Sorption of humic acid on Fe oxides, bacteria, and Fe oxide-bacteria composites

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1 J Soils Sediments (14) 14: DOI.7/s SOILS, SEC 2 GLOBAL CHANGE, ENVIRON RISK ASSESS, SUSTAINABLE LAND USE RESEARCH ARTICLE Sorption of humic acid on Fe oxides, bacteria, and Fe oxide-bacteria composites Li Jiang & Jun Zhu & Hui Wang & Qingling Fu & Hongqing Hu & Qiaoyun Huang & Antonio Violante & Li Huang Received: 9 August 13 /Accepted: 2 April 14 /Published online: April 14 # Springer-Verlag Berlin Heidelberg 14 Abstract Purpose Sorption of humic substances on other soil components plays an important role in controlling their function and fate in soil. Sorption of humic substances by individual soil components has been studied extensively. However, few studies reported the sorption characteristic of humic substances on composites of soil components. This study aimed to investigate the sorption characteristics of humic acid on Fe oxidebacteria composites and improve the understanding on the interaction among humic substance Fe oxide bacteria in soil. Materials and methods Humic acid was purchased from Sigma-Aldrich and was purified. Hematite and ferrihydrite were synthesized in the lab. Bacillus subtilis and Pseudomonas putida were cultivated in Luria-Broth medium and harvested at stationary growth phase. Batch sorption experiments were carried out at ph 5.. Various amounts of humic acid were mixed with mg of Fe oxide, bacteria, or Fe oxide-bacteria composite (oxide to bacteria of 1:1) in ml of KCl (.2 mol L 1 ) to construct sorption isotherms. The effects of phosphate concentration and addition order among humic acid, Fe oxide, bacteria on the sorption of humic acid were also studied. The sorption of humic acid was calculated Responsible editor: Saulo Rodrigues-Filho L. Jiang: J. Zhu (*) : H. Wang : Q. Fu : H. Hu (*) : Q. Huang : L. Huang Key Laboratory of Arable Land Conservation (Middle and Lower Reaches of Yangtse River), Ministry of Agriculture, College of Resources and Environment, Huazhong Agricultural University, Wuhan 47, China A. Violante Department of Soil, Plant, Environment and Animal Production Science, Faculty of Agriculture, University of Naples Federico II, Via University, 855 Portici, Naples, Italy by the difference between the amount of humic acid added initially and that remained in the supernatant. Results and discussion The maximum sorption of humic acid on hematite, ferrihydrite, B. subtilis and P. putida was 73.2, 153.5, 69.1, and 56.7 mg C g 1,respectively.Themaximum sorption of humic acid on examined Fe oxide-bacteria composite was % less than the predicted values, implying that the sorption of humic acid was reduced by the interaction between Fe oxides and bacteria. The presence of phosphate exerted negligible influence on the sorption of humic acid on bacteria while it inhibited the sorption of humic acid on Fe oxides. On Fe oxide-bacteria composites, inhibiting influences followed by promoting or weak inhibiting effects of phosphate with increasing concentration on the sorption of humic acid were found. Conclusions The interaction between Fe oxides and bacteria reduced the sorption of humic acid; moreover, the reduction was greater by the interaction of bacteria with ferrihydrite than that with hematite. Phosphate exerted negligible and inhibiting influence on the sorption of humic acid by bacteria and Fe oxides, respectively. On Fe oxide-bacteria composites, humic acid sorption was initially inhibited and then promoted or weakly inhibited by phosphate with increasing concentration. Keywords Bacteria. Composites. Fe oxide. Humic acid. Sorption 1 Introduction Humic substances closely relate with the control of soil pollution, the improvement of soil fertility, and the emission of greenhouse gas. The sorption of humic substances on other soil components could alter the physicochemical properties of relevant interfaces and may increase the resistance of humic

