Analysis of Unstructured Kinetic Modeling for a SulfateReducing Process Using Desulfobivrio alaskensis 6SR

Juan C. Figueroaa, Ricardo Aguilarb, and M. Isabel Neriaa*

a

Divisin de Ingeniera Qumica y Bioqumica, Tecnolgico de Estudios

Superiores de Ecatepec.Av. Tecnolgico S/N. CP 55120, Ecatepec, Edo. de

Mxico. Mxico.bDepartamento de Biotecnologa y Bioingeniera, CINVESTAVIPN. Av., San Pedro Zacatenco, Mexico City, Mexico, 07360.
*E-mail: ibineria@hotmail.com

RESUMEN
En este artculo se presenta un anlisis cintico de un proceso sulfato reductor
tomando como caso de estudio a la cepa Desulfovibrio alaskensis 6SR. Este anlisis
consider cinco modelos cinticos no estructurados de tipo inhibicin por producto,
adems se propone una expresin de ley de potencias para la produccin del
exopolisacrido (EPS) que se genera durante la fase de mxima produccin de sulfuro
de hidrgeno y conlleva a una condicin de estrs. Cada modelo consider las
variables de estado de consumo de sulfato y lactato, produccin de sulfuro de
hidrgeno, acetato y biomasa. Los modelos considerados fueron validados por
comparacin con los datos experimentales generados obtenindose coeficientes de
correlacin satisfactorios. El resultado de las simulaciones sugiri que el modelo de
Levenspiel es la mejor representacin matemtica del crecimiento bacteriano y del
proceso sulfato reductor al combinarse con el modelo de la ley de potencias para el
EPS. Los parmetros cinticos obtenidos fueron una max = 0.36 1/h, KS = 6559 mg/l,
P* = 610 mg/l y n = 0.89, con un ndice de correlacin de R2= 0.96. El anlisis cintico
del proceso sulfato reductor permite dar una mayor aproximacin de este tipo de
crecimiento anaerobio para explorar su comportamiento bajodiferentes condiciones de
operacin segn el inters biotecnolgico deseado.
Palabras clave: Sulfato reduccin, modelos no estructurados, inhibicin, cintica.

ABSTRACT
This paper presents a kinetic analysis of sulfate reducing process considering as a
case study Desulfovibrio alaskensis 6SR. Five unstructured kinetic models with product

BioTecnologa, Ao 2013, Vol. 17 No. 2

11

inhibition were considered, and a power law kinetic expression to exo-polysaccharide

(EPS) production was proposed. The EPS is generated when maximum production of
sulfide takes place, which provokes a stress condition. All models presented
satisfactory overall correlation coefficients and their performance is analyzed
comparing the corresponding numerical simulations with the experimental data. The
results of the simulations for each model suggest that Levenspiels model is the best
one to represent the bacterial growth, sulfate reducing process and the inhibition effect
by sulfide, with the combination of the expression to EPS production. The kinetic
parameters values obtained for this model are max = 0.36 1/h, KS = 6559 mg/l, P* =
610 mg/l and n = 0.89, and correlation coefficient of 0.96. The kinetic analysis of
process sulfate reducing allows major approximation of anaerobic growth to explore the
behavior in different operation conditions for biotechnology purposes.
Keywords: Sulfate reducing, unstructured models, inhibition, kinetic.

INTRODUCTION

(Alvarez et al., 2006; Katsoyiannis &

Sulfate reducing bacteria (SRB)

Zouboulis, 2004; Muyzer & Stams,

form a group of prokaryotes able to

2008). In contrast, the presence of SRB

transform sulfate at sulfide and are

in the oil field contribute to the souring

widespread in anoxic habitats, they

of water flooded oil reservoirs due to

have an important role in both the sulfur

the production of sulfide, also the highly

and carbon cycles (Castro et al., 2000;

reactivity and toxicity of sulfide induces

Wanger et al., 1998). Approximately

pitting metallic corrosion, causing great

half of organic carbon is mineralized by

economic losses in pipeline systems of

SRB

the petroleum industry and others

in

anoxic

ocean

sediments

(Jorgensen, 1982) or in wastewater

treatment systems (Khl, 1992). Some
SRB

can

also

decompose

more

(Videla & Herrera, 2005).

The

SRB

environments

which
under

thrive

in

undesirable

persistent organic pollutants such as

conditions, for example high levels of

polycyclic aromatic hydrocarbons and

toxic elements such as sulfide and

polychlorinated biphenyls (Widdel &

heavy metals, generally adopt special

Rabus,

metabolic

2001).

