effect of the clay mineral zeolite on ammonia inhibition of anaerobic thermophilic reactors treating...

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Effect of the clay mineralzeolite on ammoniainhibition of anaerobicthermophilic reactorstreating cattle manureR. Borja a , E. Sánchez b & M.M. Durán aa Instituto de la Grasa (C.S.I.C.), Avda. PadreGarcía Tejero 4, E‐41012, Sevilla, Spainb Departamento de Estudios sobreContaminación Ambiental (DECA), CNIC, P.O.Box 6990, La Habana, Cuba

Version of record first published: 15 Dec2008.

To cite this article: R. Borja, E. Sánchez & M.M. Durán (1996): Effect of theclay mineral zeolite on ammonia inhibition of anaerobic thermophilic reactorstreating cattle manure, Journal of Environmental Science and Health . PartA: Environmental Science and Engineering and Toxicology: Toxic/HazardousSubstances and Environmental Engineering, 31:2, 479-500

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J. ENVIRON. SCI. HEALTH, A31(2), 479-500 (1996)

EFFECT OF THE CLAY MINERAL ZEOLITE ON AMMONIA INHIBITIONOF ANAEROBIC THERMOPHILIC REACTORS TREATING CATTLEMANURE

Key Words: Anaerobic digestion, Cattle manure, Zeolite, Ammoniainhibition, Thermophilic reactors.

R. Borja (1), E. Sánchez (2) & M.M. Durán (1)

(1) Instituto de la Grasa (C.S.I.C.). Avda. Padre García Tejero 4, E-41012Sevilla, Spain.

(2) Departamento de Estudios sobre Contaminación Ambiental (DECA-CNIC),P.O. Box 6990, La Habana, Cuba.

ABSTRACT

Addition of zeolite counteracted to some extent the inhibitory effect of ammonia

during thermophilic anaerobic digestion of cattle manure. In continuously-fed reactor

experiments, addition of zeolite delayed the onset of the inhibition and aided process

recovery after initial inhibition. The effect was observed mainly when the ammonia

concentration was increased gradually, indicating that the major effect of zeolite was

not through a direct antagonistic effect towards ammonia but through an increased

process resistance to toxic compounds. In batch experiments zeolite had a similar

stimulatory effect leading to a decreased lag phase and increased methane production

rate in ammonia inhibited reactors.

479

Copyright © 1996 by Marcel Dekker, Inc.

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480 BORJA, SANCHEZ, AND DURAN

INTRODUCTION

Anaerobic digestion is often subjected to failure due to disturbance of the balance

between the different bacteria involved, caused by for instance toxic compounds

contained in waste or a change in the loading of the reactor [ 1 ]. Elimination or control

of toxic compounds is, therefore, of major importance. Ammonia (NH3 + NH4+) is

the most common toxin causing digester failure during anaerobic digestion of cattle

wastes [2]. The inhibitory level of ammonia has been the subject of numerous studies:

the toxicity of ammonia depends on pH, temperature and inoculum.

The toxicity of ammonia is strongly influenced by pH which determines

the equilibrium concentration of free ammonia to the ammonium ion in solution.

Values as low as 150 mg/1 NH r N have been reported as being toxic to anaerobic

digestion at pH 8 [3]. Under these conditions the proportion of free ammonia, which

is most toxic might be expected to be higher. Most digesters, however, work at

around neutrality or under slightly acidic conditions where the equilibrium is biased

towards the ammonium ion which has a far lower toxicity. Reports in the literature

rarely distinguish between free ammonia and the ammonium ion in analytical methods

and in the reporting of results. It is therefore not uncommon to find a wide range of

values reported at which the digestion process is deemed to have been inhibited by

ammonia/ammonium ion. It is, however, well accepted that toxicity effects may be

detrimental to the anaerobic process performance in both homogeneous and fixed film

systems. More specifically the anaerobic digestion of cattle manure [4-6] has been

found to be very difficult at ammoniacal nitrogen concentrations of 3 g/1; in both

these cases the authors attributed these difficulties to ammonia toxicity rather than

