A. Vergara-Fernández et al.
Biotechnology Advances 36 (2018) 1079–1093
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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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,