Due

to

these

pathways

mechanisms

to

environmental

environments (Flemming & Wingender,

problems, e.g. in biological sulfate

2001a, Flemming & Wingender, 2001b;

reduction, the produced sulfide can be

Zhenming & Yan, 2005). Even if the

used to precipitate metallic species

SRB have the highest tolerance to

various

BioTecnologa, Ao 2013, Vol. 17 No. 2

survive

protective

characteristics, the SRB has been used

solve

to

and

in

these

12

sulfide, their development is inhibited

fitting of sulfate reducing kinetic (Neria-

by the presence of high levels of sulfide

Gonzlez et al., 2009), in most cases

(Caffrey & Voordouw, 2009), however

Monod model is used, which does not

they have the capability to produce

takes into account the product inhibition

special bioactive compounds such as

phenomenon

extracellular

substances

accumulation inside bioreactor; much

(EPS) (Flemming & Wingender, 2001a).

less the EPS production present at later

The EPS are produced during both

stage of the reacting paths (Al-Zuhair et

suspended

al., 2008; Robinson & Tiedje; 1983).

protecting

polymeric

and

biofilm

growth

microorganisms

to

from

Beside,

the

generated

by

well-know

sulfide

Monod

predation, toxic agents, desiccation;

expression is only applicable where the

also serving as surface adhesions,

presence of toxic metabolic products is

stabilizing enzymes, storing nutrient,

not important (Luong, 1985).

etc. (Zhenming & Yan, 2005).

Nowadays,

the

sulfate

reducing

From the biotechnological point of

processes have more importance in the

view, the SRB are of great importance

bioremediation field; therefore, a clear

in

industrial

knowledge of the sulfate reducing

processes, for which demand a greater

kinetic and a mathematical model to

knowledge of the kinetic behavior of

describe

sulfate-reducing processes. However,

behavior are needed. In this work the

the determination of kinetic parameters

kinetic of sulfate reducing process,

throughout structured model on basis of

taken at Desulfovibrio alaskensis 6SR

biomass

as:

as strain model, was analyzed. The

concentration of metabolites, enzymes,

specific growth rate of 6SR strain is

DNA, and/or RNA as a complex task

estimated through five unstructured

(Arellano-Plaza et al., 2007; Bailey &

kinetic models: (a) Haldane-Bulton, (b)

Ollis, 1986; Hyohak et al., 2008). For

Haldane-Levespiel, (c) Haldane-Luong,

this reason, the kinetic parameters

(d) Moser-Bulton, and (b) Levenspiel;

more commonly used are estimated

all models includes a product inhibition

through unstructured kinetic model that

(sulfide) term that take in consideration

use

the inhibition effect by sulfur production:

environmental

and

components,

biomass,

measurements,

such

substrate,
well

reacting

Mean while, the estimation of EPS

coefficients determined in the bulk of

production rate by means of power law

the reactor (Arellano-Plaza et al., 2007;

model is carried-out. The goal is to find

Hyohak et al., 2008). Few kinetic

a kinetic model for specific growth rate

models

and the mass balance expressions of

obtained

as

the

yield

have

as

product

satisfactorily

satisfactory

BioTecnologa, Ao 2013, Vol. 17 No. 2

13

the different species (X, S, P, and EPS)

reached at the beginning of stationary

to approximate satisfactorily the kinetic

phase. A 5 ml aliquot was taken from

behavior in a batch bioreactor, in order

Postgates C medium to inoculate 95 ml

to maximize or minimize the production

of

of the desired metabolite (e.g. sulfide or

experiment was done using two series

EPS production).

of triplicate independent cultures; each

fresh

medium at

37

C.

The

set of triplicate cultures were inoculated

with 12 hours separated each other, the
MATERIALS AND METHODS

experimental run time was 72 hours.