2 J Soils Sediments (14) 14: substances to degradation (Mikutta et al. 7; Wagai and Mayer 7; Janot et al. 12). Therefore, sorption on other soil components plays an important role in controlling the function and fate of humic substances. Many studies have been conducted on the sorption of humic substances by clay minerals and oxides (Vermeer et al. 1998; Au et al. 1999; Chorover and Amistadi 1; Tombacz et al. 4; Feng et al. 5; Weng et al. 6, 7; Zhang et al. 12). Electrostatic interactions, ligand exchange, hydrophobic interactions, H-bonding interactions, and cation bridging interactions have been suggested as the possible mechanisms of the sorption of humic substances on clay minerals and oxides (Feng et al. 5; Sutton and Sposito 6; Kögel-Knabner et al. 8). The groups of Al-OH at the edge of clay mineral particles and Fe-OH on Fe oxides are considered as the most reactive sites for humic acid in the surface complexation reaction (Tombacz et al. 4). Aliphatic fractions rather than aromatic fractions of humic acid have been found to be preferentially sorbed by clay minerals (Wang and Xing 5). The sorption of humic substances on metal oxides generally decreases with the increase of ph (Weng et al. 6, 7; Antelo et al. 7). Increase of ionic strength promotes the sorption of humic substances on metal oxides by forming cation bridges or changing the structure of humic substances (Weng et al. 6, 7; Antelo et al. 7). However, the presence of anionic ligands has been found generally to inhibit the sorption of humic substances by reducing the surface charge of oxides or competing with humic substances for available sorption sites (Hur and Schlautman 4; Antelo et al. 7). The sorption of humic substances on bacteria which are the important biotic soil components has also been investigated by several studies. Hydrophobic interaction is suggested as the dominant mechanism for the biosorption of humic substances (Fein et al. 1999; Moura et al. 7). In soil environments, metal oxides and bacteria are apt to be associated with each other due to the relatively high point of zero charge (PZC) of the oxide while relatively low PZC and abundance of negatively charged functional groups of bacteria (Glasauer et al. 1; Rong et al. ; Zhang et al. 11). Fein et al. (1999) showed that sorption characteristics of humic acid on Al oxide-bacteria composite were different, to some extent, from their individual components, probably due to the differences in sorption mechanisms and surface properties. However, to date, information on the sorption of humic substances on Fe oxide-bacteria composite is scant. Hematite and ferrihydrite are respectively the typical crystalline and amorphous Fe oxides. Bacillus subtilis and Pseudomonas putida are gram-positive and gramnegative bacteria, respectively. The aim of the present study was to investigate the sorption of humic acid on the examined Fe oxide-bacteria composites and their individual components; the influence of phosphate on the sorption of humic acid on examined sorbents was also studied. The understanding on the interactions among bacteria-oxide-humic substances-phosphate might thus be improved. 2Materialsandmethods 2.1 Chemicals and humic acid Deionized distilled (DD) water was used in this study to prepare all the solutions. The chemicals used were all analytical grade. Humic acid was purchased from Sigma-Aldrich Company and was purified according to Vermeer et al. (1998). The purified humic acid was dialyzed, air-dried, and stored in dark. The content of C, N, and H in humic acid analyzed by elemental analysis (EA, Italy) was 34.54,.82, and 6.5 %, respectively. A stock solution of humic acid was prepared by dissolving an appropriate amount of humic acid in a base solution. Potassium chloride (.2 mol L 1 ) was prepared as supporting electrolyte for all experiments. 