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CLAY MINERAL ZEOLITE AND AMMONIA INHIBITION 481

high volatile solids loadings. The effect is likely to be more pronounced on the

methanogenic population in the digester as these are reported to have the greatest

sensitivity [7], Methanobacterium formicwn, for example, was shown to be at least

partially inhibited at an ammoniacal nitrogen concentration of 3.3 g/1. Not only do the

variations in pH make it difficult to produce meaningful figures relating to toxicity but

also there is a growing weight of evidence which suggests that the anaerobic

consortium of bacteria can acclimatize to high ammonia concentrations [8,9]. A

combination of both of these may explain the wide range of toxicity values reported

and even account for high values such as those encountered by Speece [10] and

Parking [11] in completely mixed and biofilm reactors where ammoniacal nitrogen

concentrations between 4000 and 14000 mg/1 have been observed.

Only a few investigations have dealt with ammonia inhibition at thermophilic

temperatures. Zeeman et al. [12] reported an initial inhibition at 1.7 g N/l at 50 °C.

Hashimoto [5] found ammonia inhibition at about 2.5 g N/l for both mesophilic and

thermophilic reactors when these were not previously acclimatized to ammonia.

However, the corresponding value was 4 g N/l for thermophilic reactors previously

acclimatized to ammonia concentrations between 1.4 and 3.3 g N/l. In their

experiments the effluent pH was 7.2.

As the free ammonia fraction increases with temperature and pH, the ammonia

level tolerated at high pH and thermophilic temperatures would be expected to be low.

Biogas reactors operating with cattle waste often have a high pH (about 8) and,

especially at thermophilic temperatures, the free ammonia concentration will be up to

ten times higher than the free ammonia concentrations reported as inhibitory [13].

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Only a few studies have dealt with ways of decreasing ammonia inhibition.

McCarty and McKinney [14] found that addition of Mg2* and Ca2+ had an

antagonistic effect on ammonia inhibition. Sprott and Patel [15] have likewise reported

that certain cations (Ca2+ or Na+) countered the toxic effects of ammonia on methane

synthesis in pure cultures.

Clay minerals and other surface-active particles have been reported to influence

microbial and enzymatic transformations of a variety of substances, including

ammonium, sulfur, carbohydrates, proteinaceous materials and phenolic compounds

[16-23]. Stotzky & Rem [24] reported that the clay mineral montmorillonite

stimulated respiration of a wide spectrum of bacterial species at all stages of their

growth but especially by shortening the lag phase. Addition of vermiculite powder,

and other biologically inert materials to cattle manure resulted in an increased biogas

yield of 15 to 30% in batch experiments [25]. Furthermore, Angelidaki et al. [26]

showed that addition of bentonite reduces inhibition caused by long-chain fatty acids.

Control of the ammoniacal nitrogen concentration could be achieved by the use

of ionic exchangers and adsorbers. Among the materials commonly used for this

purpose is zeolite [27-30] which has shown removal rates of 0.05 g NH4+/g. Used in

isolation in a column on aqueous solutions removals near to 95 % have been observed

when operated in the downflow mode. The material has also been used as a selective

exchanger of phosphorous and nitrogen compounds from municipal wastewaters

[31,32]. In addition, zeolite has been found to be a successful support for the

immobilization of microorganisms in mesophilic anaerobic digestion of different

wastewaters [33].

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Considering these roles, in the present study, the effect of the clay mineral

zeolite on thermophilic anaerobic digestion of cattle waste at different ammonia

concentrations were examined. Experiments were carried out both in batch and in

continuously-fed reactors.

MATERIALS AND METHODS

Reactor experiments

Prior to initiation of the experiments all reactors were operated at similar conditions

for two months. The experiments were carried out in eight 4-litre laboratory-scale

reactors with a working volume of 3 litres. They had an integral settling zone intended

to avoid loss of the anaerobic microorganisms responsible for the process. The

biomass was suspended and agitated with a magnetic stirrer working at 160 rpm. The

reactors were fed continuously with a peristaltic pump; the effluent left the reactor

through a hydraulic seal with a 35 cm high liquid column to prevent the entrance of

air into the reactor and the escape of biogas. Biogas produced from the reactor was

collected by positive displacement of acidified water (pH 2-3) into 5-litre gasometers.

The reactors were fed to give a hydraulic retention time (HRT) of 12 days. They were

placed in a temperature controlled room at 55 °C.

