Advances in Microbial Remediation on the Application of Heavy Metal Pollution in Agricultural Water Resources

Zhiqiang YU

College of Bioscience and Bioengineering，Jiangxi Agricultural University，Nanchang 330045，China

Advances in Microbial Remediation on the Application of Heavy Metal Pollution in Agricultural Water Resources

Zhiqiang YU*

College of Bioscience and Bioengineering，Jiangxi Agricultural University，Nanchang 330045，China

Heavy metal pollution in agricultural water resources is very serious in recent years，resulting in large losses of the agricultural economy and endangering human life and health.Due to the advantages of low cost，high efficiency and less secondary pollution，microbial remediation technology is widely used in the treatment ofheavy metalpollution in agriculturalwaterresources.Atpresent，with the progress of modern biotechnology，microbial remediation of heavy metals in agricultural water resources has grown rapidly.The sources and status quo of heavy metal pollution in agricultural water resources at home and aboard，and the principles of microbial remediation of heavy metals pollution in agricultural water resources were reviewed in this paper，as well as the several common microbial remediation technology of heavy metals in agricultural water resources.Additionally，the further research work of heavy metal contaminated agricultural water resources by microbial remediation were prospected.

Heavy metal pollution；Microbial remediation；Agricultural water resources；Microbial absorption

W ith the rapid development of social and industrial，and the broad using of agro-chemicals，heavy metal pollution problem in agricultural water resources is very serious in recent years，and has drawn attention nationwide.Heavy metals are more persistent and tend to accumulate in living organisms，causing the symptoms of toxic or carcinogenic than organic pollutants such as polycyclic aromatic hydrocarbons（PAHs），pesticides and oil products in the environment［1-2］.Microbial remediation technology of heavy metal pollution in agriculturalwater resources is to change and transform the metal ions form via the microorganisms that have the resistance of toxic heavy metal ions，reducing heavy metal toxicity in order to ameliorate and purify the polluted environment［3-4］.

Microorganisms can change or reduce the toxicity of heavy metals and metabolites to repair the effect of heavy metal pollutants in the environment by degrading，transforming and absorbing.For the heavy metal pollution in agricultural water resources，compared with flora and fauna，microorganisms directly contact the contaminants［5-7］.Obviously，the technolo gy integrating microbial remediation and others is the future trend of study on treatment of heavy metal pollution in agricultural water resources.The sources and status of heavy metal pollution in agricultural water resources at home and aboard，and the principles of microbial remediation of heavy metals pollution in agricultural water resources were reviewed in this paper，as well as the several common microbial remediation technology of heavy metals in agricultural water resources. Additionally，the further research work of heavy metal contaminated agricultural water resources by microbial remediation was prospected.

Sources and Status of Heavy MetalPollution in Agricultural Water Resources at Home and Aboard

With the increasing of industrial and urban pollution，and the application of agricultural chemicals，heavy metals pollution in agricultural water resources is becoming increasingly serious，almost threatening every country. At present，the heavy metal pollution is deteriorating year by year，beginning in 2000，and the average annual emissions of whole world are about 15 000 tons of Hg，3.4 million tons of Cu，5 million tons of Pb，15 million tons of Mn，and 1 million tons of Ni［8］.Nearly 20 million hectares （ha）agricultural cultivated area of China are affected by heavy metal pollution of Cd，Hg，As，Cr，Pb and others，with about 12 million tons food of heavy metal contamination each year and the direct economic loss of over 20 billion yuan［9-10］. The regions of heavy metal contaminated agricultural water resources in China relatively focused on the Southwest China of Yunnan，Guizhou，Guangxi，the central China of Jiangxi，Hunan，as well as the Pearl River Delta and Yangtze River Delta［9］.

The main sources of heavy metal contaminated agricultural water resources are the metal mining smelting，chemical manufacturing industrial production，the using of heavy metal pesticide and fertilizer，and industrial wastewater for irrigation and other heavy metals，in which the emissions of wastewater containing heavy metal emissions settlement，irrigation，and dissolution of solid wastes of non-ferrous metal mining and smelting is one of the main ways of heavy metal pollution in agricultural water resources. Smelting mining leads to great accumulation of heavy metal pollution in the rivers and the downstream rivers，and the pollution appears the basin-wide or typical regional distribution along the metals mining and metallurgical activities in geographic area.It is difficult to be biodegraded that the heavy metals via various channels into agricultural water resources，small migration and accumulation in agricultural soils. When the heavy metal accumulation reaches a certain level in agricultural water resources and soil，it will seriously affect the quality of agricultural products，pass to animals and humans through the food chain，and endanger human health.