Organism, culture maintenance and

One set of independent cultures were

purity test

used to measure EPS production. A

Desulfovibrio alaskensis 6SR was

maintained routinely in Hungate tubes

culture was taken for day and the EPS

was extracted.

with 5 mL of Postgates B solid medium

(Hungate; 1969; Postgate, 1981). The

Analytic Methods

presence of black colonies indicated

The bacterial growing, consuming of

the growth of sulfate reducing bacteria.

sulfate, and sulfide production were

One black colony well defined and

monitored 3 or 4 hours each, the

isolated

quickly

samples were taken carefully, avoiding

transferred at 45 mL sterile Postgates

contact with oxygen. The bacterial

C liquid medium in anaerobic conditions

growing was followed through Optical

(Postgate, 1981), and subsequently a

Density (OD) methodology, the OD

subcultures were made. The media

data were transformed into dry mass

were inoculated with 5 ml of culture and

(mg/ml) through a dry mass versus OD

incubated at 37 C. Each medium was

standard curve. The consuming of

prepared and dispended in anaerobic

sulfate in the medium was measured by

conditions under a N2 (99.998% purity)

the turbid metric method based on

atmosphere, 120 and 160 ml serum

barium precipitation (Kolmert et al.,

bottles were filled with 45 and 95 mL of

2000). Also the production of sulfide

medium, respectively, and autoclaved

was measured by a colorimetric method

at 121 C.

(Cord-Ruwisch, 1985). Each measuring

was

picked

and

was done using a Thermo SCIENTIFIC

Conditions of culture
The inoculum for kinetic study was

GENESYS

10uv

Scaning

Spectrophotometer.

cultured in 45 ml of Postgates C

The EPS was extracted by heat

medium at 37 C for 30 h until culture

treatment and filtration. The bacterial

BioTecnologa, Ao 2013, Vol. 17 No. 2

14

culture bottles were opened and placed

in water bath at 50 C for 15 minutes,
each sample was vortexed once or

Data Analysis and mathematical model

The biomass, sulfate, sulfide, and

twice, then the cellar suspension was

EPS

passed through a nylon membrane

experimental data were averaged, in

0.45m, the filtrate was collected in 250

order

ml centrifuge bottleand EPS was then

behavior of each variable, see figure 1.

precipitated from it, adding an equal

The

volume of cold ethanol overnight at -20

Desulfovibrio

C, followed by centrifugation at 2500

evaluated

g for 10 min at 4 C (Hettich Zentrifugen

unstructured kinetic models (Haldane,

UNIVERSAL 320R). The pelleted EPS

1930;

wastransferred at micro-centrifuge tube

Levenspiel, 1980; Luong, 1985; Moser

and washed in 70% (v/v) ice-cold

1958). In table 1 are shown the different

ethanol.

product inhibition models (for high

EPS

was

dried

in

oven

(ECOSHEL DOV23A) at 70 C for 24 h

concentrations

to

smooth

specific

Han

the

growth
alaskensis

with

&

of

each

experimental

rate
6SR

five

of
was

different

Levenspiel,

1988;

sulfide concentrations).

and before dry weight was recorded.

Suldife

BioTecnologa, Ao 2013, Vol. 17 No. 2

15

Fig. 1. Out line of sulfate reduction process for Desulfovibrio alaskensis 6SR.

Table 1.Unstructured kinetic models considered in this work.

Kinetic model

Equation

Haldane-Boulton

(1)

Haldane-Levenspiel

(2)

Haldane-Luong

(3)

Moser-Bulton

(4)

Levenspiel

(5)

max
P
][
]
2
S + + ( / ) P +

Haldane, 1965;

max

]
[1
]

S + + ( 2 / )
P

Haldane, 1965;

max

] [1 ( ) ]
2
S + + ( / )
P

Haldane, 1965;

=[

=[

=[

=[

The rate of change of experimental

biomass production for the parametric

Boulton, 1980.

Levenspiel, 1980

max
P
][
]

S + P +

= max [1

Estimations of kinetic parameters

References

Moser, 1958;
Boulton, 1980.

] [
]

S +

optimization
forward

Levenspiel, 1980.

was

finite

Luong, 1985.

calculated

differences

i+1

scheme

according to the following equation:

( ) ( ) = ( i+1 i )

ti

using

(1)

The kinetic parameter estimations of

the five unstructured kinetic models for

used to estimate the production rate of

EPS and the dead rate.

specific growth rate were obtained by

using

nonlinear

regressions

through

multivariable
of

Model evaluation

Levenberg-

According to the mass balances for

Marquardt algorithm (POLYMATH 6.0

biomass,

Professional

software)

employing

product (sulfide), dead biomass and

experimental

data

biomass,

EPS concentrations, the following set or

of

substrate

ordinary

The model predictions were comparing

proposed to

with

through

reducing process, in accordance with

minimizing the error sum of least

the reaction scheme showed in Figure

squares. The same methodology was

1.

data

BioTecnologa, Ao 2013, Vol. 17 No. 2

equations

and

substrate, and product concentrations.

experimental

differential

(sulfate)

modeling the

is

sulfate-

16

Biomass (X):

= X

(2)

Substrate (S):

= (S/X )(X )

(3)

Product (P):

= (P/X )(X )

(4)

= E d

(5)

Dead rate (Xd):

d

= d

(6)

The specific growth rate models for

substrate-biomass (YS/X) and product-

rx, considered in this work are Haldane-

biomass (YP/X) were calculated with the

Bulton, Haldane-Levenspiel, Haldane-

experimental data corresponding to

Luong, Moser-Bulton, and Levenspiel

exponential phase, using expressions

models.

