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Temperature and moisture effect on spore emission inthe fungal biofiltration of hydrophobic VOCsAlberto Vergara-Fernández a , Vanida Salgado-Ísmodes a , Miguel Pino a , Sergio Hernández b

& Sergio Revah ca Centro de Energías Renovables y Calidad Ambiental, Escuela de Ingeniería de ProcesosIndustriales, Facultad de Ingeniería, Universidad Católica de Temuco, Temuco, Chileb Departamento de Ingeniería de Procesos e Hidráulica (IPH), Universidad AutónomaMetropolitana-Iztapalapa, Distrito Federal, Méxicoc Departamento de Procesos y Tecnología, Universidad Autónoma Metropolitana-Cuajimalpa,Distrito Federal, México

Available online: 29 Feb 2012

To cite this article: Alberto Vergara-Fernández, Vanida Salgado-Ísmodes, Miguel Pino, Sergio Hernández & Sergio Revah(2012): Temperature and moisture effect on spore emission in the fungal biofiltration of hydrophobic VOCs, Journal ofEnvironmental Science and Health, Part A: Toxic/Hazardous Substances and Environmental Engineering, 47:4, 605-613

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Journal of Environmental Science and Health, Part A (2012) 47, 605–613Copyright C© Taylor & Francis Group, LLCISSN: 1093-4529 (Print); 1532-4117 (Online)DOI: 10.1080/10934529.2012.650581

Temperature and moisture effect on spore emission in thefungal biofiltration of hydrophobic VOCs

ALBERTO VERGARA-FERNANDEZ1, VANIDA SALGADO-ISMODES1, MIGUEL PINO1,SERGIO HERNANDEZ2 and SERGIO REVAH3

1Centro de Energıas Renovables y Calidad Ambiental, Escuela de Ingenierıa de Procesos Industriales, Facultad de Ingenierıa,Universidad Catolica de Temuco, Temuco, Chile2Departamento de Ingenierıa de Procesos e Hidraulica (IPH), Universidad Autonoma Metropolitana-Iztapalapa,Distrito Federal, Mexico3Departamento de Procesos y Tecnologıa, Universidad Autonoma Metropolitana-Cuajimalpa, Distrito Federal, Mexico

The effect of temperature and moisture on the elimination capacity (EC), CO2 production and spore emission by Fusarium solaniwas studied in biofilters packed with vermiculite and fed with n- pentane. Three temperatures (15, 25 and 35◦C) were tested and thehighest average EC (64 g m−3 h−1) and lower emission of spores (2.0 × 103 CFU m−3 air) were obtained at 25◦C. The effect of moisturecontent of the packing material indicates that the highest EC (65 g m−3 h−1) was obtained at 50 % moisture. However, lowest emission(1.3 × 103 CFU m−3 air) was obtained at 80 % moisture. Furthermore, the results show that a slight decrease in spore emission wasfound with increasing moisture content. In all cases, the depletion of the nitrogen source in the biofilter induced the sporulation, adecay of the EC and increased spore emission.

Keywords: Moisture, temperature, spore emission, Fusarium solani, fungal biofiltration, hydrophobic VOCs.

Introduction

The treatment of hydrophobic volatile organic compounds(VOCs) using filamentous fungi has been studied over thelast decade[1–4] because fungal biofilters have shown someinteresting traits including the ability to degrade a largenumber of VOCs, their resistance to low humidity andpH,[3,5,6] their capacity to colonize empty space with theaerial hyphae increasing the transport area and to penetratethe solid support increasing the availability of nutrients.[7–9]

On the other hand, fungal biofilters have some disadvan-tages such as slow startup,[10] increased pressure drop as aresult of the air flow obstruction provoked by the mycelialgrowth, the eventual air channeling formation and, finally,the possibility that, under certain conditions, spores areproduced and emitted along with the exiting air.[10,11]

One of the first reports on the emission of microorgan-isms from biofilters for VOCs treatment was performed

Address correspondence to Alberto Vergara-Fernandez, Escuelade Ingenierıa de Procesos Industriales, Centro de EnergıasRenovables y Calidad Ambiental, Facultad de Ingenierıa,Universidad Catolica de Temuco, Rudecindo Ortega 02950,Campus Norte, Casilla 15-D, Temuco, Chile; E-mail: avergara@uctemuco.clReceived June 16, 2011.

by Ottengraf and Konings.[12] Their work concluded thatthe number of microbial germs in the outlet gas of differ-ent full scale biofilters varies between 103 and 104 CFUm−3 air, which are only slightly higher than the numbersencountered in open air and of the same order of magni-tude encountered in indoor air. Later, Sanchez-Monederoet al.[13] evaluated biofiltration as a method to control theairborne microorganisms released at composting facilitiessuch as Aspergillus fumigatus and mesophilic bacteria. Re-sults showed that biofiltration achieved an average reduc-tion greater than 90 % and 39 % in the concentrations ofA. fumigatus and mesophilic bacteria, respectively. A. fu-migatus concentration after the biofilter was lower than1.2 × 103 CFU m−3 air.