Experimental design

The eight reactors were divided into two groups. In the first group, referred to as the

reference group, no extra ammonia was added. Two of the reactors were fed with

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cattle manure alone (control reactors) and the other two were fed with cattle manure

with the addition of 2% zeolite (zeolite reactors).

The other group was fed identically to the reference group, apart from the

ammonia concentration which was gradually increased by addition of extra ammonia

in the form of NH4C1. When the experiment was initiated, the ammonia concentration

was changed from 2.5 to 3 g N/l. Further changes were made at day 41 (from 3 to

4 g N/l) and at day 70 (from 4 to 5 g N/l).

The methane yield of the reactors was estimated as the methane produced

divided by the volatile solids added (1 CH4/g VS).

As the variation between duplicate reactors was always small (less than 5%)

mean values are reported.

Wastewater

The characteristics of the cattle manure used are shown in Table 1.

Zeolite used

The zeolite used had a cation exchange capacity (CEC) of 1.5 meq/g. Zeolite consists

mainly of clinoptilolite (41%). Its characteristics in cation-exchange capacity and

cation selectivity have led to its frequent use in wastewater treatments, mostly for

waters with high levels of ammonium. Zeolites are unique adsorbent materials due to

their large central cavities and entry channels. Most of the surface area is found within

the zeolite structure and represents the inner surface of dehydrated channels and

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TABLE 1

Characteristics of the cattle manure used*

Parameter Concentration

Total solids (%) 5.8Volatile solids (%) 4.1Total nitrogen (g N/l) 3.6Ammonia nitrogen (g N/l) 2.5pH 7.9VFA (g/1, as acetic acid) 5.1Total COD (g/1) 47.2Alkalinity (g/1, as CaCO3) 7.8

* Values are the averages of four determinations; the differences between the observedvalues were less than 1 % in all cases.

cavities. Molecules having diameters small enough to pass through the channels are

readily adsorbed in the dehydrated channels and central cavities. The unique

geometries contained in zeolitic channels and cavities create selective sorption

properties [34].

The composition of the zeolite used was (w/w %, sample dried at 105 °C):

SiO2l 67.9; A12O3, 11.9; F e A , 2.1; CaO, 2.8; MgO, 1.2; Na2O, 1.5; K2O, 1.1.

Batch culture experiments

The effect of zeolite on ammonia inhibition was also examined in batch culture

experiments. BA-medium was used [35] with 90 mM acetate as carbon and energy

source. The ammonia content in BA-medium was 0.25 g N/l. The medium contains

0.3 g/I yeast extract and was distributed anaerobically in 20 ml portions to 60 ml

vials. Zeolite was added (0.4 g per vial) resulting in a content of 2 w/v %. The vials

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were inoculated with 10% digested manure from a laboratory-scale thermophilic

reactor treating cattle manure with an ammonia content of 2.5 g N/l. Triplicate vials

were used. As the variation between triplicate vials was in general small (less than

4%) mean values are reported. Ammonia was added as NH4C1 from anaerobic stock

solutions. In the control vials with no extra ammonia, distilled water was added.

Analytical methods

The analysis (total and volatile solids, pH and COD) followed the recommendations

of the Standard Methods [36]. Ammoniacal nitrogen determination was carried out by

distillation of the samples previously buffered at pH 9.5 with a borate buffer solution

and titration with NaOH of the distillates collected in excess sulfuric acid. Alkalinity

measurement was done by a titration method, the end point being pH 4.5. Total

nitrogen was determined by the Kjeldahl method. Methane was determined by gas

chromatography with a stainless-steel column (200 cm x 0.3 cm) packed with active

carbon (30-60 mesh) using thermal-conductivity detection. Volatile fatty acids (VFA)

were determined by gas chromatography using a 2 m x 4 mm glass column packed

with Supelcopor (100-120 mesh) coated with 10% Fluorad FC 431. The temperature

of the column, the injection port and the flame-ionization detector were 130, 220 and

240 °C respectively. Nitrogen saturated with formic acid was used as the carrier gas

at a flow rate of 50 ml/min.

RESULTS

The methane yield of the two control reactors receiving only manure from the

reference group was 0.25 1 CH4/g VS (Standard Deviation, STD = 0.01) (Figure 1).

