Biotechnology Advances 36 (2018) 1079–1093

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Biotechnology Advances
journal homepage: www.elsevier.com/locate/biotechadv

Research review paper

Biofiltration of volatile organic compounds using fungi and its conceptual T

and mathematical modeling
⁎
Alberto Vergara-Fernándeza, , Sergio Revahb, Patricio Moreno-Casasa, Felipe Scotta
a
Green Technology Research Group, Facultad de Ingeniería y Ciencias Aplicadas, Universidad de los Andes, Chile
b
Departamento de Procesos y Tecnología, Universidad Autónoma Metropolitana-Cuajimalpa, Mexico

A R T I C LE I N FO A B S T R A C T

Keywords: Volatile organic compounds (VOCs) are ubiquitous contaminants that can be found both in outdoor and indoor
Biofiltration air, posing risks to human health and the ecosystems. The treatment of air contaminated with VOCs in low
VOC concentrations can be effectively performed using biofiltration, especially when VOCs are hydrophilic. However,
Fungi the performance of biofilters inoculated with bacteria has been found to be low with sparsely water soluble
Bacteria
molecules when compared to biofilters where fungi develop. Using conceptual and mathematical models, this
Modeling
review presents an overview of the physical, chemical and biological mechanisms that explain the differences in
Computational fluid dynamics
the performance of fungal and bacterial biofilters. Moreover, future research needs are proposed, with an em-
phasis on integrated models describing the biological and chemical reactions with the mass transfer using high-
resolution descriptions of the packing material.

1. Introduction adults (Elliott et al., 2006), induce inflammatory reaction of airways,

Atmospheric pollution has become one of the major causes of pre-
mature death in developed and developing countries. Using data from
the Global Burden of Diseases Study 2015, Cohen et al. (2017) reported
that fine particulate material (PM2.5) alone was responsible for 4.2
million deaths in 2015, compared to 3.5 million in 1990. Nearly 60% of
these deaths took place in east and south Asia. While the role of other
contaminants is well understood, such as ozone causing an additional
0.25 million deaths, the impact of volatile organic compounds (VOCs)
has not been fully quantified, despite having a role in ozone formation
and that often they are associated to PM and polycyclic aromatic hy-
drocarbons (PAHs) (Kundu and Stone, 2014). VOCs comprise a group of
organic chemicals with a high vapor pressure at room temperature and
are commonly present in indoor and outdoor air (Khan and Ghoshal,
2000). VOCs are emitted from industrial sources, such as petroleum
refineries and chemical plants (Hoyt and Raun, 2015), commercial
activities, such as gasoline refilling (Harley et al., 2006); and at the
residential level, wood and fossil fuels burning for heating and cooking
(Evtyugina et al., 2014) and products used indoor like aerosols, paints
and cleaners (Bernstein et al., 2008). VOCs such as the low-boiling
hydrocarbons (pentane, hexane, heptane, etc.), alcohols, aldehydes,
halogenated hydrocarbons, ethers and PAHs represents 7% to 10% of
all atmospheric pollutants emitted (Delhoménie and Heitz, 2005).
These compounds have been shown to reduce pulmonary function in
immunological abnormalities and neurological symptoms (Win-Shwe
et al., 2013) and an increased carcinogenic risk for formaldehyde,
benzene, acetaldehyde and naphthalene (Sarigiannis et al., 2011). The
changes and mechanisms behind some of these responses to VOCs ex-
posure have been recently studied in mice (Wang et al., 2012) and lung
cells (Gostner et al., 2016). However, the lack of understanding of the
mechanisms involved, did not preclude establishing links between
VOCs exposure and health issues. In this regard, a study lasting 12 years
and including nearly 60,000 Toronto residents, found that the exposure
to ambient levels of benzene, n-hexane and total hydrocarbons were
associated with an increased risk of cancer mortality (Villeneuve et al.,
2013).
Depending on the airflow and their concentration, VOCs can be
abated using purely physico- chemical technologies such as gas mem-
brane separation, condensation and adsorption (typically used for high
VOCs concentrations and low to medium air flows), incineration and
catalytic oxidation (for high concentration of VOCs and large air flows)
and biotechnological processes for dilute VOCs streams. The reviews by
Revah and Morgan-Sagastume (2005) and Delhoménie and Heitz
(2005) represent comprehensive assessments of the applicability of the
different technologies which can be complemented with the work of
Estrada et al. (2012) to gain a broad perspective of the applicability and
costs of the most commonly applied VOCs abatement technologies.
Biofiltration has become a viable economic and technical

⁎
Corresponding author at: Mons. Álvaro del Portillo 12455, Las Condes, Santiago 7620001, Chile.
E-mail address: aovergara@miuandes.cl (A. Vergara-Fernández).