Principles of Microbial Remediation of Heavy Metal Pollution in Agricultural Water Resources

In the past years，the interaction between microorganisms and heavy metals has been intensively studied［11-12］.In general，some microorganisms may depend on the heavy metals and heavy metals generate toxicity to inhibit microbial growth and antibiotic activities.However，microorganisms can produce a lot resistance and detoxification mechanism of heavy metals by themselves.The microbial remediationmechanismsof heavy metals include，but are not limited to biosorption， bioaccumulation，bioreduction，biomineralization and so on［13］.According to the different methods ofmicrobialremediation heavy metal contaminated waters，we summarized the principles of microbial remediation heavy metals in the following aspects.

Microbialdependenceon heavy metals

Currently，the heavy metals are known to have important functions of microorganisms:Co，Ni，Cu，Zn，Mo，and W.W is found necessary for hyperthermophilic bacterium （such as Pyrococcus furiosus） in the hot springs，wolframate are considered instead of the molybdate in this environment［14］.Co can participate vitamin B12composition and symbiotic nitrogen fixation between microorganisms and plants.Ni is one of the components of the urease enzyme and hydrogenation，as well as may stimulate certain chemoautotrophic-microbial growth. Mo can not only play a role in microbial lone，but also it’s nitrate reductase cofactor of denitrifying bacteria［15］.

As well known，microbial dependence on heavy metals refers to the needs of heavy metals on microbial vital activities，physiologicaland biochemicalprocesses.Some heavy metals are usually necessary for microbial enzyme catalysis，molecular transportation， protein structure，charge neutralization，and so on.Severalbasic features contributed by these heavy metals include:（1）they are many prosthetic groups of proteins，and play an important role in the maintenance of enzyme activities in the central configuration；（2）they are cofactors in many enzyme reactions；（3）they are ligand centers （for the porphyrin molecules）；and（4）they are redox centers，transiting participates in important redox reactions within the cell.

Resistance and mechanism of detoxification of heavy metals by microorganisms

Microbial resistance to heavy metals is divided into the universality resistance of not relying on heavy metal stress and the specific resistance of depending on heavy metal stress.The former is an universality resistance that suitable for all heavy metals，and its most basic principles is based on the fixation of heavy metals，reducing the migration of heavy metals，preventing metal into the cell，reduce the bioavailabilities of heavy metals and thus reduce the toxicity of heavy metals，which convert the biological resistance.The latter features of this specific resistance are subject to heavy metal ions by activated and specificity. This resistance is consist mainly of the followings:（1）complexation of heavy metals by metallothionein or similar protein，and Allowing separate from the heavy metal； （2）exclusion of heavy metals from the cells via energy-dependent heavy metal output system that plasmids encode［16］；and（3）heavy metal ion oxidation，reduction，methylation or demethylation into price stability，low toxicity or nontoxic compounds，thus reducing poison effects on organisms［17］.

SeveralCommon Technologies of Microbial Remediation of Heavy Metals in Agricultural Water Resources

Microbial adsorption and metabolic remediation

Conversion of heavy metal ions by microbial metabolic activities canreduce heavy metal toxicity.Some studies have shown［18-19］that acidophilic bacteria can pass itself into dissolved the high metabolic activity of Cr6+and Cr3+of less toxic，Cr ion which can reduce harm to the environment，certain microorganisms can be soluble insoluble Pu4+into Pu3+，reduced elemental Hg to Hg2+.Yeast on the surface of the bacteria can successfully to reduce the Cr6+to lower valence state of Cr ion enrichment and effective［20］. Some studies have found［21-22］that by optimizing culture medium can cause organismsto concentrationsbelow 150 mg/L following the full of Cr6+detoxification，and medium composition of microbial adaptation；Cr6+-reducing bacteria in a strong alkaline environment of initial concentration of 1 500 mg/L can be achieved 99.9% removal of Cr-containing wastewater.