Zilli et al.[14] studied laboratory scale biofilters filledwith different packing materials (peat and sieved sugar-cane bagasse) and operating with different allochthonousand autochthonous bacterial cultures. The biofilters weremonitored in parallel to assess the emission rate of airbornebacteria in the biofiltration of benzene-contaminated airstreams and it was found that the airborne bacteria concen-tration in the outlet air varied in the range of 1.0–4.0 × 103

CFU m−3 air, which was slightly higher than in the ambientair.

Water contained in the biofilters is critical to maintainproper performance; in general percentages between 40 at

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80 % are desirable for traditional supports.[15] Bohn andBohn[16] discussed the different expressions of moisturecontent and availability in porous media finding a correla-tion between moisture content, potential and water activity.This is important because, in general, the rate of metabolicactivity, which is associated to elimination capacity in biofil-ters, decreases with decreasing water availability in biofil-ters. Furthermore, mass transfer processes in biofilms arealso dependent on water content and, finally, water activ-ity of the supports may have an influence on the eventualsporulation and spore release according to Gervais et al.[17]

Evaluating the effect of moisture content is important giventhe influence of water on the physiology of fungi, includingspore production and emission, and elimination capacity(EC).

The aim of this work was to evaluate the effect of tem-perature and moisture content in the packing material onthe spore emission and EC of gaseous n-pentane in a fun-gal biofilter packed with vermiculite and inoculated withFusarium solani.

Materials and methods

Microorganisms

Fusarium solani CBS 117476, isolated initially by Arriagaand Revah,[1] was utilized in all experiments. Its preser-vation, cultivation conditions and spore production wasrealized according to Garcıa-Pena et al.[4]

Chemicals and mineral medium

1-pentanol (98.5 % ACS reagent) and n-pentane (99 %ACS reagent) were purchased from Merck, KGaA, Darm-stadt, Germany. The mineral medium used contained(g L−1): 18 NaNO3; 1.3 KH2PO4; 0.38 MgSO4·7H2O;0.25 CaSO4·2H2O; 0.055 CaCl2; 0.015 FeSO4·7H2O; 0.012MnSO4·H2O; 0.013 ZnSO4·7H2O; 0.0023 CuSO4·7H2O;0.0015 CoCl2·6H2O; 0.0015 H3BO3. The mineral mediumwas supplemented in all experiments with gentamicin(40 mg L−1) and chloramphenicol (50 mg L−1) to reducebacterial growth.

Biofilter systems

The experiments were performed in biofilters consistingof a 0.2 m height cylindrical glass column with an innerdiameter of 0.057 m (Fig. 1). All biofilters, were packedwith 97.6 g of dry vermiculite (0.5 L, bed void fractionof 60 % and particle size between 2 and 4.5 mm) mixedwith different volume of mineral medium, depending onthe desired moisture content and the fungi.

To reduce startup, each biofilter was inoculated with290 mL of mineral medium with active mycelium (fungalbiomass) to a concentration of 0.35 gbiomass L−1 (equivalent

to 1.03 mgbiomass g−1dry vermiculite). Biomass was previously

grown for 3 weeks at 25◦C with mineral medium, potatodextrose agar (2.0 g L−1) and 1-pentanol (1.0 g L−1).[10]

The effect of temperature was determined at 15, 25 and35◦C with the packing having a moisture content of 80 %.The response of moisture content was evaluated with 20, 35,50, 65 and 80 % moisture content at a constant temperatureof 25◦C. The addition of mineral medium in the biofilterswas performed at the beginning of each experiment only.

Air saturated with n-pentane was mixed with water-saturated air (using a humidification column) and intro-duced at the top of the biofilter with a flow rate of 0.4L min−1 (empty bed residence time (EBRT) of 1.25 min)corresponding to a superficial velocity of 15.4 m h−1. Then-pentane inlet concentration was 3.3 g m−3 correspondingto an inlet load of 160 g m−3

reactor h−1. For each conditiontested, one set of three replicates were made (Fig. 1). Amixture of the generated leachate and water were sprayedperiodically in order to control moisture during the time ofoperation.

