant crops that also demonstrate tolerance against environmental stresses such as drought and ultraviolet(UV)rays have,since the green revolution,dominated the food supply(WHO,2005).Insufficiencies of micronutrients in soils have now turned into a limiting factor for yield and productivity in most agricultural fields around the world.Furthermore,many food systems in developing countries cannot provide sufficient micronutrients to meet the demands of their citizens,especially low-income families(Khoshgoftarmanesh et al.,2010).

The amphiphilic nature of biosurfactant molecules allows them to partition at surface interfaces and reduces surface and interfacial tension.The surface tension of water was found to be reduced even through exposure to low concentrations of biosurfactants(Law and Kunze,1966).Biosurfactants can reduce the surface tension of water from 72 to 30 mN m1or less of liquid-liquid interfaces such as oil-water interfaces.Researchers also found that biosurfactants have the ability to reduce the interfacial tension to as low as 1 mN m1(Mulligan,2005).There is no further reduction in surface or interfacial tension above the CMC.At the CMC,the biosurfactant molecules themselves assemble to form structures such as vesicles,bilayers,and micelles.Formation of CMC is dependent on pH,ionic strength,and temperature.Biosurfactants exhibit low CMC with the values ranging from 0.15 to 30 mg L1(Desai and Banat,1997;Pichot et al.,2013).Biosurfactants with lower CMC values are better and more efficient than their synthetic counterparts(Figs.1 and 3).

Surface and interfacial tension of biosurfactants

Along with increasing environmental concern among consumers,governmental legislation forces industry to search for easily biodegradable microbially produced surfactants(Cameotra and Makkar,1998;Nitschke and Costa,2007).Chemically synthesized surfactants are generally non-biodegradable,while biosurfactants such as sophorolipids,surfactins,and arthrofactins are rapidly degradable in the environment(Hirata et al.,2009).Mohan et al.(2006)indicate that microbially produced biosurfactants are easily degraded and are particularly suited for environmental applications such as nutrient solubilization and bioremediation.Conversely,Pei et al.(2009)studied the degradation of rhamnolipids by incubation in black loamy soil and red sandy soil for 7–8 d and concluded that the degradation rate was slow(Pei et al.,2009;Lima et al.,2011).

从图13可以看出,由斜拱加载引起的围护桩桩身水平位移增量随斜拱加载时基坑开挖深度Z的增大而减小。斜拱加载引起的围护桩桩身水平位移增量最大值出现部位随斜拱加载时基坑开挖深度的增大逐渐下移,最大值出现部位集中在围护桩中上部,所以当基坑开挖较浅时要及时架设支撑,防止围护桩变形过大。

The movement of micronutrients in soil is mainly controlled by solid-liquid interfacial reactions between the surface of soil particles and the metal in soil water.Therefore,when we deal with micronutrientdeficient soils,it is essential to understand how trace metals/nutrients behave at the solid-liquid interface(Fig.3).

无土栽培基质蒸汽消毒机主要包括蒸汽制备输送、基质搅拌和蒸汽消毒机控制系统3大部分。无土栽培基质蒸汽消毒机底盘下部装有4只充气轮胎,底盘一端配有牵引钩,拖拉机通过牵引钩牵引无土栽培基质蒸汽消毒机在各温室之间移动。农民购置该机可以进行跨区作业服务。

Solubility and mobility of biosurfactants

Compounds that decrease the surface tension of a fluid and the pressure at the interface between two fluids or between a fluid and solid are known as surfactants.These are usually amphiphilic organic compounds containing hydrophobic tails and hydrophilic heads(Fig.1).The basic structure of a surfactant contains hydrophilic(water-soluble)and hydrophobic(water-insoluble)components,which is achieved using mono-,di-,and polysaccharides and unsaturated and saturated fatty acids,respectively.The ability of a surfactant to develop micelles in solution through the monomers gives detergent and solubilizing properties to the surfactant in metal-deficient soil,which can be formed in four different types according to the condition,i.e.,normal,reverse,liposomic,and mixed micelles(Fig.1).