https://doi.org/10.1016/j.biotechadv.2018.03.008
Received 9 January 2018; Received in revised form 9 March 2018; Accepted 14 March 2018
Available online 17 March 2018
0734-9750/ © 2018 Elsevier Inc. All rights reserved.
A. Vergara-Fernández et al.
alternative for the treatment of airstreams with low concentrations of
volatile organic and inorganic compounds (such as H2S and NH3) in
waste gas streams. It is based on the capacity of an active microbial
population, usually growing on a solid support in a biofilm, to trans-
form the pollutants into less harming molecules, namely carbon di-
oxide, sulfates, nitrates, etc. (Revah and Morgan-Sagastume, 2005) in a
process that shares similarities with the microbial degradation of pol-
lutants in soils (Ren et al., 2018).
The inherent heterogeneity and complexity of biofilters make the
analysis and mathematical modeling of these systems a challenging
task. In such models, not only mass transport, fluid flow through porous
beds and biochemical reactions are entangled; but also, the properties
of the biofilm, such as the thickness of the active biomass layer, and of
the solid inert support play a role, for example in determining the area
of the biofilm (Spigno and Tronci, 2015; Vergara-Fernández et al.,
2008).
As the deployment of industrial biofilters has consistently grown
since the late 80’s, so has been the increasing complexity of the con-
ceptual and mathematical models developed for VOCs abatement in
fixed bed biofilters. In this regard, reviews in the area are devoted to the
conceptual analysis of biofiltration systems (Devinny and Ramesh,
2005), to the use of fungi in biofilters (Kennes and Veiga, 2004), the
mass transfer aspects in biofilters (Kraakman et al., 2011) and on how
to reduce the mass transfer limitations (Cheng et al., 2016; Ferdowsi
et al., 2017). However, a revision of the action of fungi in the treatment
of volatile organic compounds and its modeling, including detailed
descriptions of the phenomena occurring in the reactor (mass, heat and
momentum transport) and of the microbial growth and biodegradation
kinetics, is missing.
In this review, results from biofiltration experiments are expressed
in terms of the empty bed residence time (EBRT, s), VOCs inlet load (L,
g m−3
reactor h
−1
), biofilters elimination capacity (EC, g m−3
reactor h
−1
) and
removal efficiency (RE, %) according to:
Vr
EBRT =
Q (1)
Q contaminants are transferred from the gas phase to the liquid phase
EC = (CG0 − CG (out ) )
Vr (2)
Q fungal biofilters. The contaminants diffuse or are transported to the
L= (CG0)
Vr (3)
(CG0 − CG (out ) )
RE = 100
CG0 (4)
where CG0 and CG(out) are inlet and outlet VOCs concentration, re-
spectively, Q is airflow and Vr is the reactor volume.
This review is organized as follows: the individual biological and
physicochemical phenomena involved in fungal biofiltration are re-
viewed and compared with the bacterial case; (Section 2) next, the
modeling efforts to integrate these aspects, understanding of the ex-
perimental information and optimization of biofilters design are re-
viewed in Section 3. Finally, the characteristics and performance, in
terms of elimination capacity, are compared and analyzed for fungal
and bacterial biofilters treating several VOCs.
The remaining of this paper is devoted to reviewing the current
understanding of the physical, chemical and biological phenomena in-
volved in fungal biofiltration and its modeling compared to bacterial
biofiltration.
2. Physicochemical and biological phenomena in a fungal biofilter
and its mathematical modeling
Biofilters are multiphasic reactors that respond to diverse spatial
and temporal scales. From molecular diffusion and reaction to micro-
bial growth and gas or liquid channeling, modeling of phenomena in-
volved in the operation of biofilters presents challenges to the modeler
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Biotechnology Advances 36 (2018) 1079–1093
on whether using an approach tailored to each spatial and temporal
scale or using an aggregated (or lumped) model. Despite the approach
used, models must produce macroscopic outputs, often the only mea-
sured quantities in an experimental system, to compare model predic-
tions, such as elimination capacity for contaminants and pressure drops,
with the operation of the system being modeled. This section aims at
introducing the general principles involved in the phenomena of mass
and energy transport, as well as the biomass growth and biodegradation
kinetics. Each aspect will be the subject of the forthcoming sections,
dedicated to reviewing the application of these principles to the mod-
eling of fungal biofilters. Before introducing the physical, chemical and
biological mechanisms involved in biofiltration of air, a precision re-
garding biofilters and biotrickling filters needs to be made. While bio-
filters have a static water phase associated to the biofilm and the sup-
port; in biotrickling filters water is constantly supplied producing a thin
water film flowing over the packing and the biofilm. However, in the
laboratory and industrial practice, biofilters are intermittently supplied
with water, or a nutrient solution, to ensure appropriate moisture
contents at regular time intervals, some are washed for as much as
20 min in each hour (Devinny and Ramesh, 2005). On the other hand,
because unsaturated gravitational flow in porous media is difficult to
control, biotrickling filters are likely to include patches that are not
properly covered with water.
For highly soluble organic compounds, such as alcohols, the parti-
tion coefficient favors a higher concentration in the water phase, which
promotes the biodegradation of the contaminant by increasing its
concentration in the environment surrounding the biofilm (Cohen,
2001). On the other hand, in fungal biofilters, if a layer of flowing water
would be created over the solid support, then it would decrease the
surface area created by the aerial hypha, thus impairing the transfer of
VOCs, especially hydrophobic ones, to the biomass phase (Sugai-
Guérios et al., 2015).
Fig. 1 shows a conceptual model of a biofilter. Contaminants are
transported into the biofilter by the air at rates that justify assuming
that the flow is laminar. However, dispersion occurs due to the tortu-
osity of the porous packing. As the air flows through the packing,
embedded in the biofilm (for bacterial biofilms), or to the fungal hypha
and to the water embedded in the non-aerial portion of the biomass in
biofilm and then degraded by the microbial catabolic activity. As most
biofilters are used to treat polluted air and thus are based on the activity
of aerobic microorganisms, the availability of oxygen is also an im-
portant issue as well as the retro-diffusion of metabolic products such as
CO2. Relevant variables affecting the mass transfer of contaminants and
oxygen in the reactors include the flow regimes, pressure drop, void
fraction of the packed-bed, biofilm wetting; and for trickle-bed bio-
filters, the flow of liquid and liquid hold-up (Lobo et al., 1999) and
therefore are often considered in models of biofilter operation.
In biofilters, the mass transfer parameters associated with the fluid
mechanics of the system, e.g. the diffusion coefficient of the con-
taminant in air, have been traditionally estimated using the correlation
proposed by Fuller et al. (1966), based on the molecular diffusivity of
the species. Similarly, the diffusion coefficients of the nutrients from the
liquid media in the biofilm have been estimated using de Nernst-Haskell
equation (Vergara-Fernández et al., 2008) and the axial dispersion
coefficient, a measure of the deviation from plug-flow regime in a re-
actor, has been approximated using the correlation proposed by
Edwards and Richardson (1968). However, the aerial mycelia and the
colonization of the void space in the biofilter, when filamentous fungi
are used, might lead to discrepancies between the predicted and ob-
served values of these coefficients.
2.1. Mass transfer of species in the gas phase and reaction in the biofilm
The temporal variation of the concentration of a compound; either a
A. Vergara-Fernández et al.
Fig. 1. Scheme of a conceptual model of a fungal biofilter showing the different scales involved.
pollutant, oxygen or any other chemical species, in a differential vo-
lume of gas can be obtained by assuming that there is no radial dis-
persion, that a species enters the control volume by advection (bulk
transport in the air) but its transport is delayed by axial dispersion
(accounted for using an effective dispersion coefficient, DDz) leaving the
control volume at a rate governed by the specific mass flux of compo-
nent i from the gas phase to the interface (NG,i), the specific area of the
gas-liquid or gas-biofilm interface (a, interface surface per unit volume
of biofilter bed), and the void fraction occupied by the gas (ε). These
purely physical transport mechanisms are regarded as the mass balance
for component i in the gas phase (Eq. 5).
∂CG, i ∂CG, i ∂2CG, i a
= vg − DDz − NG, i
∂t ∂z ∂z 2 ϵ (5)
where, CG,i = CG,i(t,z) represents the concentration of contaminant i in
the gas phase at a given position in the axial direction (z) of the reactor
at a certain time (t) and υg is the gas velocity. Considering that com-
ponent i is being transferred from the bulk of the gas phase to a stagnant
layer of gas, the specific mass flux (NG,i) can be calculated using the
Fick's law:
Cb, i
NG, i = Db, i ∂
∂x x=0
Where, Db,i is the diffusion coefficient in the biofilm, Cb,i is the
concentration of contaminant i in the biofilm, and coordinate x de-
scribes the thickness of the stagnant layer of gas and x = 0 denotes the
interface between the stagnant layer of gas and its bulk (Fig. 1).
The next transfer step delivers the contaminant from the stagnant
layer of gas to a layer of water in biotrickling filters, or to the biofilm in
biofilters. In the latter, and when bacteria are the oxidizing micro-
organisms, the transport across a layer of water can be omitted if the
biofilm is assumed to be a pseudo-homogeneous phase composed of
water and microorganisms (Fig. 2.b). The mass balance of any com-
ponent, considering reaction and diffusion within the biofilm according
to Fick's Law, can be written as:
Biotechnology Advances 36 (2018) 1079–1093
∂CG, i ∂2CG, i
= Db, i +r
∂t ∂x 2 (7)
where, Cb,i = Cb,i(t, xb) is the concentration of contaminant i at a given
time and thickness in the biofilm (x). The reaction rate (r) accounts for
the catabolic reaction that allows the microorganisms embedded in the
biofilm to oxidize the contaminant.
In fungal biofilters (Fig. 2.a), a contaminant is transported directly
from the gas phase to the aerial hyphae (Vergara-Fernández et al.,
2016). This situation can be represented by a simplified form assuming
a negligible concentration gradient within the hyphae and an overall
mass transfer coefficient (KG):
∂CG, i CG, i
= K G a ⎛⎜ − Cb, i⎞⎟ + r
∂t m
⎝ i, G , b ⎠ (8)
where, mi,G,b represents the partition coefficient of contaminant i be-
tween the gas phase and the biomass.
As it can be seen, the driving force for the transfer of the con-
taminant to the biofilm is determined by the difference between the
equilibrium concentration at the gas-biofilm interface, where the par-
tition coefficient plays a key role, and the concentration of the pollutant
in the biofilm, controlled by the catabolic activity of the microbial
population.
(6)
The diffusivities of low molecular weight contaminants in the gas
phase are in the range of 1⋅10−5 m2 s−1 (Tang et al., 2015) while in
water is close to 1⋅10−9 m2 s−1 (Harms and Bosma, 1997). The diffu-
sivity within biofilms can be expected to be lower than in pure water. If
the biofilm is conceptualized as a cluster of cells surrounded by water
and exopolymers, then, transfer of substances within the biofilm can be
regarded as a combination of advection within voids and water chan-
nels permeating the biofilm and diffusion within cell clusters and the
exopolymeric matrix (Guimerà et al., 2016). Thereby, since a biofilm
cannot be regarded as a homogeneous system, the measured diffusion
coefficient is an effective diffusion coefficient (De).
In fungal biofilters the aerial mycelium is in direct contact with the
gas phase while the non-aerial mycelium lies within the watery biofilm.
The formation of the aerial hyphae requires decreasing water surface
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A. Vergara-Fernández et al. Biotechnology Advances 36 (2018) 1079–1093

Fig. 2. Conceptual model of an aerial biofilm (a) and a monolayer biofilm (b) (Vergara-Fernández et al., 2016).