Results from the biofiltration experiments are expressedin terms of n-pentane inlet load (L, g m−3

reactor h−1), biofil-ter elimination capacity (EC, g m−3

reactor h−1) and sporeconcentration (SC) based on the colony forming units(CFU m−3air) according to:

L = QVr

Sin (1)

EC = QVr

(Sin − Sout) (2)

SC = CFUQ · tm

(3)

where Sin and Sout are inlet and outlet n-pentane concen-tration, respectively (g m−3), Q is air flow (m3 h−1) and Vr isthe reactor volume (m3), tm is the time elapsed in the sporecounting method (h) and CFU is the colony forming units.

For equilibrium conditions between the liquid, solid, andvapor phases, the water potential may be related to thewater activity by Eq. 4[17]:

ϕ = RT · ln(aW)Vw

(4)

where R is the universal gas constant (8.31 × 10−5 m3 barmol−1 K−1), T is temperature (K), Vw is the partial molalvolume of water (18 × 10−6 m3 mol−1 up to moderate soluteconcentrations), aw is the water activity value and ϕ is waterpotential (bar).

Analytical methods

Gaseous n-pentane concentration and CO2 productionwere measured in triplicate by FID-GC and TCD-GC

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Fungal biofiltration of hydrophobic VOCs 607

Fig. 1. Schematic diagram of the laboratory-scale biofilter.

respectively, (Shimadzu 2014, Japan) equipped with a capil-lary column, model Rtx-5 Restex UE (30 m × 0.32 mm ×0.25 µm) and a Carbomex 1000 column. The n-pentaneconcentration was determined with a detector temperatureof 220◦C, injection temperature of 80◦C and column tem-perature of 200◦C and using nitrogen as a carrier gas. TheCO2 concentration was determined with an injection tem-perature of 65◦C, an oven temperature of 80◦C and the TCdetector at 100◦C.

The moisture content of packing material was mea-sured online using a ProCheck meter (Decagon Devices,Inc.), equipped with an EC -5 Soil Moisture detector.Water activity (aw) values for the vermiculite with dif-ferent water content were determined using a DecagonModel CX-2 Water Activity System according to the man-ufacturer’s instructions. The temperature in the bioreactorwas measured using a thermo-couple system (Cole-Parmer,USA).

The experimental system for the collection of spores wasadapted from Gorny et al.[18] The exiting gas from the biofil-ter was passed during a tm of 5 minutes through a system

with two glass cones of 0.044 m diameter, separated bya porous glass, where a hydrophilic mixed cellulose estersmembrane (MF, Whatman, 0.45 µm, 47 mm diameter) wasplaced (Fig. 2). Subsequently the membranes were placedon Petri dishes containing potato dextrose agar (PDA) andcultured at 30◦C for five days. The colony count was per-formed using a Leica lens model 2000 × 45. The fungalbiomass in the vermiculite was measured as volatile solidswith a thermogravimetric analyzer according to Arriagaand Revah.[1] The suspended biomass was determined bydry weight at 105◦C during 24 h. Measurements were donein triplicate.

Results and discussion

Elimination capacity

Figure 3 shows the EC and CO2 production rates obtainedat 25◦C with the support having different moisture con-tent. Figure 5 shows the same parameters obtained at 80 %

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608 Vergara-Fernandez et al.

Fig. 2. Schematic experimental system for the collection of spores.

of moisture content and different temperatures. In bothcases, the adaptation period for n-pentane degradation wasaround 2 days and the performance close to the maximumdeveloped in about 4–5 days, which was about three timesshorter than the time obtained by Ortiz et al.[6] in the n-pentane biofiltration with microbial consortia. This lowerstartup time is attributed to the use of active mycelium toreduce the lag phase.

Figure 3 shows the effect of the moisture content on theEC and CO2 production rate as a function of time. Watercontained in the biofilters is critical to maintain a properperformance and its availability, expressed water activityand water potential, are important because they directlyaffect mycelial growth and spore formation.[16, 17] The re-sults obtained during this work shows a direct dependencebetween the EC and the moisture content, this is when thebiofilter was operated at 20, 35, 50, 65 and 80 % of moisturecontent, a ECmax of 38, 52, 75, 65 and 75 g m−3 h−1 with anaverage steady state of around 36, 55, 65, 63 and 61 g m−3

h−1 were obtained, respectively.A mass balance was performed on the carbon of the