2.2 Syntheses and characterization of Fe oxides Hematite was synthesized according to Schwertmann and Cornell (). Briefly, 5 ml of.2 mol L 1 Fe(NO 3 ) 3 was precipitated at 9 C by the addition of ml of 1molL 1 KOH and 5 ml of 1 mol L 1 NaHCO 3 under vigorous stirring. The resulting mixture was diluted to 1 L by DD water and then aged at 9 C in an airtight beaker for 48 h. Ferrihydrite was synthesized by precipitating.1 mol L 1 Fe(NO 3 ) 3 at ph 5.5 with.5 mol L 1 NaOH as described in our previous study (Zhu et al. ). The precipitates of ferrihydrite and hematite were finally dialyzed, air-dried, and ground to pass a -mesh sieve. Both the synthesized hematite and ferrihydrite were identified by X-ray diffraction (XRD). The surface area of the Fe oxides determined by high-speed automated surface area analyzer (Quantachrome Autosorb-1, USA) was 54.5 m 2 g 1 for hematite and m 2 g 1 for ferrihydrite. The PZC was 8.2 for hematite and 8.3 for ferrihydrite as measured by Mehlich method. 2.3 Preparation of bacteria B. subtilis and P. putida were cultivated in Luria-Broth medium(5.gl 1 yeast extract,. g L 1 tryptone, and 5. g L 1 NaCl) at C for 24 h to attain the stationary growth phase. The cells were harvested by centrifugation at

3 138 J Soils Sediments (14) 14: Fig. 1 Langmuir sorption isotherms of humic acid (HA) on Fe oxides and bacteria at ph 5. 5 Hematite Ferrihydrite 25 P.putida B.subtilis , rpm for min. After washing by DD water twice, bacterial biomass was resuspended in a suitable volume of.2 mol L 1 KCl. The ph of the cell suspension was adjusted to 5. by dilute HCl or KOH. To determine the concentration of the biomass in the suspension, an aliquot volume of cell suspension was centrifuged and then dried at 6 C to a constant weight. 2.4 Sorption experiments Various amounts of humic acid were mixed with mg of Fe oxide, or bacteria, or Fe oxide-bacteria composite (oxide to bacteria of 1:1) in ml of KCl (.2 mol L 1 ) at ph 5. to construct sorption isotherms. The influence of the addition order among humic acid ( mg C L 1 ), Fe oxide, and bacteria on the sorption of humic acid by mg of Fe oxide-bacteria composite (oxide to bacteria of 1:1) in ml of KCl (.2 mol L 1 ) at ph 5. were conducted as following cases: (1) humic acid was mixed firstly with oxide for 1 h and then mixed together with bacteria for 23 h (O- HA/B); (2) humic acid was mixed firstly with bacteria for 1 h and then mixed together with oxide for 23 h (B- HA/O); (3) humic acid, oxide, and bacteria were mixed simultaneously for 24 h (O-B-HA); and (4) oxide was mixed firstly with bacteria for 1 h and then mixed together with humic acid for 24 h (O-B/HA). The effects of phosphate on the sorption of humic acid at ph 5. were studied by adding a constant amount ( mg C L 1 ) of humic acid and increasing concentrations of phosphate from to 5 mmol L 1. Each suspension described above was shaken at 25 C for 24 h; the ph of each suspension was kept constant at 5. by.1 mol L 1 of KOH or HCl. The supernatant in the final suspension was collected by centrifugation at, rpm for min. The concentration of humic acid in the collected supernatant was determined by spectrophotometry at 45 nm. The sorption of humic acid was calculated by the difference between the amount of humic acid added initially and that remained in the supernatant. 3 Results and discussion 3.1 Sorption isotherms of humic acid on Fe oxide and bacteria The sorption isotherms of humic acid on individual hematite, ferrihydrite, B. subtilis and P. putida are shown in Fig. 1.The sorption data were satisfactorily fitted by Langmuir equation: X=X m KC/(1+KC), where C is the concentration of humic acid in the solution (mg C L 1 ), X is the amount of humic acid sorbed on the sorbent (mg C g 1 ), X m stands for the maximum amount of humic acid that may be sorbed (sorption capacity), and K is a constant related to the sorption energy. The greater the K value, the higher the affinity of humic acid for the sorbent (Sparks 2). The Langmuir parameters are listed in Table 1. It was observed that the maximum sorption of humic acid on hematite and ferrihydrite was 73.2 and mg C g 1 and that on B. subtilis and P. putida was 69.1 and 56.7 mg C g 1, respectively. The K values of humic acid on hematite and P. putida were higher than that on ferrihydrite and B. subtilis. These results indicated that higher amounts of humic acid could be sorbed by ferrihydrite than hematite and by B. subtilis than