Fig. 3. Model for the formation of aerial hyphae aided by hydrophobins. The model was adapted from Wösten et al. (1999). A very similar model was proposed to explain the aerial
growth of the bacteria Streptomyces coelicolor (Claessen, 2003).

tension from 72 mJ m−2 to values as low as 30 mJ m−2 (Wösten et al.,
1999). To overcome the barrier imposed by the surface tension of
water, the submerged hyphal cells secrete hydrophobins, see Fig. 3.
Hydrophobins are thus surfactant proteins (with molecular weight of
≈10 kDa), capable to self-assembly at hydrophilic-hydrophobic inter-
faces and which protect the fungal aerial structures (Vigueras et al.,
2009). These proteins, containing 100 or more amino acids (Schor
et al., 2016; Vigueras et al., 2008), also form a hydrophobic coating on
the aerial hyphae, fruiting bodies and spores, allowing hyphae to co-
lonize hydrophobic materials (Wösten et al., 1994), possibly playing a
role in preventing desiccation (Linder et al., 2005) and facilitating the
dispersion of spores into the air (Bayry et al., 2012). Hydrophobins

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A. Vergara-Fernández et al.
promote the solubilization of hydrophobic VOCs in biofilters by acting
as a coating of the aerial mycelium. The solubilizing of hydrophobic
VOCs can be quantified using partition coefficients.
In general, models reported in the available literature are based on
mass transfer principles, with the main objective of determining the
elimination capacity of fungal biofilters. In order to do this, the gas
phase and biofilm transport equations are mainly considered, as well as
their relation to diffusion conditions of the contaminants and nutrients,
dispersion (described in the previous section), partition coefficient, and
mass transfer coefficient, among others (Kraakman et al., 2011).
2.1.1. Partition coefficient
In general, fungal biofilters are modeled considering a contaminant
partition coefficient in the gas phase/biomass as an air/water Henry's
constant. Systems were this assumption was made include α-pinene
degradation using an Ophiostoma specie (Jin et al., 2006), xylene and
mixed bacteria and fungi (Li and Liu, 2006), hexane and Fusarium solani
(Arriaga and Revah, 2009; Hernández-Meléndez et al., 2008; Vergara-
Fernández et al., 2006), toluene and a fungi consortium (Dorado et al.,
2008). Nevertheless, the partition is modified when fungal biomass is
present in the aqueous biofilm. This situation was observed by Vergara-
Fernández et al. (2006), by determining that n-hexane solubility can
increase up to 200 times with respect to the solubility of water in
presence of filamentous fungi.
The partition coefficient (Kbiomass) of fungal biomass may be ex-
pressed as proposed by Vergara-Fernández et al. (2006) and Davison
et al. (Davison and Barton, 2000):
Cheadspace
KBiomass =
Cbiomass (9)
where, Cheadspace and Cbiomass are the concentration of the contaminant
in the headspace and biomass, respectively.
The partition coefficient of the dried biomass can be expressed as a
function of its composition and the individual partition coefficients of
the lipid-free biomass and the lipid component by Eq. (10). Similarly,
the partition coefficient for the biomass on a wet basis can be calculated
by Eq. (11) that includes the water fraction and the partition coefficient
in water (which correspond to the Henry Coefficient).
lipid − free
1 xlipid xbiomass
= +
dry
Kbiomass Klipid lipid − free
Kbiomass (10)
1
dry
xbiomass x water
wet
= dry
+ at the bottom of the packing. Then, the following equations represent
Kbiomass Kbiomass Kwater (11)
where, x represents the mass fractions of water, lipids or biomass; and K
represents the partition coefficient in biomass, water and lipids.
Vergara-Fernández et al. (2011b; 2006), obtained biomass partition
coefficient values with Fusarium solani in the range of 0.033–0.04 for n-
hexane and 0.015–0.032 for n-pentane, respectively, which are around
three orders of magnitude lower as compared to water. Furthermore,
Vergara-Fernandez et al. (2011b), determined the n-pentane/dry-bio-
mass partition coefficient in microcosms for the same fungus when
grown in four packing materials (compost, peat, perlite and vermicu-
lite) at different temperatures (15 °C, 25 °C and 35 °C). Results indicated
that the n-pentane/wet-biomass partition coefficients in organic
packing material were 160-fold lower (0.21 ± 0.09) than those in
water (33.2 ± 9.4), while for inorganic packing material they were
700-fold lower (0.05 ± 0.04). The authors attributed this result to the
fact that, when grown over an inorganic packing material, the growth
of F. solani is supported only by n-pentane in the gas phase and not from
the carbonaceous material present in the organic packing material.
Thus, an increased hydrophobicity of the surface of the mycelium,
caused by the presence of hydrophobins, would result in a more effi-
cient mass transfer of n-pentane from the gas phase. The role of hy-
drophobins in the biofiltration of slightly soluble contaminants is
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Biotechnology Advances 36 (2018) 1079–1093
supported by the fact that when F. solani is grown in glucose, or other
soluble carbon sources such as 1-hexanol and glycerol, the partition
coefficients are higher than those obtained when grown in n-hexane (in
the gas phase).
In another approach, Salehahmadi et al. (2012), in their mathe-
matical model for fungal biofiltration, applied the method described by
Mackay (Mackay, 2001), in order to determine the n-hexane/biomass
(K) partition coefficient. The model is based on that the organic content
of the biomass is responsible for the hydrophobic VOCs absorption,
which in turn can be related to the octane/air (Koa) (Eq. 12) coefficient.
1
= 4.1·10−4 [K oa yρb ]
Kbiomass (12)
where, ρb is the biofilm density and y represents the organic content.
2.1.2. Axial dispersion
Axial dispersion is the deviation from the ideal plug-flow regime in
a pipe, column or reactor. It can be caused by multiple factors, in-
cluding the packing geometry and size, a non-uniform distribution of
the feed stream, channeling or short-circuiting creating dead zones, and
specifically for fungal biofilters, the growth of aerial hyphae occupying
the void space (Prenafeta-Boldú et al., 2008).
The correlation proposed by Edwards and Richardson (1968) was
used by Vergara-Fernández et al. (2008) in the estimation of the axial
dispersion coefficient in the phenomenological modeling of a fungal
biofilter treating n-hexane. Helfferich (Helfferich, 1985) proposed an
empirical correlation for the axial dispersion coefficient in a packed-bed
as a function of the bed porosity (ε), gas velocity (ug), packing diameter
(dp) and the specie diffusion coefficient (DA) (Eq. 13). Although this
expression does not account for the presence of bacterial or fungal
biofilms, it was nevertheless used by Salehahmadi et al. (2012) in
fungal biofilters.
D = (0.45 + 0.55ϵ) DA + 0.5dP ug /ϵ (13)
In a different approach, Prenafeta-Boldú et al. (2008) showed that
the gas residence time distribution (RTD) can be determined using an
air dispersion model. The model was experimentally validated in a
fungal biofilter inoculated with Cladophialophora sp. using methane as
tracer-gas. The dispersion study was carried out in two laboratory scale
biofilters packed with granular perlite and polyurethane foam. The
recorded pulse RTD curves were modeled as being equivalent to a series
of CSTR (Eq.15). Two additional CSTR compartments of constant vo-
lume were added to account for the void spaces present at the top and
the proposed CSTR system for the estimation of the RTD:
dM0 Q
= − M0
dt Vin (14)
dMi n
= (Mi − 1 − Mi ), i = 1, 2, …, n with Mi − 1 = 0 if i = 1
dt τ (15)
dMn + 1 Q
= (Mn − Mn + 1)
dt Vout (16)
where Mi is the contaminant gas concentration in tank i and τ is the
mean residence time of the tracer gas equivalent to that of the flowing
air, the effective bed void volume can be calculated as:
Ve = τ ·Q (17)
Spigno and De Marco Faveri (2005) analyzed the RTD in a biofilter
model of a fungal biofilter inoculated with Aspergillus niger for n-hexane
abatement. They found a small axial dispersion coefficient of
1.22·10−4 m2 s−1.
2.1.3. Diffusion coefficient in the biofilm
The main parameters affecting the diffusion of a contaminant in the
fungal biofilm are the temperature and the biomass density, where the
A. Vergara-Fernández et al.
diffusion coefficient for biofilms is found to be slightly lower than the
one for water. However, this parameter should be considered only for
the cases in which the biomass attached to the support is modeled (not
the aerial biomass), since it is customary to consider that the con-
taminant reacts instantaneously once it is in contact with the surface of
the aerial hyphae (Vergara-Fernández et al., 2016, 2008).
The diffusion coefficient for fungal biofilters, might be approxi-
mated by applying the empirical correlation of Wilke and Chang
(1955). This method was used by Spigno and De Marco Faveri (2005)
by assuming the value of the diffusion coefficient to be 40% of its value
in water, with a resulting estimated diffusion coefficient of 0.74
×10−9 m2 s−1. Instead, Arriaga and Revah (2009) applied the ex-
pression for impermeable sphere-packed porous media by Neale and
Nader (1973) in a mathematical model of hexane degradation in fungal
biofilters, obtaining the following effective diffusivity for hexane (Eq.
18):
Def 2ϵ
= 2.3. Drying, metabolic activity and heat generation
DHwater 3−ϵ (18)
where, Def is the effective diffusivity in the biofilm, ε is the bed void
fraction, and DHwater is the diffusivity in water. The bed void fraction
can be obtained according to:
Vwater
ϵ=
Vtotal (19)
where, Vwater is the volume occupied by the water in a total volume
(Vtotal) packed with a support material. The authors reported a Def/
DHwater of 0.35 for bacterial biofilms, and 0.19 for fungal biofilms, with
effective diffusivity in fungi of 4.1×10−7 m2 h−1.
2.2. Pressure drop
The pressure drop in fungal biofilters is one of the most important
operational parameters to be considered. The increase in the pressure
drop can be caused by several factors including entrapment of particles
transported in the air entering to the reactor, bacterial growth and by
the aerial growth of filamentous fungi, diminishing the void fraction,