Because of the microbial cells and extracellular materials have many potential metal binding sites，so far has begun to adsorb the heavy metals by suspending or immobilized cells［23］.Microorganisms can dissolve and mineralize heavy metal ions by their directly or indirectly life metabolic activities. Organic acids，amino acids and other substances produced by metabolism can dissolve the heavy metals and heavy metal containing minerals，and also accelerate heavy metals to release from the weathering crust［24］. These effects can change the presence of heavy metals in agricultural water resources，and reduce the degree of pollution.Microorganisms can also influence the behavior of heavy metals by producing siderophores，metallothionein，plant-chelating peptide，changing the pH of waters and other activities［25-26］.

Heavy metal biosorption by microorganisms is very important because it contributes to the removal of toxic heavy metal ions and collection of metal resources from contaminated waters.Microbial adsorption remediation has a better effects of heavy metals at low concentrations，easy to operate and so on，so that has a broad application prospects in the removal of heavy metal pollution in agricultural water resources.Most microbial surface charges are negative，which is conducive to the adsorption of heavy metals，but the absorption depends mainly on the different combining sites for heavy metal selectivity.Microbial adsorption of heavy metals on capability depends on the properties of the microorganism itself（such as adsorption type，the number of active sites，strain age，etc），the types and valence of heavy metals，simultaneously it is affected by externalenvironmental factors（such as pH，temperature，coexistence of pollutants，etc.）［27］.

Microbial-phytoremediation

Microbial-phytoremediation as a kind of enhanced heavy metal phytoremediation technology has gradually become a research hotspot at home and abroad［28］.Microbial-phytoremediation of heavy metal contaminated agricultural water resources has two main forms，one is secreted by microorganisms producing Fe-containing cells，biological surface activator and organic acids，such as increased mobility of metals in waters，promoting plants absorbing the heavy metals；another is that though the plant growth promoting rhizosphere bacteria and mycorrhizal fungi associated to increase plantbiomass，thereby increasing the accumulation of heavy metals.Some studies［29-30］have shown that arbuscular mycorrhizas fungus（AMF）can significantly improve the heavy metal tolerance of the host plants in the pollution environment.

Microbial-phytoremediation mainly through the heavy metal hyperaccumulator roots by microbial activity absorption，transformation，and transport of heavy metal ions and enrichment to the plant’s neck and leaves［31］.Marques，et al.［32］showed that the presence of both Glomus claroideum and Glomus intraradices， enhanced Solanum nigrum absorption and accumulation of Zn（Zn accumulation up to 83 and 49，respectively）.Andrade，et al.［33］studied that Glomus etunicatum can maintain an efficient symbiotic moderate Zn concentrations in contaminated environment with Canavalia ensiformis，increase the composite behaviour of Canavalia ensiformis under these conditions may be due to physiological and nutritional changes caused the intimate relationship between fungi and plants.Leung，et al.［34］found that AMF’s main role is to help As absorption and accumulation of the centipede grass （as hyperaccumulator），and showed that the centipede grass roots of indigenous mycorrhizal fungi enhanced As accumulation.By above-mentioned examples，we know that microbial-phytoremediation technology can effectively repair heavy metal pollutants in the environment，not only can play a role to beautify the environment，also can receive some economic benefits.

Biofilm system

Biofilm systems can be from one or more single or multiple species of microbial communities such as bacteria，fungi，algae and archaea in different electron acceptors and donors，and nutrient concentration of environment［35-36］.Biofilm systems can though microbial adsorption，biological reduction，biological sequestration，bio-accumulative effects of heavy metal pollutants，in order to reach the high effects of heavy metals pollution in agricultural water resources［37］.

Costley，et al.［38］successfully applied the membrane systems remove the heavy metal pollution in wastewater，which showed Cu＞Zn＞Cd，removal，respectively，and73% and 33%.Golby，et al.［39］showed that use of bio-mineralization of the biofilm system，they also studied the Cu，Ag，Pb，Ni，Zn plasma concentration was measured after viability.They found that the mixture of species biofilm-resistant metal，of which up to 20 mg/L Pb，16 mg/L Zn，1 000 mg/L Sr，and 3.2 mg/L Ni.It can visual observation ofheavymetalsmineralization by scanning and metal crystals of Cu，Ag，Pb and Sr exudation membranes.After contacting with heavy metals，mixture species biofilm was found to maintain a high level of complexity by molecular biological methods.