(7) and (8).

The

yield

coefficients

by

S/X = 0i
i

(7)

P/X = i0
i

To
models,

(8)

validate

the

experimental

mathematical
data

were

specific growth parameter values (see

Table 2) of the five unstructured kinetic

collected from two set batch cultures

models.

The

with the following initial concentrations:

(library

ODE45

biomass (X = 117 mg/l), substrate

employed to solve the system given by

(SO42- =5000 mg/l) and sulfide (34

equations (2-6). The performance of

mg/l). The values calculated of yields

each model was evaluated by means of

are YS/X = 14.13 and YP/X =2.14. The

the

simulation of the kinetic behavior was

coefficient

obtained

regression between the experimental

integrating

the

set

of

Runge-Kutta

method

MATLABTM)

corresponding
calculated

was

correlation
by

linear

differential equations (2-6) using the

BioTecnologa, Ao 2013, Vol. 17 No. 2

17

and predicted data for the biomass,

substrate, and products concentrations.

Table 2. Kinetic parameters estimated for Desulfovibrio alaskensis 6SR and EPS.
max

ks

ki

kp

P*

KE

39.84

86070.00

9850.19

7.24

---

---

---

---

---

0.39

2227.03

2298.68

554.19

---

---

---

Haldane-Luong

7.00

2227.00

565.53

557.12

---

---

---

---

---

Moser-Bulton

10.55

1.26 E+9

---

2.70

---

2.53

2.53

---

---

Levenspiel

0.36

6550.00

---

---

610.00

0.89

0.89

---

---

---

---

---

---

---

--

---

9.78E-07

Model
Haldane-Bulton
HaldaneLevenspiel

EPS

RESULTS AND DISCUSSION

---

---

dynamic behavior in a laboratory. Then

Desulfovibrio alaskensis 6SR was

mathematical models, together with

taken as bacterium model for sulfate

carefully designed experiments, make it

reducing

was

possible to evaluate the behaviors of

isolated from a developed biofilm inside

sulfate reducing process more rapidly

face of oil pipeline (Neria et al., 2006).

than with laboratory experiments alone

However, the strain 6SR have the

(Bellomo et al., 2010; Bianca et al.

ability of resistance high concentrations

2009; Prez-Lpez et al., 2012). Also,

of heavy metals (Cd2+, Pb2+, Zn2+ and

the

Cr6+) in comparison with other species

considered in the mathematic model

(Lpez-Prez et al., 2013) is tolerant at

can

oxygen, growths at pH 5.59.0 (7.0),

representation

1555 oC (4 oC) and in 30% (w/v) NaCl.

(Bellouquid,

These characteristics of growing are

2010). In this work the dynamic sulfate

important in environmental processes

reducing

and other as the biocorrosion (Videla &

considering four state variables using

Herrera, 2005, Neria-Gonzlez et al.,

different

2006; Padilla-Viveros et al., 2006;

figure 1. The average of experimental

Hernndez-Gayosos et al., 2004). For

date was graphed to analyze the

this reason, each day the sulfate-

evolution of growth of strain 6SR on

reducing bacteria are important in the

base at consumption of sulfate, sulfide

biotechnological processes and for their

and production of biomass and EPS,

anaerobic nature is difficult to study the

figure 2. An induction phase of growth

process;

this

stain

BioTecnologa, Ao 2013, Vol. 17 No. 2

number

help

of

to

state

give

2010;

process

variables

more

of

real

biosystem

Bellomo

was

mathematical

et

al.,

analyzed

models,

see

18

of three hours and an exponential

no structure model with inhibition to

phase

were

analyze the dynamic for this process,

observed. Before 45 hours a maximum

Table 1. The predictions obtained for

concentration of biomass and sulfide is

each mathematical model: Haldane-

over

maximum

Bulton, Haldane-Levenspiel, Haldane-

consumption of sulfate is also reached;