P. putida. Moreover, Fe oxides showed greater sorption capacity than bacteria for humic acid. Electrostatic interactions and ligand exchange are considered as the primary mechanisms of the sorption of humic acid on Fe oxides while hydrophobic interactions are regarded as the predominant mechanism of the sorption of humic acid on bacteria (Vermeer et al. 1998; Fein et al. 1999; Weng et al. 6, 7; Moura et al. 7). For Fe oxides, the positive charge on ferrihydrite (PZC 8.2) is similar to that on hematite (PZC 8.3) in the present study (ph 5.), but the surface area of ferrihydrite was much higher than that of hematite. For Table 1 Isothermal parameters for the sorption of humic acid on Fe oxides and bacteria at ph 5. Sorption capacity (X m )(mgcg 1 ) K value R 2 value Ferrihydrite Hematite B. subtilis P. putida

4 J Soils Sediments (14) 14: Fig. 2 Langmuir sorption isotherms of humic acid (HA) on Fe oxide-bacteria composites at ph 5. 5 Ferrihydrite - P.putida Ferrihydrite - B.subtilis 5 Hematite - P.putida Hematite - B.subtilis bacteria, the hydrophobicity of B. subtilis is greater than that of P. putida while the surface area of the former is less than that of the latter (Rong 8). Therefore, greater sorption capacity of ferrihydrite than hematite for humic acid is probably mainly ascribed to the higher surface area of the amorphous Fe oxide, while larger sorption capacity of humic acid on B. subtilis than that on P. putida could be mainly due to the stronger hydrophobicity of the former bacteria strain. 3.2 Sorption isotherms of humic acid on Fe oxide-bacteria composites The sorption isotherms of humic acid on the examined Fe oxide-bacteria composites can also be fitted well by the Langmuir equation (Fig. 2). The parameters obtained are listed in Table 2. The maximum sorptions of humic acid on ferrihydrite-b. subtilis, ferrihydrite-p. putida, hematite- B. subtilis, and hematite-p. putida composites were 51.3, 45., 51.1, and 43.9 mg C g 1 (observed value), respectively. All of the above values were lower than the maximum sorption of humic acid on individual Fe oxides or bacteria (Table 1). Based on the sum of sorptions of humic acid on the individual components, the sorption of humic acid on ferrihydrite-b. subtilis, ferrihydrite-p. putida, hematite- B. subtilis, and hematite-p. putida composites would be predicted as 111.3, 5.1, 71.2, and 65. mg C g 1,respectively. Compared with these predicted values, the observed sorption amounts of humic acid on ferrihydrite-b. subtilis,ferrihydrite- P. putida, hematite-b. subtilis, and hematite-p. putida composites decreased by 53.9, 57.2, 28.2, and 32.4 %, respectively. These results implied that the sorption of humic acid was reduced by the interaction between Fe oxides and bacteria. Moreover, the reduction of humic acid sorption was greater by the interaction of bacteria with ferrihydrite than that with hematite and slightly more by the interaction of Fe oxide with P. putida than that with B. subtilis. Electrostatic attraction is generally regarded as the main mechanism of the interaction between negatively charged bacteria and positively charged Fe oxide (Rong et al. ). The positive charge on the exposed surface of Fe oxide in the composites could be reduced or neutralized by the interaction with bacteria, just as anion sorption can reduce the positive charge of metal oxides (Erdemoğlu and Sarıkaya 6), thus weakening the attraction of exposed Fe oxides for humic acid. The particles of Fe oxide are generally attached on the surface of bacteria in their associations because of the smaller size of oxide particles compared with bacteria cells (Glasauer et al. 1; Rong et al. ). A part of the sorption sites for humic acid on bacteria fraction in the composites thus was probably masked by steric hindrance due to the macromolecular nature of humic acid. Therefore, the sorption sites for humic acid on Fe oxide and bacteria could be weakened, neutralized, or masked by the interaction between particles and cells. As discussed above, the PZC of ferrihydrite and hematite were similar, while ferrihydrite had higher surface area than hematite. Greater reduction of sorption sites by the interaction of bacteria with ferrihydrite than that with hematite thus could be due, at least in part, to the higher surface area of amorphous Fe oxide, which could facilitate the contact with and/or attachment on bacteria cells. 