and therefore reducing the permeability of the porous media of the
bioreactor. Since air entering to biofilters is commonly prefiltered and
humidified, the load of particles that can cause cloging of the reactor is
reduced, along with the concentration of highly water soluble VOCs.
Estrada et al. (2013) found pressure drop increments for fungal (Pae-
cilomyces variotti) and bacterial biofilters of 91 to 912 Pa m−1
bed and 91 to
372 respectively, for the treatment of a VOC mixture, showing how
fungi can introduce significant resistance to the moving flow compared
to bacteria. Similar values, between 98 and 350 Pa m−1 bed, were obtained
Prenafeta-Boldú et al. (2008) in a fungal biofilter inoculated with Cla-
dophialophora sp. strain CBS 110553 for the removal of toluene using
perlite granules as packing material.
The pressure drop evolution over time in a fungal biofilter was
evaluated by Vergara-Fernández et al. (2008) by applying the Darcy
equation (Eq. 20).
ΔP 72ω (1 − ϵ)2 ⎞ ⎛ μf ⎞
⎛ ⎞ = ⎛⎜
⎝H ⎠ ⎝ ϵ 2dp2
⎟⎜ ⎟ vg
⎠ ⎝ ρg g ⎠ (20)
where, ΔP is the pressure drop, H is the biofilters height, ϖ is the tor-
tuosity factor, ε is the bed porosity in the biofilters, dp is the particle
diameter, μf dynamic viscosity of the fluid, ρg is the gas density, g is the
acceleration of gravity, and vg is the gas superficial velocity.
Where the void fraction can be evaluated as a function of fungal
growth by application of Eq. (21):
ϵ(t ) =
Vr − ⎡VE +
⎣ ( )d
π
4
2
hyphae Lhyphae, Total (t ) ⎤
⎦
Vr (21)
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Biotechnology Advances 36 (2018) 1079–1093
Above, Vr is the reactor total volume, VE is the total volume of the
support, dhyphae is the hyphae diameter obtained from morphological
observations and Lhyphae,Total is the total length of the hyphae which can
be calculated as shown in Eq. (26).
An important aspect to be considered when simulating the pressure
drop in a fungal biofilter at the initial stages of operation, is the amount
of static liquid present in the bed. This behavior can generate a de-
viation of up to 11% from experimental measurements when it is not
accounted for in the mathematical model (Vergara-Fernández et al.,
2008). The maximum pressure drop obtained in the latter study goes up
to about 45 mmH2O m−1 bed. On the other hand, Zamir et al. (2011a,
2011b) obtained a pressure drop approximately four times smaller
(11 mmH2O m−1 bed), than those obtained by Vergara-Fernández et al.
(2008) using a gas flow three times lower and half the residence time in
the toluene elimination in a fungal biofilter inoculated with the fungus
Phanerochaete chrysosporium.
Packing and biofilm moisture content, metabolic activity and heat
generation are intimately intertwined. Moisture balance is affected by
thermodynamic phenomena, the equilibrium between the content of
water in the biofilm and the moisture in the gas stream, the water
transfer rate from the solid support to the biofilm (in biofilters).
Humidification of the contaminated air stream entering the biofilter is a
common practice to avoid biofilm drying, incomplete humidification of
the air stream (relative humidity < 100%) evaporates moisture from
the solid support and biofilm at a rate that depends on inlet tempera-
ture, initial relative humidity and empty bed residence time. The heat
liberated by the oxidation of gaseous pollutants, especially those with
high upper heating values such as alcohols, alkanes and alkenes, in-
creases the evaporation rate. van Lith et al. (1997) estimated that a
biofilter operated with inlet contaminant concentration of 0.5 g m−3
and volumetric load of 50 g m−3 h−1 loses 30 L of water per cubic
meter of packing in a period of 3 to 6 days. This drying mechanism is
especially relevant near the biofilter influent where the highest VOCs
concentrations are found. In this regard, Gostomski et al. (1997) pro-
vide experimental results showing that the degradation caused by heat
generation and water evaporation started in a narrow zone at the inlet
of the bed, however, as the loss of water inhibited the microbial activity
of this area, the degradation region progressed through the bed.
Insufficient moisture prevents the formation of either bacterial or
fungal wet biofilms, that can support microbial growth and respiration,
promotes the contraction of the support and the consequent medium
cracking reducing retention times (Swanson and Loehr, 1997). On the
other hand, excessive moisture reduces mass transfer rates of hydro-
phobic substances, reduces biofilm surface area by clogging available
pore space, increases pressure drop (Ferdowsi et al., 2017; van Lith
et al., 1997) and creates anaerobic zones that promote odor formation
and low degradation rates (Ferdowsi et al., 2017; Swanson and Loehr,
1997).
The moisture content of the biofilter support, both for fungal and
bacterial biofilters, is one of the main parameters affecting reactor
performance. The control of the moisture content requires under-
standing the dynamics of drying of the biologically active support due
to the air temperature changes at the inlet, the air relative humidity,
and the metabolic heat produced by the oxidation of VOCs. Morales
et al. (2003) developed a mathematical model to study the drying effect
on a biofilter inoculated with five different types of bacteria and two
types of yeast used for the elimination of toluene. The model considers
the effect of temperature, water content, and contaminant concentra-
tion in the biological reaction. The latter model allows the prediction of
the biofilter performance and water evaporation from the support
media because of the metabolic heat generation and the variation of the
inlet air current relative humidity. The water vapor in the gaseous
phase (air absolute humidity) can be estimated from Eq. (22):
A. Vergara-Fernández et al.
∂XH F ∂XH −RV ρC
= +
∂t ρa ηg ∂Z ηg (22)
where XH is the absolute humidity of air, F is the air mass flow, ηg is the
ratio of gas-phase volume to elementary representative volume, ρa is the
real density of air, ρc is the apparent density of the packing material,
and RV is the water evaporation rate based on dry support.
When analyzing the energy balance in the biofilter, the convective
heat must be considered due to its importance in: the biofilter drying,
the water evaporation and the reaction heat, as stated in Eq. (23):
∂T
β = Qconv + Qevap − Qrx
∂t (23)
where, β is a parameter associated to the accumulation of heat and it
represents the average heat capacity of the medium, Qconv represents
the convective volumetric heat, Qevap is the evaporative volumetric
heat, and Qrx depicts the volumetric heat associated to VOCs degrada-
tion and T is the operation temperature. The combustion heat from the
reaction can be estimated from each VOCs combustion enthalpy. The
CO2 production rate because of the VOC mineralization can be used as a
correction factor of the combustion enthalpy.
Water content can affect also other important aspects of fungal
biofilters such as spore production, emission and retention. The effect of
biofilter water content on spores generation was studied by Vergara-
Fernández et al. (2012b) and Saucedo-Lucero et al. (2014) operating
fungal biofilters for the elimination of n-pentane and n-hexane, re-
spectively. The number of colony forming units (CFU m−3 air ) in the PDA
Petri dish according to Eq. (24), was used for the determination of the
spore concentration (SC):
CFU
SC =
Q·tm (24)
Where, tm is the elapsed time for spore collection and Q the filtered gas
flow rate.
The results show that a low water content in the biofilter promote
sporulation, while a higher water content decreases sporulation and
favors spore retention. Vergara-Fernandez et al. (2012), concluded that
the periodic addition of mineral medium in biofilters based on in-
organic materials promotes rapid recovery of the biodegradation per-
formance and reduces spore emission. However, an excess of irrigation
can increase the pressure drop across the biofilter bed and hinder hy-
drophobic VOCs transfer from the gas phase, with a subsequent de-
crease in EC. Interestingly, the increase in VOCs inlet load in a non-N-
limited scenario triggered spore emission and increased the EC, with
average spore counts of 1.8 ×104 CFU m−3 −3
air and ECmax of 110 g mreactor
−1
h . Finally, lower empty bed residence times (EBRTs) can support an
increase in the emission of spores and a deterioration in the EC. Similar
results, between 2.4×103 to 9.0×104 CFU m−3, were reported by
Saucedo-Lucero et al. (2014) in the hexane abatement in a fungal
biofilter inoculated with a fungal consortium, obtaining a EC of
35 g m−3 h−1.
2.4. Biomass growth and biodegradation kinetics
Though the main problem in biofilters relates to the description of
the mass and momentum transfer phenomena between the gas, the li-
quid and the biofilm; the knowledge of the intrinsic microbial growth
and biodegradation rates is a key issue in the design and optimization of
this type of bioreactors. Coupling both phenomena can be done con-
sidering a micro approximation in order to determine the intrinsic
biodegradation kinetics (Iranmanesh et al., 2015).
2.4.1. Fungal biofilm
Fungal biofilm modeling in biofilters has been scarcely studied. In
general it is considered as a flat biofilm with constant thickness
(Fig. 2b), within the range of several μm to > 100 μm (Dorado et al.,
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Biotechnology Advances 36 (2018) 1079–1093
2008; Spigno and De Marco Faveri, 2005). In contrast, studies carried
out by Vergara-Fernández et al. (2016, 2008) show that the aerial
growth of filamentous fungi plays an important role in the VOCs bio-
degradation. This is mostly due to the increase of transport area, which
can reach values up to 107 m2 m−3, in comparison to 102 m2 m−3 for
non-aerial biofilm (Arriaga and Revah, 2009).
Vergara-Fernández et al. (2016) developed a simple mathematical
model with the objective of describing the contribution of aerial and
non-aerial biodegradation of n-pentane using Fusarium solani. They
found that, although the aerial mycelium represents only 23% of the
biomass on a dry weight basis, is responsible for 71.6% of n-pentane
degradation. This result highlights the key role of the aerial hyphae on
hydrophobic VOCs degradation. In this study, together with mass bal-
ances in the gas phase and the bioreactor biofilm, the mass transfer