Stability of biosurfactants under different environmental conditions

Most of the biosurfactants and their surface activity are resistant towards changing environmental conditions such as temperature and pH(Vijayakumar and Saravanan,2015).McInerney et al.(1990)found that lichenysin produced by Bacillus licheniformis is effective at a temperature of up to 50°C,over the pH range of 4.5–9.0,and at up to 50 g L1NaCl or 25 g L1 CaCl2.In addition,a biosurfactant from Arthrobac-ter protophormiae was found to be stable at 30–100°C and at pH 2–12(Singh and Cameotra,2004;Vijayakumar and Saravanan,2015).Similarly,Sudha et al.(2010)observed that sophorolipid production and stability from Candida tropicalis was optimum at 30°C.Moreover,the optimum temperature for bioemulsifier production and stability was found to be from 37 to 100°C(Jagtap et al.,2010).Below pH 7 and at a temperature of 20°C,lipopeptide from B.subtilis LB5a was stable after autoclaving(121°C,20 min)and after 6 months at 18°C;in addition,the surface activity did not change between pH 5 and 11 and between 0%and 20%NaCl(Nitschke and Pastore,2006;Nitschke and Costa,2007).

有高度的点状符号是一种体状符号,它是三维数字地形图的重要组成部分。每一种符号对应一个程序和命令,所有带高度的点状符号都需要以调用命令的方式来绘制。绘制该类符号时,需提供一个三维点坐标来确定地物的空间位置,实体高度值可以根据高度点来确定,也可以直接在命令行内手工输入。

Fig.3 Interrelationship between biosurfactant concentration and physical properties.Concentration of monomers in a biosurfactant solution represents the micelle formation and its role in surface and interfacial tension reduction.CMC=critical micelle concentration at which there is a sudden increase in metal solubility in the system(Mulligan,2005).

Degradability of biosurfactants

A good surfactant can lower the surface tension of water from 72 to 25 mN m1and the interfacial tension of water/hexadecane from 40 to 1 mN m1(Mulligan,2005;Muthusamy et al.,2008;Vijayakumar and Saravanan,2015).Biosurfactants have a structure with two different characteristics,i.e.,hydrophilic and hydrophobic,making them surface active and increasing the absorbance properties,causing an interface between polar and nonpolar media so that the head aggregate is soluble in the polar and the tail in the nonpolar medium.Surface tension is quite similar to interfacial tension in that cohesive forces are also included;however,the interfacial tension involves the adhesive forces between the liquid-liquid,liquidsolid,and liquid-gas phases of two different substances(Bustamante et al.,2012).Biosurfactants also may enhance the release of trace metals from soil through ion exchange and electrostatic and other attractions(Shin et al.,2005).Since rhamnolipids are negatively charged,they may form metal-surfactant complexes with cations(micronutrients)(Wang and Mulligan,2004).