3.3 Effect of addition order among Fe oxide, bacteria, and humic acid on the sorption of humic acid The effects of addition order among Fe oxide, bacteria, and humic acid on the sorption of humic acid by Fe oxide-bacteria composites are depicted in Fig. 3. A sequence of B-HA/O O- HA/B O-B-HA>O-B/HA for the sorption of humic acid was Table 2 Isothermal parameters for the sorption of humic acid on Fe oxide-bacteria composites at ph 5. Composite Sorption capacity (X m )(mgcg 1 ) K value R 2 value Composite Sorption capacity (X m )(mgcg 1 ) K value R 2 value Ferrihydrite-B. subtilis Hematite-B. subtilis Ferrihydrite-P. putida Hematite-P. putida

5 1382 J Soils Sediments (14) 14: Fig. 3 Effect of the addition order among oxide, bacteria, and humic acid (HA) on the sorption of HA by Fe oxide-bacteria composites at ph 5. HA sorbed (%) 8 6 O+HA/B B+HA/O O+B+HA O+HA/B B+HA/O O+B+HA 6 Ferrihydrite-B.subtilis-HA system Ferrihydrite-P.putida-HA system HA sorbed (%) 5 O+HA/B B+HA/O O+B+HA O+HA/B B+HA/O O+B+HA Hematite-B.subtilis-HA system Hematite-P.putida-HA system found in the Fe oxide-bacteria-humic acid systems. Several studies reported that the attachment of Fe oxide on bacteria can reach equilibrium within 1 h (Rong et al. ; Zhang et al. 11). The least sorption of humic acid in O-B/HA system compared to that in other systems may confirm that the interaction of the oxide with bacteria was the factor that resulted in the reduction of the sorption of humic acid. 3.4 Effect of phosphate on the sorption of humic acid by Fe oxides, bacteria, and their composites Negligible influence of phosphate on the sorption of humic acid by bacteria was observed (data not shown). The effect of increasing concentrations of phosphate on the sorption of humic acid by Fe oxides and their composites with bacteria is illustrated in Fig. 4. To evaluate the difference of phosphate in affecting the sorption of humic acid on different sorbents, the inhibiting ( ) or promoting (+) efficiency was calculated as follows: Percentage efficiency (%)=[(the sorption of humic acid in the presence of phosphate/the sorption of humic acid in the absence of phosphate) 1]. It was observed that the sorption of humic acid on Fe oxides was inhibited by the presence of phosphate (Fig. 4). The inhibition was intensified with the increase of phosphate concentration from to 5 mmol L 1 and was stronger on ferrihydrite than on hematite (Table 3). The inhibiting influence of phosphate on the sorption of humic acid was in agreement with previous studies (Hur and Schlautman 4; Antelo et al. 7) and was ascribed to the reduction of surface charge on oxides or the competition for the homogenous sorption sites by anionic ligands. Greater inhibition on ferrihydrite than on hematite could be partly due to the lower sorption affinity of humic acid for the amorphous Fe oxide (Table 1). An initial decrease followed by an increasing trend of the sorption of humic acid was found on the examined Fe oxidebacteria composites with the increase of phosphate concentration from to 5 mmol L 1 (Fig. 4). The inhibiting efficiency on ferrihydrite-b. subtilis composite increased from to 16.8 % and then decreased slightly to 14.1 % in the examined range of phosphate concentration. An inhibiting efficiency of 8.3, 4.4, and 7.7 % at 5 mmol L 1 phosphate while a promoting efficiency of 14.2, 5., and 9.4 % at phosphate Fig. 4 Effect of the concentration of phosphate on the sorption of humic acid (HA)byFeoxides and their composites with bacteria at ph 5. Hematite Ferrihydrite Ferrihydrite-P.putida composite Ferrihydrite-B.subtilis composite Hematite-P.putida composite Hematite-B.subtilis composite 5 5 Concentration of phosphate (mmol L-1) Concentration of phosphate (mmol L-1)