surface area (av) was determined, according to Eq. (25), where the
biofilm area (aa) can be determined as reported by Arriaga and Revah
(2009), considering a total hyphal length, Lhyphae (Eq. 25).
a v = am + aa ·α (25)
where, α denotes the fraction of the aerial biomass. Hence, the super-
ficial area available for VOCs transfer can be defined as:
Vbiomass
Lhyphae =
dh yphae 2
π ( 2 ) (26)
where, Lhyphae is the hyphae length, Vbiomass is the biomass volume and
dhyphae is the hyphae diameter.
The total fungal interfacial area per reactor volume, aa, is:
dhyphae Lhyphae π
aa =
Vr (27)
where, Vr is the reactor volume.
A similar approach was applied by Spigno and De Marco Faveri
(2005), to establish the amount of aerial biofilm in the mass balance of
the gaseous phase of a fungal biofilter. This was carried by sensibility
analysis of the variation of the contaminants concentration throughout
the biofilter for values of α between 0.25 and 1.0.
The specific transport area obtained from several simulations reach
values around 2×105 m2 m−3, considering hyphae diameters between
2.1 μm and 2.9 μm (Arriaga and Revah, 2005; Vergara-Fernández et al.,
2008). These values are between 50 and 130 times larger than those
obtained for bacterial biofilters (Iliuta and Larachi, 2004; Zhu et al.,
2004).
2.4.2. Kinetics
Biofilter performance is ultimately determined by the catabolic ac-
tivity of the microbial biomass which, in turn, depends both on the
microbial mass present and the intrinsic activity of this biomass. The
amount of biomass results from growth and decay rates and the in-
trinsic activity on the identity of the microbial population (genotype),
how it is expressed (phenotype) and the reactor conditions (pH, tem-
perature, water content, presence of inhibitors, etc.). Substrate uptake
is utilized for biomass growth when conditions are appropriate using
the chemical energy generated by the catabolic reactions and producing
CO2.
Modeling fungi growth decay has received less interest due to the
complex processes involved in the growth of filamentous fungi. The
nature in which fungi grow, makes it troublesome to define cellular
death when compared to unicellular organisms. Szewczyk and Myszka
(1994) applied an Arrhenius type of equation to represent specific
growth rate as a function of temperature, where there is a term de-
scribing growth and another describing cellular death. Smits et al.
(1999) did not develop an explicit model for cellular death, yet they
proposed an equation describing specific respiration activity of the
microbial mass decay over time.
In the other hand, hyphae elongation of the first hyphae, during the
A. Vergara-Fernández et al.
germination of one spore, has been represented by many authors as
Monod type kinetics (Aynsley et al., 1990; Carlsen et al., 2000;
Larralde-Corona et al., 1997). This representation has been applied to
determine time and branching frequency. Vergara-Fernandez et al.
(Vergara-Fernandez et al., 2011), considered the principles proposed in
the Larralde-Corona et al. (1997) and López-Isunza et al. (1997)
models, to develop an individual hyphae growth model taking into
account the primary hypha and same diameter branching, with a cy-
lindrical shape and constant density. The total biomass and the total
hyphae length were determined with the initially added spores, con-
sidering that each spore germinates forming a sole primary hypha with
many branches.
As important as knowing the rate of biomass growth, is to establish
biodegradation rate of the contaminants involved in the biofiltration.
This is because the kinetic study of the degradation of the contaminants
is contemplated as one of the main steps in the characterization of the
biofilter operation. It is important to consider that normally VOCs
biodegradation studies for biofiltration are carried out as batch culture
(microcosms), where the adsorption phenomena in the support, the
pore diffusion and the gas dispersion can be considered negligible
(Delhoménie et al., 2008; Iranmanesh et al., 2015; Vergara-Fernández
et al., 2006). The expression used for fungal microcosms with gaseous
substrate for the determination of the relation between the COV con-
sumption rate and the specific growth rate is shown in Eq. (28):
dCG 1 dX
=− + mX
dt YX / S dt (28)
where, CG is the limiting contaminant concentration, t is time, Yx/s is
the yield coefficient and m is the maintenance coefficient, and X is the
fungal biomass. Vergara-Fernandez et al. (2011b) apply the same re-
lation to determining the biodegradation of n-pentane, howbeit ig-
noring the maintenance coefficient. The maintenance coefficient can be
expressed as:
[dCG / dt ]m
m=
X (29)
Vergara-Fernández et al. (2006) established that, under the micro-
cosms conditions, in the n-hexane fungal biodegradation, the main-
tenance was approximately 2% of the total removal. This confirms the
importance of the presence of nutrients in biofilters to sustain high
uptake rates.
The kinetic equations employed in biofiltration studies are nu-
merous. From these the most commonly used for the elimination of
hydrophobic VOCs in fungal biofiltration systems are Haldane type
models of inhibition by substrate, and the Monod type models.
Furthermore, a series of other expressions have been used to model the
kinetics of biodegradation in fungal biofilters, which are summarized in
Table 1.
Kinetic studies for the biodegradation of gaseous compounds in
biofiltration systems can be investigated from micro-kinetics (as shown
above) or macro-kinetics. Nonetheless, the micro-kinetics methodology
cannot be extended, in some cases, to systems in gaseous phase (Zamir
et al., 2011a, 2011b). The latter happens because the biodegradation
and the transport phenomena involved in a liquid media system are not
comparable to those in solid media with biofilm. The macro-kinetic
method, for the determination of different kinetic parameters in fungal
biofilters, has been applied by numerous authors (Mathur et al., 2006;
Spigno and De Marco Faveri, 2005; Zamir et al., 2011a, 2011b). The
different kinetic constants are found solving and linearizing the equa-
tion of change of concentration in the gaseous phase in the biofilter and
the applied kinetic model. For example, for the case of Monod type
kinetics Eq. (30) is obtained (Spigno and De Marco Faveri, 2005; Zamir
et al., 2011a, 2011b).
V /Q KS/X 1 1
= +
Cgi − Cg 0 rmax CLn rmax (30)
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Biotechnology Advances 36 (2018) 1079–1093
where, V is the reactor volume; Q is the gas flow; Cgi and Cgo are the
inlet and outlet contaminant concentration, respectively; KS/X corre-
sponds to the saturation constant, rmax is the maximum rate of biode-
gradation and CLn is the concentration of a contaminant in the liquid.
In the phenomenological model simulation of a fungal biofilter done
by Vergara-Fernández et al. (2008), it was found that there is a certain
degree of energetic decoupling throughout the start-up period. This
situation was verified by Vergara-Fernandez et al. (2014) in a following
study. In the literature is possible to find several mathematical models
applied to biofiltration systems inoculated with bacteria and fila-
mentous fungi, which have used the yield parameter as a constant
(Arriaga and Revah, 2009; Dorado et al., 2008; Spigno and De Marco
Faveri, 2005; Vergara-Fernández et al., 2008). The latter occurs be-
cause the models applied only consider the yield parameter as con-
sumption of substrate (VOCs) for the biomass growth, and therefore
neglecting cellular maintenance, product formation, and heat loss,
among others. Nevertheless, the presence of filamentous fungi increases
the solubility of hydrophobic VOCs, being able to generate a substrate
excess with respect to the present nutrients, causing decoupling be-
tween anabolism and catabolism leading to energy spilling. Vergara-
Fernandez et al. (2014) suggested a model that allows to establish the
effect of the ratio of initial substrate concentration to biomass in the
yield and the energetic decoupling coefficient (Eqs. 31 and 32).
1 1 1 Cbi0/ X0
= +
Yobs (Yobs )max (YW )min Cbi0
X0
+ KS/X (31)
(Yobs )max − Yobs
Eu =
(Yobs )max (32)
where Yobs is the observed cell yield, (Yobs)max denotes the observed
growth yield of substrate-limited culture, (YW)min is the minimum en-
ergy spilling-related cell yield, KS/X corresponds to the saturation con-
stant, C i b0 depicts the initial VOCs concentration in wet biomass, ×0 is
initial biomass concentration, and Eu is the energy uncoupling coeffi-
cient.
Results show that Yobs in the gaseous phase is inversely proportional
to the C i b0/ X0 ratio, and that over 60% of VOCs was consumed due to
the loss of energy, and a strong dissociation of catabolism and anabo-
lism takes place for high C i b0/ X0 ratios.
2.4.2.1. Temperature effect in the fungal biodegradation kinetics. As
aforementioned, temperature effect in fungal growth is one of the
main environmental outcomes considered in fungal biofiltration,
however it is rarely considered in models due to its complexity.
Different heat and mass transfer models acknowledge this effect over
the increment of the partition coefficient (lower solubility) and bed
drying (Salehahmadi et al., 2012). On the other hand, some models
have incorporated the effect of temperature in the kinetics of
contaminants biodegradation, as reported by Jin et al. (2007) and
Salehahmadi et al. (2012), assuming an Arrhenius type equation and an
optimal biodegradation temperature, where an increment in
temperatures below the optimal temperature increases the
biodegradation while decreasing the reaction rate (Eq. 33).
Ea
r (T ) = r (Topt ) exp ⎡ (T − Topt ) ⎤
⎢ RTTopt ⎥
⎣ ⎦ (33)
where, r(T) is the biological reaction rate, T denotes operation
temperature, Topt represents the optimal temperature, R depicts the
ideal gas constant and Ea represents the activation energy of biological
reaction.
The ratio Ea/(RTTopt) in Eq. (33) can be assumed as constant for the
operation range in biological processes (Jin et al., 2007). These authors
observed, during the biofiltration of α-pinene in a fungal bioreactor, an
increased in removal efficiency when the operating temperature was
increased from 20 to 30 °C, from 60% to 100% respectively, for an inlet
A. Vergara-Fernández et al. Biotechnology Advances 36 (2018) 1079–1093