Environmental friendly nature of biosurfactants

Many studies have reported ecofriendly nature of biosurfactants through assessment of their toxicity to various test organisms,and they are generally very low or non-toxic products and are appropriate for pharmaceutical,cosmetic,and food uses(Kuyukina et al.,2007;Hwang et al.,2009;Sahnoun et al.,2014).The properties of any biosurfactant control its suitability for application in any environment in that it should be low in toxicity,ecofriendly,eco-biodegradable,and stable in nature(Bezerra de Souza Sobrinho et al.,2013).Ivshina et al.(1998)reported that the toxicity of a biosurfactant produced by Rhodococcus ruber at the concentration that inhibits 50%of test species(bacterium Vibrio fischeri)(inhibitory concentration,IC50)is 10–100 times lower(and therefore 10–100 times more efficient)than several commercial synthetic surfactants(Ivshina et al.,1998).A study suggested that an anionic synthetic surfactant(Corexit)has a concentration that is lethal to 50%of test species(lethal concentration,LC50)against Photobacterium phosphoreum ten times lower than rhamnolipid,indicating the greater toxicity of synthetic surfactant.In comparison to cationic synthetic surfactants(e.g.,CTAB,tetradecyltrimethylammonium bromide(TTAB),and cetyltrimethylammonium chloride(CTAC))and anionic synthetic surfactants(e.g.,SDS),biosurfactants show much lower hemolytic activity to human erythrocytes(Shin et al.,2005;M¸edrzycka et al.,2009).Bezerra de Souza Sobrinho et al.(2013)indicated that the biosurfactant from Candida sphaerica UCP 0995 demonstrated no toxicity against the seeds of Brassica oleracea,Chicoria intybus,and Solanum gilo employed as bioindicators.Toxicity screening of the biosurfactant from Lactobacillus helveticus MRTL91 had much lower cytotoxicity and phytotoxicity in comparison to SDS(Sharma et al.,2014).Therefore,given their much lower level of toxicity,biosurfactants are more sustainable for use and are considerably safer to living organisms than synthetic surfactants(Rebello et al.,2014).However,biosurfactants are also known to increase the mobility and bioavailability of toxic metals such as Pb and Cd in soil(Juwarkar et al.,2007)and uptake of Cd in grass(Gunawardana et al.,2010).Sitespecific considerations for application of biosurfactants should therefore also include a preliminary assessment of site history,soil heavy metal content,and underlying geology in order to safeguard the environment and human health.

In India,land around the cities receives sewage wa-ters containing both domestic and industrial wastes.These wastes can be suitable for crops that are to be cooked,provided that the content of major plant nutrients is high,that the content of toxic elements is low,and importantly,that any sewage has been treated to reduce pathogen load-associated risks to human health(Subramani et al.,2014).Sewage effluents are typically rich in plant nutrients.However,the buildup of heavy metals,particularly Zn,Cu and Ni,in sewage-irrigated soils needs to be monitored periodically in view of their significant accumulation in bioavailable pool associated with decline in pH(Rattan et al.,2005).

BIOSURFACTANT APPLICATION FOR PLANT NUTRIENT AVAILABILITY IN MICRONUTRIENTDEFICIENT SOIL

Advanced food production technology is required to meet the food demand of the growing world population.Worldwide,millions of hectares of arable land are deficient in plant-available trace elements such as Cu,Fe,Mn,and Zn(Li et al.,2013).Among the most important risk factors for disease in low-income countries,the deficiencies of Zn and Fe are ranked the fifth and sixth,respectively,by WHO(2002).Trace element deficiencies affect both global food production and human nutrition and health.There are several factors such as soil pH,CEC,salinity,organic matter,calcium carbonate,and texture and climate(Schnug et al.,1998;Stacey et al.,2007;Naja fi-Ghiri et al.,2013)that can substantially reduce the efficacy of trace element fertilizers and thus decrease the solubility and availability of these metals/nutrients in soil and plant.Biosurfactants play an important role in providing micronutrients in nutrient-deficient soil;they chelate and form complexes with trace metals,followed by adsorption,desorption,and removal of the metals from the soil surface interfaces(Table V),resulting in increased micronutrient concentrations and bioavailability in soil(Abdul et al.,1990;Roy et al.,1997).

从近些年的案例来看,在互联网领域,各商家应该遵守广电总局颁布的法律法规。2017年6月份,国家对新浪、凤凰网等下达了明确的规定,在这些网络新闻平台中如不符合相关的管理条例,就要停顿进行整改。2018年1月份,国家约谈了花椒直播软件的负责人,责令其对平台中不法行为进行全面整改。同年4月份,国家广播电视总局约谈了受社会舆论关注的“快手”“今日头条”两家网站的主要负责人,并责令“今日头条”网站关闭“内涵段子”板块,并且永久不能开启。

[8]阿兰·罗伯-格里耶:《理论有什么用》,《快照集/为了一种新小说》,余中先译,长沙:湖南美术出版社,2001年,第74页。

TABLE V Application of biosurfactants to solubilize metals and enhance their availability

a)NS=not specified.