6 J Soils Sediments (14) 14: Table 3 Promoting (+) or inhibiting ( ) efficiency (%) of phosphate concentration (PC, mmol L 1 ) on the sorption of humicacidbyfeoxideandtheir composite with bacteria PC Fe oxide Fe oxide-bacteria composites Ferrihydrite Hematite Ferrihydrite-B. subtilis Ferrihydrite-P. putida Hematite-B. subtilis Hematite-P. putida concentration of 5 mmol L 1 was observed on ferrihydrite- P. putida, hematite-b. subtilis, and hematite-p. putida composites, respectively (Table 3). These results suggested that the sorption of humic acid on Fe oxide-bacteria composites was generally inhibited by phosphate when phosphate concentration was relatively low, while a higher concentration of phosphate promoted or at most weakly inhibited the sorption of humic acid. It was noteworthy that the inhibiting efficiency on the sorption of humic acid by phosphate with relatively low concentration was greater on ferrihydrite-bacteria composites than on hematite-bacteria composites (Table 3), which was in agreement with the stronger inhibition of phosphate on the sorption of humic acid on pure ferrihydrite than that on pure hematite (Table 3). Meanwhile, negligible influence of phosphate on the sorption of humic acid by bacteria was found in the present study (data not shown). Both above phenomena probably imply that only the sorption of humic acid on the oxide fraction in the composites was inhibited by phosphate. Higher concentration of phosphate promoted or at most weakly inhibited the sorption of humic acid. An explanation for the promoting behavior of phosphate could be that a high concentration of phosphate reduced the association of Fe oxide and bacteria and thus diminished the weakening, neutralization and masking of sorption sites for humic acid. In fact, electrostatic interaction and ligand exchange are considered as the main mechanisms of the interaction of both phosphate and bacteria with Fe oxides (Vermeer et al. 1998; Weng et al. 6, 7; Rong et al. ; Elzinga et al. 12; Wu et al. 12), so phosphate and bacteria could compete with each other in the interaction with Fe oxides. The inhibition of anionic ligands including phosphate on the association between bacteria and Fe oxide was found by Wu et al. (11). 4 Conclusions The sorption capacity of humic acid was higher on ferrihydrite than hematite and was greater on B. subtilis than P. putida. The interaction between Fe oxides and bacteria reduced the sorption of humic acid, and the reduction was greater by the interaction of bacteria with ferrihydrite than that with hematite and slightly more by the interaction of Fe oxide with P. putida than that with B. subtilis. The presence of phosphate exerted negligible influence on the sorption of humic acid on bacteria while it inhibited the sorption of humic acid on Fe oxides. On Fe oxide-bacteria composites, the sorption of humic acid was inhibited by phosphate when the concentration of phosphate was relatively low while it was promoted or at most weakly inhibited by phosphate with higher concentration. The information obtained in this study could promote the understanding on the behavior and function of humic substance in soil environment. Acknowledgments We are grateful to Dr. Abdallah Naidja (University of Saskatchewan, Canada), Dr. Sudipta Rakshit (Tennessee State University, USA), and an anonymous reviewer for revising the manuscript and to National Natural Science Foundation of China (Grant number: and ) for the financial support on the research. References Antelo J, Arce F, Avena M, Fiol S, Lopez R, Macias F (7) Adsorption of a soil humic acid at the surface of goethite and its competitive interaction with phosphate. Geoderma 138:12 19 Au KK, Penisson AC, Yang S, O'Mella CR (1999) Natural organic matter at oxide/water interfaces: complexation and conformation. Geochim Cosmochim Ac 63: Chorover J, Amistadi MK (1) Reaction of forest floor organic matter at goethite, birnessite and smectite surfaces. Geochim Cosmochim Ac 65:95 9 Elzinga EJ, Huang JH, Chorover J, Kretzschmar R (12) ATR-FTIR spectroscopy study of the influence of ph and contact time on the adhesion of Shewanella putrefaciens