Table 1
Kinematic models used in VOCs biodegradation of fungal biofilters.

Type Model Contaminant Type of fungi Reference

Haldane μ = μmax
S n-hexane Fusarium solani (Vergara-Fernández et al., 2006)
S2
S + KS +
KI
Monod μ = μmax
S Toluene n-pentane Bacterial/fungal consortium Fusarium solani (Dorado et al., 2008)
S + KS
(Vergara-Fernández et al., 2016)
Monod-Haldane n-hexane; nitrogen source Fusarium solani (Vergara-Fernández et al., 2008)
⎡ ⎤
μ = μmax ⎢
S ⎥ ⎡ SN ⎤
⎢ S2 ⎥ ⎣ SN + KN ⎦
⎢ S + K S +
⎣ KI ⎥
⎦
Webb μ = μmax
S (1 + S / K ) n-hexane Fungal consortium (Iranmanesh et al., 2015)
S2
S + KS +
KI
Yano μ = μmax
S n-hexane Fungal consortium (Iranmanesh et al., 2015)
S2
S + KS +
KI (1 + S / K )
Teissier n-hexane Fungal consortium (Iranmanesh et al., 2015)

μ = μmax ⎡exp
⎣
( ) − exp ( ) ⎤⎦
−
S
KI
−
S
KS

Aiba S n-hexane Fungal consortium (Iranmanesh et al., 2015)

S ⎛⎜exp ⎛− ⎞ ⎞⎟
⎜ ⎟

⎝ ⎝ KI ⎠ ⎠
μ = μmax
S + KS
Andrews μ = μmax
S n-hexane Aspergillus niger (Spigno and De Marco Faveri, 2005)
S⎞
(S + K S ) ⎛1 +
⎜ ⎟

⎝ KI ⎠
Exponential μ = μmax
S n-hexane Fungal consortium (Iranmanesh et al., 2015)
S
(S + K S ) exp ⎜⎛− ⎟⎞
⎝ KI ⎠

concentration of 150 ppm. However, an opposite trend was observed at
temperatures between 30 and 40 °C. A similar effect was observed by
Vergara-Fernández et al. (2012b) in the biofiltration of n-pentane with
the fungus Fusarium solani, obtaining an increase in the ECmax from 45
to 65 g m−3 h−1 when the temperature increased from 15 °C to 25 °C,
however a decrease to 60 g m−3 h−1 was obtained when the tempera-
ture was increased to 35 °C.
(2008) found that the toluene elimination capacity in a biofilter in-
oculated with species of Pseudomonas decreases as the inlet load of
hydrogen sulfide increases. On the other hand, Woertz et al. (2001)
found that toluene was consumed as a source of carbon and reducing
power in a fungal biofilter for the oxidation of nitric oxide, with a
maximum removal efficiency of 93%.

3. Modeling of VOCs elimination in fungal biofilters

2.4.2.2. Biodegradation kinetics of a mixture of contaminants. The
presence of more than a sole contaminant in different emission
sources is common, hence the study of fungal biofiltration under the
aforementioned condition is mandatory. Iranmanesh et al. (2015)
studied the effect of the presence of toluene in the biodegradation of
n-hexane using an undefined fungi consortium. The results were fitted
into a Haldane equation for biodegradation of both substrates (Eq. 34).
μmax ,1 CG,1
μ= +
CG2 ,1
KX / S,1 + CG,1 + KI ,1
+ I2,1 CG,2 KX / S,2 + CG,2 +
where μ is the specific rate of growth, μmax is the specific rate of
maximum growth, CG is the contaminant concentration, KX/S is the
constant of affinity contaminant, KI is the inhibition constant and Ii,j
indicates the degree of interaction of substrate i affecting the
biodegradation of substrate j (high values indicate higher degree of
inhibition). On the other hand, Vergara-Fernández et al. (2008) used a
coupled kinetic model of Haldane for the contaminant and a Monod
model for the use of nutrients (nitrogen source) (Eq. 35), to establish
the rate of growth of the filamentous fungus Fusarium solani in the n-
hexane biofiltration.
CG ⎤ ⎡ CN
μ = μmax ⎡ ⎤
⎢ Cg + KX / S + C 2/ KI ⎥ ⎢ CN + KN ⎥
⎣ G ⎦⎣ ⎦ (35)
where, CN is the nutrient concentration and KN is the nutrient affinity
constant.
Finally, the kinetics of microbial growth and pollutants metaboli-
zation can be influenced by inorganic gases, such as ammonia, hy-
drogen sulfide or nitrogen oxides, with effects over VOCs degradation
ranging from beneficial to detrimental. For example, Galera et al.
The following paragraphs illustrate the evolution in the models
describing fungal biofilters, explicitly stating the physicochemical and
biological phenomena considering in the models. Fig. 4 displays this
information in a graphical fashion. Among the first models for fixed bed
biofilters, Ottengraf and Van Den Oever (1983) considered steady-state
operation, axial plug flow, diffusion of the pollutant in the biofilm and
μmax ,2 CG,2 zero or first-order kinetics. Shareefdeen and Baltzis (1994) developed
CG2 ,2 an unsteady-state model of a biofilter treating toluene vapors in air
KI ,2
+ I1,2 CG,1
considering mass balances in the bacterial biofilm, gas phase and solid
(34) support. The reactions performed by the bacteria in the biofilm were
mathematically described using Monod kinetics.
Deshusses et al. (1995) later proposed a model for the degradation
of methyl ethyl ketone (MEK) and methyl isobutyl ketone (MIBK) in a
biofilter. The microbial kinetics consider a Monod-type expression in-
corporating competitive inhibition towards the MEK and MIBK mixture.
A different approach was adopted by Hodge and Devinny (1995), who
propose a model describing transfer between the air and the biotic
solids/water phases, biological substrate degradation, CO2 production
and accumulation and pH changes resulting from CO2 accumulation. A
mathematical model describing the biofiltration of a mixture of hy-
drophilic and hydrophobic compounds was developed by Mohseni and
Allen (2000). Based on the work of Ottengraf and Van Den Oever
(1983) for a single COV, the steady-state model considers the biofilm as
an organic matrix and uses Monod kinetics with inhibition.
Although mass transfer and biodegradation kinetics are at the core
of most biofilter models, other aspects of the biofilter operation have
been considered. Morales et al. (2003) included in their model the
drying and loss of activity of the humid solid support (peat) induced by
the metabolic heat generated by the degradation of the gaseous sub-
strate. Iliuta and Larachi (2004) addressed the problem of extensive