n-pentane consumed and CO2 produced in the differentexperiments, the results shown that the biofilters operatedat 20, 35, 50, 65 and 80 % moisture yielded 69, 73, 77,76 and 80 % mineralization, respectively (the results aresummarized in Table 1). The EC results with 20 % mois-ture content were significantly lower which is related tothe water activity as shown in Figure 4. Morales et al.[19]

reported for toluene biofiltration a removal efficiency de-crease of 50 % when the moisture content decreased from70 % to 40 %. However, when the moisture content was in

the 50 % to 80 % range no significant effects on the EC andn-pentane mineralization with values of 63(±1.9) g m−3 h−1

and 78(±2) %, respectively were observed.The EC results between 65 % and 80 % moisture content

are similar to those reported by Ortiz et al.[6] on the n-pentane biofiltration with the fungus Fusarium solani. Onthe other hand, for the moisture content below 50 %, then-pentane EC was similar to that reported by Dupasquieret al.[20] and twice of that reported by Paca et al.[21] us-ing bacterial biofilters. This may be due to the decreasein biological activity when the moisture content of pack-ing material is less than 50 %, which is not enough for theelimination of VOCs, although the lower moisture contentin the packing material may increase the bioavailability ofhydrophobic VOCs (lower partition coefficient).[8] On theother hand, the EC decreased 15 % (Table 1) when the mois-ture content was higher than 80 %, which may be relatedto a reduction in n-pentane solubility (partition coefficientincrease) associated to a more significant water film in thepacking materials.

Figure 5 presents an ECmax of 45 g m−3 h−1 when theexperiment was performed at 15◦C, with an average in thesteady state of 28 g m−3 h−1 and 80 % of the n-pentaneremoved was converted to CO2 (mineralization) (Table 1).At 25◦C, the ECmax obtained was 65 g m−3 h−1, with anaverage in the steady state of 63 g m−3 h−1 and 85 % miner-alization. Finally, at 35◦C, the ECmax obtained was 60 g m−3

h−1, with an average in the steady state of 58 g m−3 h−1 anda 63 % mineralization. The highest EC obtained at 25◦Creflects an appropriate equilibrium between the increasingbiological rates at higher temperatures which also reduce

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Fungal biofiltration of hydrophobic VOCs 609

Fig. 3. Effect of moisture content in the EC, CO2 production and spore emission at constant temperature of 25◦C. (•) Eliminationcapacity, (�) CO2 production and (bars) SC.

n-pentane bioavailability as the solubility of hydrophobicVOCs decreases (higher partition coefficient).[8,22]

The ECmax obtained at 25 and 35◦C were similar to thoseobtained by Ortiz et al.[6] (about 70 g m−3 h−1 for loads of100 g m−3 h−1) in the n-pentane biofiltration, operating ata temperature of 30◦C. On the other hand, the n-pentaneEC were under all conditions higher than the value of 12 gm−3 h−1 reported by Dupasquier et al.[20] using a biofil-ter inoculated with Pseudomonas aeruginosa at 30◦C incometabolism with MTBE.

In all the experiments, EC decayed after a short steadystate. This consistent behavior can be attributed to the de-pletion of nitrogen source in the biofilter, since only 0.23 gnitrogen were added at the startup of the experimentand not nutrients were supplemented during the opera-tion period. The nitrogen balance, considering the averagebiomass produced in all experiments (57.6 ± 4.7 mgbiomassg−1

dry vermiculite), and the percentage of nitrogen of Fusariumsolani of 6.47 %[10] suggested nitrogen limitation causingboth EC decay and sporulation.

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Table 1. Mineralization of n-pentane at different moisture contents of the packing material and temperature of operation.

Exp. Operation (d)

Total consumedn-pentane

(g m−3reactor)

Total producedCO2

(g m−3reactor)

Avg. EC insteady state(g m−3 h−1)

n-pentanerecovered asCO2 ( %)

Average finalbiomass

(mgbiomassg−1

dry vermiculite)

Temperature (∗)15◦C 22 10,823 26,457 28.3 80 50.325◦C 13 6,403 16,631 63.7 85 63.735◦C 15 11,551 22,236 58.7 63 68.7

Moisture content (∗∗)20 % 13 6,243 13,164 36.1 69 58.935 % 13 8,433 18,679 55.2 73 62.750 % 15 11,534 27,177 65.1 77 52.365 % 13 10,922 25,226 63.1 76 53.380 % 16 11,784 28,694 61.2 80 55.4

(∗) constant moisture content (80 %).(∗∗) constant temperature (25◦C).