bacterial cells to the surface of hematite. Environ Sci Technol 46: Erdemoğlu M, Sarıkaya M (6) Effects of heavy metals and oxalate on the zeta potential of magnetite. J Colloid Interf Sci : Fein JB, Boily JF, Gü lü K, Kaulbach E (1999) Experimental study of humic acid adsorption onto bacteria and Al-oxide mineral surfaces. Chem Geol 162:33 45 Feng X, Simpson AJ, Simpson MJ (5) Chemical and mineralogical controls on humic acid sorption to clay mineral surfaces. Org Geochem 36: Glasauer S, Langley S, Beveridge TJ (1) Sorption of Fe (hydr)oxides to the surface of Shewanella putrefaciens: Cell-bound fine-grained minerals are not always formed de novo. Appl Environ Microbiol 67:

7 1384 J Soils Sediments (14) 14: Hur J, Schlautman MA (4) Effects of ph and phosphate on the adsorptive fractionation of purified Aldrich humic acid on kaolinite and hematite. J Colloid Interf Sci 277: Janot N, Reiller PE, Zheng X, Croue JP, Benedetti MF (12) Characterization of humic acid reactivity modifications due to adsorption onto a-al 2 O 3. Water Res 46:731 7 Kögel-Knabner I, Guggenberger G, Kleber M, Kandeler E, Kalbitz K, Scheu S, Eusterhues K, Leinweber P (8) Organo-mineral associations in temperate soils: integrating biology, mineralogy, and organic matter chemistry. J Plant Nutr Soil Sci 171:61 82 Mikutta R, Mikutta C, Kalbitz K, Scheel T, Kaiser K, Jahn R (7) Biodegradation of forest floor organic matter bound to minerals via different binding mechanisms. Geochim Cosmochim Ac 71: Moura MN, Martín MJ, Burguillo FJ (7) A comparative study of the adsorption of humic acid, fulvic acid and phenol onto Bacillus subtilis and activated sludge. J Hazard Mater 149:42 48 Rong X (8) Thermodynamic investigations on the interactions of bacteria with soil clay minerals. Ph.D. thesis, Huazhong Agricultural University, Wuhan Rong X, Chen W, Huang Q, Cai P, Liang W () Pseudomonas putida adhesion to goethite: studied by equilibrium adsorption, SEM, FTIR and ITC. Colloids Surf B 8:79 85 Schwertmann U, Cornell RM () Iron oxides in the laboratory: preparation and characterization, WILEY-VCH Verlag GmbH Sparks DL (2) Environmental soil chemistry. Academic, New York Sutton R, Sposito G (6) Molecular simulation of humic substance-camontmorillonite complexes. Geochim Cosmochim Ac 7: Tombacz E, Libor Z, Illes E, Majzik A, Klumpp E (4) The role of reactive surface sites and complexation by humic acids in the interaction of clay mineral and iron oxide particles. Org Geochem 35: Vermeer AWP, Riemsdijk WHV, Koopal LK (1998) Adsorption of humic acid to mineral particles: 1. Specific and electrostatic interactions Langmuir 14: Wagai R, Mayer LM (7) Sorptive stabilization of organic matter in soils by hydrous iron oxides. Geochim Cosmochim Ac 71: Wang K, Xing B (5) Structural and sorption characteristics of adsorbed humic acid on clay minerals. J Environ Qual 34: Weng L, Riemsdijk WHV, Koopal LK, Hiemstra T (6) Adsorption of humic substances on goethite: comparison between humic acids and fulvic acids. Environ Sci Technol : Weng L, Riemsdijk WHV, Hiemstra T (7) Adsorption of humic acids onto goethite: effects of molar mass, ph and ionic strength. J Colloid Interf Sci 314:7 118 Wu H, Jiang D, Cai P, Rong X, Huang Q (11) Effects of lowmolecular-weight organic ligands and phosphate on adsorption of Pseudomonas putida by clay minerals and iron oxide. Colloids Surf B82: Wu H, Jiang D, Cai P, Rong X, Dai K, Liang W, Huang Q (12) Adsorption of Pseudomonas putida on soil particle size fractions: effects of solution chemistry and organic matter. J Soils Sediments 12: Zhang W, Rittmann B, Chen Y (11) Size effects on adsorption of hematite nanoparticles on E. coli cells. Environ Sci Technol 45: Zhang L, Luo L, Zhang S (12) Integrated investigations on the adsorption mechanisms of fulvic and humic acids on three clay minerals. Colloids Surf A 6:84 9 Zhu J, Pigna M, Cozzolino V, Caporale AG, Violante A () Competitive sorption of copper(ii), chromium(iii) and lead(ii) on ferrihydrite and two organomineral complexes. Geoderma 159:9 416

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