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A. Vergara-Fernández et al.
Fig. 4. Summary of models to describe the biofiltration of hydrophobic VOCs using fungi (except for the model of Ottengraf and Van Den Oever, 1983) and their assumptions.
biomass growth and clogging considering a unidirectional dynamic
flow model based on the volume-average mass, momentum and species
balance equations coupled with conventional diffusion/reaction equa-
tions describing apparent kinetics in the biofilm.
Several models have been reported describing fungal biofilter in
contrast to those models described in the previous paragraphs, where
no distinction is made as which are the agents (bacteria, yeast or fungi)
of the biological activity. Spigno et al. (2003) and Spigno and De Marco
Faveri (2005) proposed a model for the elimination of n-hexane by
Aspergillus niger based on a steady-state description considering axial
dispersion in the gas phase. However, the model treats the biofilm using
the same assumptions involved in microbial consortiums or bacterial
biofilters modeling, considering a homogeneous and constant fungal
biofilm where the reactions take place in the so called “effective bio-
layer”, where the pollutants diffuse. Both models were developed using
a steady state assumption.
An improvement including actual partition coefficient in the fungi,
biofilm thickness, superficial area and effective diffusivity was pre-
sented by Arriaga and Revah (2009). The model is based on the work by
Ottengraf and Van Den Oever (1983) modified by considering that a
fraction of the biomass is active in degrading the substrate, a fraction
controlled by the diffusion rate within the biofilm. Another modifica-
tion from the original model is that zero-order kinetic was assumed.
Dorado et al. (2008) developed a dynamic model describing the
elimination of toluene in a bacterial-fungal biofilter, the model was
calibrated and validated against experimental data. The model is based
on mass balances, including convection, absorption, diffusion and
biodegradation. The biofilter was initially inoculated with a bacterial
consortium, and after 60 days of operation, the biofilter was colonized
by fungi as confirmed by a change in the reactor pH and microscopy.
In general, previous models were developed assuming the biofilm as
a pseudo-homogeneous phase. However, in the case of aerial biofilms,
such as those generated by the hyphae of filamentous fungi, those
pseudo-homogeneous phase models do not provide all the information
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Biotechnology Advances 36 (2018) 1079–1093
of intra and inter-particle phenomena occurring in the biofilter. As the
aerial growth in filamentous microorganisms develops, it occupies the
empty void between the solid support particles in the biofilter.
Filamentous growth in fungal biofilters favors the transport from the
gas to the biotic phase by both the increase in the exchange surface, due
to hyphal growth, and by increased solubility of the hydrophobic VOCs
due to the hydrophobic nature of the fungal surface (Vergara-Fernández
et al., 2006).
The diffusive transport of the contaminant across the biofilm cannot
be analyzed using a model based in an aerial biofilm. In such model,
there is no homogeneous film where diffusion can occur, thereby it is
assumed that the contaminant is in direct contact with the hypha of the
filamentous fungi (Vergara-Fernandez et al., 2012).
Vergara-Fernández et al. (2008) developed a mathematical model
considering the physical and biological phenomena in a fungal biofilter.
The biofilter is mathematically described and the main physical, kinetic
data and morphological parameters of aerial hyphae were obtained by
independent experiments for model verification. The model proposed
describes the increase in the transport area by the growth of the fila-
mentous cylindrical mycelia and its relation with n-hexane elimination
in quasi-stationary state in a biofilter. In order to mathematically de-
scribe the system, four processes were considered: (1) mass transfer of
VOCs in the bulk gas, (2) mass transfer of VOCs into the gas layer
around the mycelium considering the experimentally obtained gas-
biomass partition coefficient, (3) mass transfer and uptake of the ni-
trogen source through the elongating mycelia, (4) and the kinetic of
mycelial growth. The model describing fungal growth includes Monod-
Haldane kinetic and hyphal elongation and ramification. A maximum
EC of 250 g m−3 h−1 was predicted in simulations and experimentally
validated.
Recently, Vergara-Fernández et al. (2016) developed a mathema-
tical model predicting the influence of the fraction of aerial biomass
and its partition coefficient on the biodegradation of n-pentane by the
filamentous fungi Fusarium solani in a fixed-bed continuous biofilter,
A. Vergara-Fernández et al.
obtaining an EC close to 680 g m−3 h−1.
3.1. Artificial neural networks models in fungal biofilters
As discussed previously, several phenomenological mathematical
models have been developed to describe the performance of fungal
biofilter systems. The evolution of these models has led to cumbersome
sets of non-lineal equations of momentum, heat and mass transfer.
Furthermore, these models require the experimental determination of a
series of parameters, such as kinetic constants, constants of pollutant
diffusion in the biofilm, oxygen consumption and carbon dioxide pro-
duction, heat and mass transfer coefficients, among others. A solution
to the aforementioned set of equations, lays in the use of a non-linear
modeling method that focuses on the simulation and prediction of the
biofilter performance, based exclusively on available data (Zamir et al.,
2011a, 2011b). One of these alternatives, suggested in a recent pub-
lication, is to use artificial neural networks to model biological pro-
cesses. Chairez et al. (2009), proposed a model using continuous neural
networks with the aim to design and predict the behavior and elim-
ination capacity of a fungal biofilter (Paecilomyces variotti) for toluene
abatement, as an alternative to the complexity and simplification as-
sumptions of phenomenological models. This model concludes that the
application of neural networks in this type of problems reduces the cost
of the biofilter performance due to the reduction in the number of re-
quired sensors.
Additionally, Spigno and Tronci (2015) developed a model for the
elimination of hexane in a fungal biofilter inoculated with Aspergillus
niger, based on hybrid models, obtained by the connection of the mass
balance equation with a feedforward neural network, used as a black-
box model of the reaction and transport phenomena. A similar ap-
proach for the development of an experimental model for the analysis
of a compost biofilter treating n-hexane was developed by Zamir et al.
(2011a, 2011b), over a wide range of inlet loads (between 8 and
598 g m−3 h−1). The neural model showed the ability to predict the
performance of biofilter under intermittent operating conditions. The
results suggested that neural network can be considered as a suitable
alternative to conventional knowledge-based models; however, the
sudden changes in the value of removal efficiency have an impact on
the neural networks training/generalization pattern.
3.2. Modeling for design and operational optimization
Optimization of the operation of a biofiltration system requires
knowledge of the rate-limiting steps controlling the efficiency of the
system. Depending on system's setup and operational parameters, bio-
filters can be operated under either mass transfer or kinetically limited
conditions. Several strategies can be used to determine the rate-limiting
step. In biotrickling filters, bioscrubbers and bubble tank reactors a
straightforward strategy is to increase the biomass concentration in the
liquid phase. If a change in the amount of pollutant removed per reactor
volume is achieved when biomass concentration is increased, then the
system is kinetically limited (Kraakman et al., 2011). However, this
procedure is not feasible in a biofilter. Barton et al. (1999) and
Iranmanesh et al. (2015) suggested a technique to distinguish between
kinetically o mass transfer limitation by changing the operating tem-
perature of the system. An important increase in removal efficiency as
temperature increases measured at different gas velocities is indicative
of a kinetically-limited system as mass transfer parameters such as so-
lubility (increasing with temperature), diffusion (increasing with tem-
perature) and Henry's constant (decreasing with temperature) are less
sensitive to temperature compared to biodegradation parameters.
Mathematical modeling of biofilters can be used to ascertain mass
transfer and kinetic limitations. Particularly, sensitivity analysis of di-
mensionless numbers such as the Damköhler number, the ratio of the
reaction rate to the mass transfer rate; the Thiele number, defined as the
ratio of the reaction rate to the diffusion rate, and the Peclet number,
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Biotechnology Advances 36 (2018) 1079–1093
the ratio of the advection to diffusion rates, can be effective in ana-
lyzing the interplay of mass transfer and biodegradation kinetics.
Different authors have used this method to identify whether the op-
eration of the reactor was mass transfer or kinetically limited (Vergara-
Fernández et al., 2008; Xi et al., 2015).
In air biopurifications systems, such as biofilters and biotrickling
filters, the pollutant degrading microorganisms are attached to a
packing media. The packing media can be conformed by different types
of porous materials such as compost, mineral grains and artificial foams
(Kim et al., 2007; Yang et al., 2011; Znad et al., 2007). The con-
taminated air flows through this media which translate into direct
contact of air with the attached biomass (biofilters), or diffusion of the
contaminant in a flowing liquid in which the biomass is immersed
(biotrickling filters). There, the biomass degrades the contaminant
which is converted to innocuous products and more biomass (Moe and
Irvine, 2001). The effectivity of the latter process depends, among
others, on how much of the contaminant is bioavailable for the de-