Luong, Moser-Bulton, and Levenspiel

then the product formation kinetics is a

are represented in the figures 3-6,

simple

where

close

to

taken

between

40

hours

and

stoichiometric
product

connection

be

observed

that

the

and

mathematical models (Equations 2-6),

substrate utilization or cell growth. After

which are based on mass balances

of this time the sulfide is maintained

principles; represent adequately the

constant and presented an inhibition by

corresponding

product affected the growth, and the

Equation 2 considers the biomass

consumption

decreases

concentration production as a function

because the cell begin to die. In this

of sulfate and sulfide concentrations, as

phase, the EPS apparently not is

well as endogenous metabolism via first

related

order biomass dead kinetic. Equations

with

of

formation

can

sulfate

the

using

substrate

at a non-growth associated (Bailey &

generation and the sulfide production,

Ollis,

as a function of the specific microbial

In

addition,

the

represent

growth

induces the producing of EPS as a

corresponding yield coefficients, which

cellular protective mechanism (Caffrey

represents an assimilatory behavior. On

& Voordouw, 2009). Finely, at 170

other side, equation 5 is related with the

hours,

concentrations

EPS production, which is proposed as a

(biomass, sulfate, sulfide and EPS)

function of life and dead biomass

enter in a steady state, the biomass

concentration, this last one variable,

stop to die, there is not consumption of

generated by the inhibitory effect of the

sulfate and formation EPS is stopped.

sulfide concentration.

four

considering

sulfate

accumulation and toxicity of sulfide

the

rate,

the

data.

(sulfate), and such behavior can relate

1986).

and

experimental

the

These results confirmed the use of the

BioTecnologa, Ao 2013, Vol. 17 No. 2

19

Fig. 2. Curve of growth for Desulfovibrio alaskensis 6SR, experimental date of in Postgates C
medium. The symbols indicate: () biomass, () sulfate, () sulfide y () EPS.

Fig. 3. Biomass prediction using kinetic models. The symbol () stands for experimental EPS
data, Haldane and Bulton (
Moser and Bulton (

), Haldane and Levenspiel (

), and Levenspiel (

BioTecnologa, Ao 2013, Vol. 17 No. 2

), Haldane and Luong (

),

).

20

Fig. 4. Sulfate prediction under different kinetic models. The symbol () stands for experimental
EPS data, Haldane and Bulton (
), Moser and Bulton (

), Haldane and Levenspiel (

), and Levenspiel (

), Haldane and Luong (

).

Fig. 5. Sulfide prediction under different kinetic models. The symbol () stands for experimental
EPS data, Haldane and Bulton (
), Moser and Bulton (

), Haldane and Levenspiel (

), and Levenspiel (

BioTecnologa, Ao 2013, Vol. 17 No. 2

), Haldane and Luong (

).

21

Fig. 6. EPS prediction under different kinetic models. The symbol () stands for experimental
EPS data, Haldane and Bulton (
), Moser and Bulton (

), Haldane and Levenspiel (

), and Levenspiel (

), Haldane and Luong (

).

The kinetic parameters estimated

Bulton model presents the same case

on each model are displayed in Table

and Haldane-Luong model only exceed

2, and overall correlation coefficients

the

from each models were higher than

Levenspiel

0.93 (Table 3). However the correlation

models

coefficients for Levenspiel and Moser-

Levenspiel

Bulton models were the highest, 0.96

overall correlation coefficients. Besides,

and 0.98, respectively. Strictly, the best

all models represent the effect of

kinetic model to be used to describe the

substrate and product inhibition, except

bacterial growth should be the highest

Levenspiels model in which product

correlation coefficient (Arellano-Plaza et

inhibition is only considered. In previous

al., 2007; Agarwal et al., 2009), in this

publications has been mentioned that

case Mosser-Bulton (0.98), but the

the Moser and Haldane models were

value of maxis higher than at maximum

designed to achieve better adjust to

rate reported by Feio (0.13 1/h) (2004)

experimental data (Heijnen & Romein

and

the

1995; Trejos et al., 2009), and in this

experimental inhibition concentration of

case the corresponding models adjusts

sulfide (> 500 mg/l) and KS exceed the

only in different parts of growth curve

experimental value, (Table 2). Haldane-

from all variables, but Levenspiels

KP

does

not

represent

BioTecnologa, Ao 2013, Vol. 17 No. 2

value

of

max,

and

would

so

Haldane-

Levenspiel
be

model

kinetic

employed,
presented

but
better

22

model presented the best adjust along

of the curve of growth see Fig. 7-10.