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CLAY MINERAL ZEOLITE AND AMMONIA INHIBITION

0.35Methane yield (l/g VS)

40 60 80 100 120 140Time (days)

487

-B-CONTROL - A - ZEOLITE

180 200

Figure 1. Methane yield (1 methane produced/g VS in a 5 days average) for the

continuously-fed reactor experiment with no extra ammonia addition.

Differences between the two reactors were always lower than 5%. In the reactors

receiving 2% zeolite in addition to manure, the methane yield was higher i.e.

approximately 0.31 1 CH4/g VS (STD = 0.01). Concentrations of the VFA were

comparable and varied around 1 g/1 as acetic acid in all the reactors (Figure 2),

although the values for zeolite reactors were always lower than those control reactors.

When the ammonia concentration was increased to 4 g N/l, at day 41 in the

feed to the second group of reactors, the methane yield decreased in the control

reactors (Figure 3). The process seemed to adapt to this concentration of ammonia and

the methane production gradually increased after 29 days in the control reactors. The

zeolite reactors did not show any decrease in the methane production at this ammonia

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VFA (g/l)

-B-CONTROL -A- ZEOLITE

40 50 60 70 80 90 100 110 120 130 140 150 160 170 180

Time (days)

Figure 2. VFA concentration (calculated as acetic acid) for the continuously-fed

reactor experiment with no extra ammonia addition.

concentration. When 5 g N/l was introduced at day 70, methane production dropped

in all the reactors, especially in the control reactors (Figure 3). The methane yield of

the control reactors decreased to less than 0.151 ( W g VS, and in the zeolite reactors

to 0.20 1 CH4/g VS. Following this initial drop, methane production in the zeolite

reactors gradually increased, reaching the same level as before inhibition. The control

reactors did, however, not recover to the same extent and the methane yield was 0.19

1 CH4/g VS at the end of the experiment. In the zeolite reactors the methane yields

at the end of the experiment was 0.28 1 CH4/g VS.

VFA concentration (Figure 4) was stable at approximately 1 g/l as acetic acid

until the ammonia concentration in the feed was increased to 4 g N/l. This resulted

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0.3

I

0.25

0.2

0.15

0.1 -

0.05 -

0 -40

Methane yield (l/g VS)

\ \ y

- S - CONTROL -A" ZEOLITE

f T (

60 80 100 120 140Time (days)

160 180 200

Figure 3 . Methane yield (1 methane produced/g VS in a 5 days average) for the

continuously-fed reactor experiment with increasing ammonia

concentration. At day 41 ammonia concentration was changed from 3

to 4 g N/l, and at day 70, from 4 to 5 g N/l.

in an increase in the VFA concentration of the control reactors. VFA concentration

in the reactors with zeolite addition increased only after the ammonia concentration

was elevated to 5 g N/l. After 160 days the VFA concentration of the zeolite reactors

stabilized and returned to the same level as before extra ammonia was introduced.

Batch culture experiments

Methane production from the control vials with no extra ammonia was alike in all

vials, independent of addition of zeolite (Figure 5). When extra ammonia was added

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VFA (g/l)

5 -

4 -

3 -

2 -

1-0 S£

" ^ - B - CONTROL -^-ZEOLITE

1 f 1 1 I 1 1 1 1

40 50 60 70 80 90 100 110 120 130 140 150 160 170 180

Time (days)

Figure 4. VFA concentration (calculated as acetic acid) for the continuously-fed

reactor experiment with increasing ammonia concentration. At day 41

ammonia concentration was changed from 3 to 4 g N/l, and at day 70,

from 4 to 5 g N/l.

to the medium the methane production rate decreased and the lag phase increased

(Figures 6, 7 and 8). In the vials with zeolite the increase in lag phase was slightly

lower than in vials without zeolite. This effect was more pronounced as the ammonia

concentration increased, i.e. the lag phase was shortened by 4, 8 and more than 26

days by addition of zeolite for ammonia concentrations of 2, 5 and 7 g N/l,

respectively, compared to controls with 0.25 g N/l. In addition to the shortening of

the lag phase, zeolite had a positive effect on the methane production rate (Figures 6,

7 and 8). Zeolite did not influence the methane yield from acetate. The ultimate

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No extra ammonia addition

Methane production (ml)

491

40

20 -

090 10 15 20 25 30 35

Time (days)

• without zeolite —©- with zeolite

Figure 5. Batch experiment with no extra ammonia addition. Bars are the

standard deviations of the means.

methane yield from acetate was the same in all vials except for the vials with 7 g N/l

ammonia and no zeolite, where no methane was found when the experiment was

terminated.