grading microorganisms (Cheng et al., 2016), either from the bulk gas
to the biofilm, or from the gas phase to liquid phase and from there to
the biofilm.
The porous media accommodates in a biofilter generating void
spaces or pores, as well as porous channels that are irregular in shape
(Devinny and Ramesh, 2005). Porosity and porous channel configura-
tion plays a major role on residence time, pressure drop and pre-
ferential flow, and therefore affecting the overall performance of the
biofilter. And this is only the tip of the iceberg, since the growth of
biofilm over time may generally lead to changes in all previous char-
acteristics (Devinny and Ramesh, 2005). Furthermore, depending on
the pores size, for the case of biotrickling filters, the flow may be
subjected to capillarity effects.
From the previous description, it seems relevant to study in depth
the dynamics of the air flowing through the porous media selected for
the biopurification treatment system, since it might affect the actual
treatment. In other words, how does the selected porous bed will en-
hance pressure drop, boost preferential flow increasing death zones and
therefore reducing bioavailability in the biofilter in average, and finally
decreasing residence time. In this regard, computational fluid dynamic
studies (computational simulations) coupled with a realistic re-
presentation of the media may be of great help. This can be done by
discretizing the porous volume within the biofilter in computational
cells, and solving the flow of air passing through it, by means of the
Navier-Stokes equation, with the corresponding boundary conditions.
Through this type of studies, it might be possible to understand at the
microscale level the complex physical phenomena involved in the in-
teraction between the fluid and the porous structure. Validation can be
achieved by comparison of pressure drop and flow velocity with ex-
perimental studies. Since flow velocities are usually very low, and be-
cause of the practical limitations in measuring flow velocity at the pore,
a residence time distribution (RTD) study can be carried out, and
compared to the RTD simulation results. This is in a way, and indirect
measurement of the velocity distribution in the biofilter. Once vali-
dated, important properties of the porous structure can be assessed,
such as permeability (in the flow and transverse directions), pre-
ferential flow (by defining a threshold velocity), etc. Moreover, for the
case of trickling filters a two-phase (liquid and air) computational si-
mulation may deliver a better understanding of the combination of flow
conditions that enhance contaminant diffusion into the liquid phase.
Taking into account that surface tension might be an important vari-
able, a capillarity force should be added to the Navier-Stokes equations.
Thus, again, a detailed and realistic description of the porous structure
is needed.
As previously mentioned, a highly resolved description of the
porous media is very important to find reliable information at the pore
scale. That can be achieved by digitalizing the actual porous media to
be used in the biofilter. This is possible nowadays by, for example,
computational tomography. Figs. 5 are good examples of the level of
A. Vergara-Fernández et al.
detail that can be obtained for a grain (vermiculite) porous structure
and a synthetic foam (polyurethane), respectively. Once validation is
achieved, different studies of interest can be carried out in order to
better understand several important characteristics and properties of
the effects of the porous media in the final performance of the bior-
eactor.
4. Comparison of fungal and bacterial biofilters and its
performance
In this section, a comparison of experimental results from biofilters
operated with bacteria or fungi treating several VOCs is performed.
Instead of using the rather common approach of revisiting each pub-
lished report and describing the results (for example the recent review
of Cheng et al. (2016)), we adopt a comparative approach as follows.
Four categories of VOCs were distinguished: BTEX (benzene, toluene,
ethylbenzene and xylene) and styrene as slightly hydrophobic VOCs,
with partition coefficients between 1.66 (xylene) to 4.68 (styrene),
hydrophobic VOCs (α-pinene with a partition coefficient of 8.33), al-
kanes as very hydrophobic VOCs (partition coefficients > 40) and
water-soluble VOCs. The literature was surveyed to collect experi-
mental results of reactors treating these VOCs by either bacterial or
fungal biofiltration. When possible, the inlet concentration of the con-
taminant, the EBRT, L and EC were collected at 100% relative efficiency
(also called critical load) and at the maximum recorded EC. These va-
lues were used to construct Fig. 6 A to D, where it can be seen that the
fungal biofilters outperform its bacterial counterpart in the treatment of
hydrophobic VOCs. On the other hand, the data is scarce on the use of
fungal biofilter for the abatement of hydrophilic compounds, and that
the available information shows no distinct advantages for the fungal
based biofilters over bacterial ones.
The high performance of fungal biofilters for the treatment of hy-
drophobic VOCs over bacterial biofilters has been previously reported
in literature for individual compounds (Estévez et al., 2005; Estrada
et al., 2013; Jorio et al., 2009; Kennes and Veiga, 2004; Vergara-
Fernández et al., 2011). However, to the best of our knowledge, Fig. 6
represents the first systematic comparison reported to date comparing
multiple results grouped by contaminant hydrophobicity for bacterial
and fungal biofilters. From its analysis, it can be concluded that bio-
filters where fungi are used as the biocatalyst: (i) attained high elim-
ination capacities for hydrophobic compounds compared to its bacterial
counterparts at higher inlet loads, keeping a high relative efficiency
(panels A to C in Fig. 6), (ii) can be operated at higher inlet
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Biotechnology Advances 36 (2018) 1079–1093
Fig. 5. Left: Clipped computational tomography image of a
biofilter column with vermiculite as porous media. The
vermiculite has an average diameter above 4 mm. The
column is comprised by a PVC pipe with flanges at the top
and bottom. The porous media is supported at the bottom
by a fixed plastic screen. The pipe has an internal diameter
of 7.5 cm, the pipe with flanges has 30 cm in height. Right:
Computational tomography image of 16 by 16 by 8 mm in
length, height and depth, respectively, of a polyurethane
foam.
concentration of the contaminant and, (iii) for hydrophilic pollutants in
the gas phase (panel D in Fig. 6), its performance is inferior to bacterial
biofilters.
As discussed in Section 3, these observations have been accounted
for, in both the conceptual and mathematical modeling of fungal bio-
filters, through the use of partition coefficients of the contaminant in
the biomass, which can be considered as an attempt to capture the
surface properties of the aerial hyphae (such as the presence of hy-
drophobins), and by including descriptions of the increased surface area
available for the transport of contaminants to the fungal biomass.
Finally, applications of fungal biofiltration under development are
represented by the abatement of extremely low solubility contaminants,
such as methane (Lebrero et al., 2016), and large and complex mole-
cules such as polycyclic aromatic hydrocarbons (Vergara-Fernández
et al., 2018).
5. Conclusion
Biological technologies for the abatement of pollutants in diluted air
streams offer economic advantages over physicochemical methods as
shown by the industrial application of bacterial biofiltration in the last
decades. However, when the organic pollutants to be treated are hy-
drophobic, the performance, in terms of elimination capacity and inlet
load, of bacterial biofilters is typically lower than the ones attained in
fungal biofilters.
As many factors, including the mass transfer of VOCs, the microbial
kinetics, the structure of the packing media and the fluid flow in the
reactor, can have an impact on the performance of a biofilter, mathe-
matical models are often developed to disentangle the effects of each
variable in the overall performance of the biofilter. For fungal reactors,
models have evolved from those in which the same considerations as in
bacterial biofiltration were used, to models specially designed to ac-
count for traits, such as the development of hyphae, that are unique to
fungi.
Further research is still needed for the optimization of the packing
to improve the flow of the gas within the biofilter, minimizing death
zones and short-circuiting, thus reducing the size of a biofilter for a
given task. This can be accomplished by a combination of highly re-
solved descriptions of the porous media with computational fluid dy-
namics. Coupling such models with mathematical descriptions of the
biodegradation kinetics and mass transfer could provide new insights in
fungal biofilters optimization using conventional packing (vermiculite
and perlite), but could also open the possibility of designing new
A. Vergara-Fernández et al. Biotechnology Advances 36 (2018) 1079–1093

Fig. 6. Elimination capacity and load for fungal (circle) and bacterial (square symbols) biofilters. Panel A: biofilters treating benzene (B), toluene (T), styrene (S) and xylene (X). Panel B:
biofilters treating α-pinene. Panel C: biofilters treating n-pentane (C5), n-hexane (C6) and n-heptane (C7). Panel D: biofilters treating methanol (M), ethanol (EtOH), formaldehyde (F) and
methyl-propyl-ketone (MPK). Colored symbols indicate the inlet contaminant concentration according to the color bar at the bar at the right hand side of each plot, while the size of the
marker is proportional to the EBRT. A complete list of the references and data used to generate this figure is presented as supplementary material.

structured and unstructured packing. 18, 87–92. http://dx.doi.org/10.1002/ep.670180212.

Acknowledgments
The present work has been sponsored by CONICYT – Chile (National
Commission for Scientific and Technological Research) (Fondecyt
1160220).
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.biotechadv.2018.03.008.
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