Biosurfactant Microbe producing the biosurfactant Metal(s) Plant(s) Reference Di-rhamnolipid Pseudomonas aeruginosa BS2 Cd,Pb – Juwarkar et al.(2007)Lipopeptide Bacillus sp.J119 Pb,Cd,Cu, Tomato,maize, Sheng et al.(2008)Ni,Zn sudangrass,canola Rhamnolipid Pseudomonas aeruginosa Cu – Venkatesh and Vedaraman(2012)NSa) Zn,Cd Sun flower Wen et al.(2016)NS Cu,Cd,Pb Perennial ryegrass Gunawardana et al.(2010)NS Cd,Zn Maize,sun flower Wen et al.(2010)Saponin NS Pb,Cd,Zn Italian ryegrass Zhu et al.(2015)

Biosurfactants can enhance the mobility of metals by reducing the interfacial tension between the metals and soil and by forming micelles(Pacwa-P′lociniczak et al.,2011).Interfacial tension is normally measured in mN m1,and it is the power/force that holds two different phases together.Under conditions of reduced interfacial tension,biosurfactants can bind to sorbed micronutrients directly and transfer them to the root zone interface(Singh and Cameotra,2004).

The use of bacterial strains capable of producing biosurfactants is a relatively new approach increasing the availability of micronutrients to plants(Pacwa-P′lociniczak et al.,2011).Biosurfactants and inorganic ligands are efficient for simultaneous solubilization of micronutrients and trace metals in soil(Olaniran et al.,2013).Hydrophilic and hydrophobic groups are the two basic domains of biosurfactants;therefore,biosurfactants have the ability to reduce surface and interfacial tension of two immiscible liquids as well as to enhance the solubility of inorganic and organic components in insoluble compounds(Bustamante et al.,2012).Glycolipids are the best studied microbial surfactants for metal complexes.The best-known glycolipids are rhamnolipid,trehalolipid,sophorolipid,and mannosylerythritol lipid(Edwards et al.,2003;Thavasi,2011).The addition of a biosurfactant,such as a rhamnolipid,in soil can effectively decrease the interfacial tension between solid surfaces and trace metal cations,therefore increasing the solubility and mobility.This may also be applicable for explaining desorption of weakly bound trace metals/micronutrients from solid surfaces of soil(Wang and Mulligan,2004).Biosurfactants are able to increase the availability of metals such as Zn,Mn,Cu,and Fe in soil to plants in various ways.According to Le Chatelier’s principle,biosurfactants can chelate and form a complex with ionic and nonionic metals and then release them from soil(Miller,1995).With anionic characteristics,biosurfactants can form complexes with positively charged metals.This offers the opportunity to use biosurfactants as metal-sequestering agents permitting metal desorption from soil and contaminated water.Interestingly,as suggested by Pacwa-P′lociniczak et al.(2011),the electrostatic interactions between the positively charged metal and the negatively charged surfactant is so strong that flushing water through soil removes the surfactant-metal complex from the soil.This is because the polar head group of micelles can bind metals,thereby mobilizing the metals in water(Fig.4)(Mnif and Ghribi,2015).

Fig.4 Impact of micronutrient deficiency on plant growth and soil quality on a micronutrient-deficient soil(a)and mechanisms of biosurfactant application enhancing micronutrient availability in micronutrient-deficient soil to the plant,soil quality,and related water quality through increasing nutrient solubility at a fixed concentration of biosurfactant molecule(modified from Mao et al.,2015)(b).CMC=critical micelle concentration at which there is a sudden increase in metal solubility in the system(Mulligan,2005).

Microbially produced surfactants confer a wide range of properties including the ability to lower surface and interfacial tension of liquids and the formation of micelles and microemulsions between two different phases(Banat et al.,2010).This also enhances the bio-availability of the products which helps to increase the availability of micronutrients and metals from soil to plant(Fig.4).Therefore,biosurfactant-enhanced solubility of trace elements has potential applications in agriculture(Bezza et al.,2015).Soil alkalinity is one of the major causes of micronutrient deficiency in soil.In this case,biosurfactants help to unbind the metals from the soil complex and form new bioavailable metalbiosurfactant complexes(Ru fino et al.,2011).