Effect of moisture content on spore emission

The results for spore emission (represented as SC) as a func-tion of the moisture content are shown in Figure 3 for eachexperiment. In all cases the results showed two distinct pe-riods, one associated to startup and the second when thebiofilter performance showed activity decay possibly due tonitrogen limitation as mentioned previously. According toDahlberg and Van Etten[23] the spore emission in the firstperiod could be associated with transferring the myceliafrom liquid medium (culture) to packing material (biofilter)as reported for Aspergillus nidulans; and changes in the car-bon source (from PDA and 1-pentanol to n-pentane) thatstimulate the differentiation and are one of the more com-mon methods used to induce sporulation in diverse fungi.The second period started after 150 hours of operation andcan be correlated to EC decay derived from the depletionof nitrogen source in the biofilter. Sporulation under starv-ing and nutritional depletion has been described for manyfungi by Dahlberg and Van Etten.[23] Furthermore, sporu-lation is a defense mechanism to adverse conditions andstress.[24, 25]

Figure 6 was constructed for the second sporulation pe-riod for each moisture content from the EC and averagespore emission data depicted in Figure 3. The results glob-ally show an increased spore emission with reduced mois-ture, which may be explained from both the higher sporeformation expected by the stress provoked by reduced watercontent (Fig. 4) and possibly by better spore retention fa-vored by the increased filtering capacity with a more humidsupport. In general, the results show that the average SC arein range of 1.8(±0.5) × 103 CFU m−3 (Fig. 6). These valuesare similar to those already reported for airborne bacteriaemissions from biofilters operating with a moisture con-

Fig. 4. Relation of packing material moisture contents to waterpotential and water activity. The aw of natural packing material(15 % moisture content) is 0.792.

tent of packing material between 40–60 % (w/w)[12] andonly slightly higher than the concentration measured in theindoor air (1.0 × 103 CFU m−3).[14]

Effect of temperature on spore emission

Figure 5 shows that spore emission at the three temper-atures studied had the same pattern previously describedfor the moisture effect and that no emission was detectedduring the period of ECmax (steady state). Temperature af-fected spore emission during the second sporulation periodand the highest SC of 8 × 103 CFU m−3 air was quantifiedin the biofilter operated at 15◦C, while it was 2.0 × 103 CFU

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Fungal biofiltration of hydrophobic VOCs 611

Fig. 5. Effect of temperature in the EC, CO2 production and spore emission at constant moisture content of 80 %. (•) Eliminationcapacity, (�) CO2 production and (bars) SC.

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Fig. 6. Effect of moisture content on the EC and spore emissionat constant temperature (25◦C). (•) EC and (bars) SC.

m−3 air at 25◦C and 4 × 103 CFU m−3 air at 35◦C. These val-ues are slightly higher than the concentration reported forairborne Aspergillus fumigatus emissions (1.2 × 103 CFUm−3) from biofilters operating with a temperature between18–22◦C and a moisture content of packing material be-tween 50–70 % (w/w).[13]

Finally, is possible to establish that temperature playsan important role in affecting both the EC and the sporeemission. In the first case similar EC (60 g m−3 h−1) wasfound in the biofilters operated at 25 and 35◦C. However,the average number of spores generated at 25◦C was 50 %lower than those obtained at 35◦C. Therefore, it is possi-ble to establish that the operation at 25◦C causes the leastimpact on the spore emission, while allowing the highestn-pentane EC.

Conclusions

The results suggest that the fungal biofilter can be aneffective treatment process for the removal of n-pentane.The results of spore emissions obtained are slightly higherthan those reported in indoor air. This suggests that fun-gal biofilters do not pose a significant risk to health, if theoperating conditions (temperature, moisture and nutrients)are secured. The best conditions found were a temperaturearound 25◦C and a moisture content of around 80 %, whichyielded higher EC and lower spore emission. Spore emis-sion in fungal biofilters was shown to be generated in twostages during its operation, the first period occurs duringthe inoculation of the fungus and adaptation to the packingmaterial and carbon source gas (hydrophobic VOCs), andthe second associated with the decline of the EC (limitingsource of nitrogen). The extent of the EC decay, favored inthese experiments by limiting nitrogen availability, has animpact on spore emission which has shown to depend onmoisture and temperature. In general it can be concluded

that maintaining high metabolic activity (i.e. high EC) wasnecessary to limit spore emission.

Acknowledgments

The present research has been sponsored by theCONICYT-Chile (National Commission for Scientific andTechnological Research) (FONDECYT Project Number11080036).

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