MFCs

MFCs technology has recently become a promising technologies of remediation of heavy metal pollutants，which repairs the heavy metals at the same time comes with a power generation.MFCs convert the chemical energy of organic matter contained in the design ofmicrobialcatalysis（metabolism）active power bioelectrochemical system［40］.As the bioelectrochemical system，the MFCs and themicrobialelectrolysis cells （MECs）were developed to selectively recover Cu2+and Ni2+ions from wastewater［41］. A typical dual-chamber MFCs consists of an anode and a cathode，separated by a cation specific membrane，whose wastewater treatment is carried out in MFCs cathode，heavy metal ions can be effectively removed by the system［42］.

Atpresent，MFCshavebeen widely used in heavy metal wastewater treatment.Huang，et al.［43］showed that MFCs can help reducing lithium cobalt oxide and with synergistic interaction energy of Co3+concentration in MFCs，by conventional chemical processes and acid-free control，resulting in Co3+leaching speed 3.4 times the rate of the sum.Wu，et al.［44］used a new MFC method to greatly increase the efficiency of Cr6+restoration，mainly attributing the biological cathode to have a high biomass concentration and the low resistance of Cr3+precipitation cathode than common acclimation method （no-treatment control）. These examples showed that in the MFCs，microorganisms can convert chemical energy into electricity when organic matter degraded by anaerobic features［45］.

Conclusion and Outlook

Heavy metal pollution in agricultural water resources intensifies daily，so we need the efficient remediation methods and an urgent need for effective measures for monitoring and controlling heavy metal pollution.Microorganismscan absorb，degrade and transform the heavy metals by physical and chemical effects itself and its metabolites，and thus changing or reducing the toxicity of heavy metals residues in agriculturalwaterresources.Due to microbial remediation having cheapness and efficiency，it has good prospects in remediation of heavy metal contaminated agricultural water resources.Despite the rapid development of microbial remediation，but further research is needed:

（1）With the development and application of genetic engineering and molecular biology techniques，we will filter down to high efficiency，high strain to repair a variety of toxic heavy metals，and for heavy metals the wide application of bioremediation technology to provide more favourable conditions；

（2）We need further study on efficient microbialdegradation repair genes，enzymes and some manipulation factors，genetic diversity and functional microbial remediation. Through continuous research and study a variety ofefficientrepair mechanisms of the bacterium，and competence of the repair pathways，it will make towards the desired direction of mankind；

（3）We should further study the states and forms of heavy metal pollutants in agricultural water resources to enable which after bioremediation can be recycled as much as possible.Trying to find a effective bioremediation and recycle more waste method of heavy metal pollution in the environment is more important in the future；

（4）In order to meet the increasingly stringent environmental regulations，a variety of water treatment technologies have developed and tried to remove heavy metals and its inherent strengths and limitations，such as chemicalprecipitation，coagulation，flocculation，flotation，ion exchange and membrane filtration，and so on［46］. Due to the widely range sources and vary greatly of heavy metals with different industries and processes，if we only use a single microbial remediation method has its limitations，and difficult to achieve the desired effect.Therefore，with the development of biotechnology，bioremediation technologies and other technologies will be the future restoration of heavy metal pollutants in water resources research.

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微生物修复农业水资源重金属污染的应用研究进展

虞志强*（江西农业大学生物科学与工程学院，江西南昌 330045）

近年来，农业水资源中重金属污染十分严重，造成大量农业经济损失以及危及人类生命健康。微生物修复技术具有成本低廉、效率高和产生二次污染少等优点，广泛应用于农业水资源重金属污染治理。目前，随着现代生物技术的进步，农业水资源中重金属污染的微生物修复技术也得到十分迅速的发展。本文重点从农业水资源重金属污染来源和国内外现状、微生物修复农业水资源重金属污染的原理以及几种常见的农业水资源重金属微生物修复技术等方面进行综述。此外，还对微生物修复农业水资源重金属污染的进一步研究工作进行了展望。

重金属污染；微生物修复；农业水资源；微生物吸附

虞志强（1990-），男，江西万年人，硕士研究生，研究方向：环境污染物的微生物治理与修复，E-mail：vip_yuzhiqiang@163.com。

2015-10-03

*Corresponding author.E-mail:vip_yuzhiqiang@163.com

Received:October 3，2015 Accepted:November 15，2015

*通讯作者。

修回日期 2015-11-15