3)在进行植物造景时,主要应用的生态理念是营造一个理想景地。此时,最重要的设计就是植物的应用和选择,同时这也是生态环境建设的关键要素[6]。在此次的城市湿地公园景观设计项目中,主要应用的是比较适宜的乡土植物,形成“四季有景、三季有花”的公园景观。

The method of increasing the uptake of micronutrients by a plant through application of biosurfactants to the soil surrounding the plants root may be a useful tool in developing sustainable agriculture.Ionic biosurfactants in trace metal/micronutrient-deficient soil can create metal-biosurfactant complexes.These bonds are stronger than the metal bonds with soil,and metal-biosurfactant complexes are desorbed from the soil matrix to the soil solution due to the lowering of the interfacial tension by which trace metals become readily available to plant roots(Gregory,2006;Pacwa-P′lociniczak et al.,2011).One of the more common ways of delivering the appropriate metal micronutrient has been to form a chelated complex of the metal ion with surfactant/biosurfactant or any synthetic chelants as this maintains the metal ion in a soluble form for ease of application and reduces metal adsorption and fixation in soil(McLaughlin et al.,2012).The efficiency and availability of micronutrient in soil(to plants)might be increased,either by the bioaugmentation of biosurfactant-producing bacteria or through amendments of biosurfactants in micronutrient-deficient soil.Several studies have reported the bioaugmentation of potential bacteria in soil for improving plant growth and soil quality(Singh et al.,2011).For example,Sheng et al.(2008)investigated a biosurfactantproducing Bacillus sp.strain J119 for its ability to promote plant growth and trace metal uptake in canola,maize,sudangrass,and tomato.In addition,Stacey et al.(2007)investigated the formation and plant uptake of lipophilic metal-rhamnolipid complexes.In this case,monorhamnosyl and dirhamnosyl rhamnolipids formed lipophilic complexes with Cu,Mn,and Zn,facilitating the uptake of these metals by Brassica napus and Triticum durum roots.

CONCLUSIONS

Soil fertility is one of the most important factors controlling the yields of crops.The characterization of soil fertility status is important for sustainable and productive agriculture.Use of biosurfactant,a multifunctional microbial metabolite,is an approach that can increase nutrient availability thereby facilitating success in agriculture,provided that the mobility of toxic elements such as Cd,Pb,and Ni are also considered.To enhance micronutrient availability from deficient sites there are several advantages of using of biosurfactants over synthetic surfactants∶biosurfactants are biodegradable,cost effective,and of low toxicity and can be produced from renewable resources at low cost.Biosurfactants increase the availability of metals/micronutrients from soil columns through solubilization.Bonds formed between anionic biosurfactants and cationic metals are strong,and the resultant complexes are readily taken up by plant roots.In short,biosurfactants are capable of enhancing the nutrient/trace metal mobility in soil through reduction of surface and interfacial tension and micelle formation.Currently,the increased interest in the application of biosurfactants is due to their potential use in industry and in the field as a replacement for synthetic surfactants.Biosurfactants exhibit greater emulsification,foaming,and surface activity properties than synthetic surfactants.In addition,biosurfactants are stable over a wider range of environmental conditions compared to synthetic surfactants,including pH,temperature,moisture,and salinity.Thus,the potential role and application of biosurfactants in agriculture is promising although additional research is required in nutrient-deficient soil for sustainable agriculture.

ACKNOWLEDGEMENT

The first author Miss Ratan Singh is thankful to the Ministry of Human Resource and Development(MHRD),India,for granting a fellowship(No.RGNF-2012-13DGEN-UTT-56466).

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RatanSINGH,BernardR.GLICK,andDheerajRATHORE
《Pedosphere》 2018年第2期
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