DISCUSSION

The methane yield from digestion of cattle manure with an ammonia concentration of

2.5 g N/l was approximately 0.25 1 CH,/g VS. This yield is similar to results from

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492

Figure 6.

BORJA, SANCHEZ, AND DURAN

Ammonia concentration: 2 g N/l


10 20 30

Time (days)

" without zeolite with zeolite

40

Batch experiment at 2 g N/l ammonia concentration. Bars are the


previous experiments where the ammonia content was 1.5 g N/l [37] indicating that

the process was not inhibited by this increase in ammonia concentration.

The clay mineral zeolite exhibited a slight positive effect on the methane

production or the level of the VFA found in uninhibited biogas reactors (the reference

group) (Figures 1 and 2). The same result was obtained from the batch experiments

(Figure 5).

When the process was inhibited by ammonia, however, a clear positive effect

of zeolite was observed, resulting in less drastic changes in the biogas production and

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493

20 30Time (days)

- without zeolite - with zeolite

Figure 7. Batch experiment at 5 g N/l ammonia concentration. Bars are the


more rapid recovery of the process. This clearly demonstrates that an increased

resistance to ammonia inhibition is introduced by addition of zeolite. Besides, the

addition of zeolite in these reactors seems to counteract the inhibition by ammonia,

and this effect was probably a stabilization of the process, and not a directly "curing"

effect.

The exact mechanism of zeolite on ammonia inhibition has not yet been

revealed. Stotzky and Rem [24] observed that although montmorillonites buffering

capacity was one of the mechanisms by which montmorillonite stimulated bacteria,

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20 30

Time (days)

- without zeolite " with zeolite

Figure 8. Batch experiment at 7 g N/l ammonia concentration. Bars are the


additional mechanisms were involved. In our experiments the buffering capacity of

the zeolite was of no significance, as manure is already very strongly buffered by

ammonia and bicarbonate. There was no significant difference in pH in the reactors

where zeolite was added in comparison to the control reactors.

The major difference between the behaviour of the zeolite and the control

reactors was not clearly shown until 5 and 7 g N/l ammonia concentrations were

added, the range of concentrations in which the total ammoniacal nitrogen and

therefore the ion ammonium concentrations were higher. On the other hand, the

amount of zeolite used (2%) could not be higher because it would increase the

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apparent viscosity of the medium, hindering the mass transfer and decelerating the

process. Even so, it was sufficient to exchange the fraction of ammonium ion

concentration generated in the levels of ammonia nitrogen added. Thus, natural zeolite

containing clinoptilolite (41 %) have ion exchange properties showing high selectivity

for ammonium ion [38, 39]. Because of the properties of these materials as ionic

exchangers and adsorbers [40] they neutralize biological media by ionic exchange, and

can trap cells increasing their viability. The property of ionic exchange is very useful

in anaerobic wastewater treatment as cattle manure, because of the high amounts of

ammoniacal nitrogen and therefore of ammonia ions generated by bacteria metabolism

during the anaerobic treatment.

On the other hand, the presence of cations such as Ca2+ and Na+ in zeolite

could also partly explain the observed effect since these ions have been shown to

counteract the inhibitory effect of ammonia [14, 15].

During recent years many large scale joint anaerobic reactors have been

established in Europe. These plants receive raw materials from several farmers along

with industrial waste, for instance food industries. The mixing of several wastes leaves

the possibility of appropriate raw material management in order to achieve a more

stable digestion and to maximize biogas production [41]. Thus, addition of certain

types of wastes with properties similar to zeolite could, beside the actual treatment of

these wastes, be a cheap way to counteract inhibitory effects of different toxins.

ACKNOWLEDGEMENTS

The authors want to acknowledge the support of the Alexander Von Humboldt

Foundation to develop this work.

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RECEIVED: October 5, 1995ACCEPTED: November 10, 1995

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effect of the clay mineral zeolite on ammonia inhibition of anaerobic thermophilic reactors treating...

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