Table 3. Correlation coefficients calculated for each kinetic model.

Correlation coefficient
Model

Overall r2

Biomass

Sulfate

Sulfide

EPS

Haldane-Bulton

0.88

0.92

0.94

0.98

0.94

Haldane-Levenspiel

0.92

0.87

0.98

0.93

0.94

Haldane-Luong

0.92

0.87

0.97

0.93

0.93

Moser-Bulton

0.95

0.99

0.97

0.99

0.98

Levenspiel

0.92

0.95

0.98

0.98

0.96

Fig.7. Error calculated from simulations of biomass for each model. The symbols represent
models, Haldane and Bulton (), Haldane and Levenspiel ( ), Haldane and Luong ( ), Moser
and Bulton ( ), and Levenspiel ().

BioTecnologa, Ao 2013, Vol. 17 No. 2

23

Fig.8. Error calculated from simulations of sulfate for each model. The symbols represent models,
Haldane and Bulton (), Haldane and Levenspiel ( ), Haldane and Luong ( ), Moser and Bulton(
), and Levenspiel ().

Fig.9. Error calculated from simulations of sulfide for each model. The symbols represent models,
Haldane and Bulton (), Haldane and Levenspiel ( ), Haldane and Luong ( ), Moser and Bulton(
), and Levenspiel ().

BioTecnologa, Ao 2013, Vol. 17 No. 2

24

Fig.10. Error calculated from simulations of EPS for each model. The symbols represent models,
Haldane and Bulton (), Haldane and Levenspiel (), Haldane and Luong (), Moser and Bulton (),
and Levenspiel ().

In this kinetic analysis was observed

consequence, the model of Levenspiel

that the effect of inhibition occurred

represented

approximately at 600 mg/l of sulfide.

behavior of this process type, see Fig.

This effect is represented in all models,

11. A mathematical model with more

except on model Haldane-Bulton, see

variables can describe better the real

table 2, also correspond with previously

world, in the sense that their qualitative

date

Harrison,

predictions are in accordance with the

2006). The accumulation of sulfide in

observed data. This is illustrated on

the

some recently obtained results on

reported

(Mossa

environment

affect

&

the

free

adequately

cadmium

behavior of sulfate-reducing processdo

alaskensis 6SR, where is remarked that

not be represented by single Monod

the using mathematical model with

model and more when are considering

more of one variable (Lpez-Prez et

more than two variables, due to poor fit

al. 2013) the cadmium removal can be

(Gonzlez-Silva

estimated.

al.,

2009).

In

BioTecnologa, Ao 2013, Vol. 17 No. 2

using

overall

multiplication cellular, then the kinetic

et

removal

the

at

D.

25

Fig.11. Comparison of the experimental and predicted data, employing model kinetics Levenspiel.
Experimental biomass (), experimental sulfate (), experimental sulfide (), and experimental EPS
(+). The continua line represents prediction data.

In conclusion, kinetic models are a

expression to EPS production kinetic,

grand tool in the bioprocesses allowing

the overall behavior of system is

biochemical

satisfactory.

engineers

to

design,

optimize, control microbial processes

and, predicting the behavior of a
bioprocess too (Bellouquid & Delitala,
2005).

Then

together

models,

carefully

designed

with

experiments,
evaluate

mathematical

the

make

it

possible

behaviors

of

to

sulfate-

ACKNOWLEDGMENTS
J. C. Figueroa-Estrada would like to
thank to Consejo Nacional de Ciencia y
Tecnologa

(CONACyT)

corresponding

for

the

postgraduate

scholarship.

reducing process more rapidly than with

laboratory experiments alone, due at

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Nomenclature
X

: Biomass concentration (mg/l)

: Substrate concentration (mg /l)

: Product concentration (mg/l)

Xd

: Concentration of dead biomass (mg/l)

EPS

: Extracellular polymeric substances concentration (mg/l)

P*

: Inhibitory product concentration (mg/l)

KS, Ki, KP

: Substrate affinity constant, inhibition constant, term inhibition (mg/l)

KE

: Constant for EPS (1/h)

rX

: Growth rate (mg-biomass/l per h)

rd

: Death rate (mg-death biomass/l per h)

, d, max

: Specific growth rate, specific death rate, maximum rate growth (1/h)

YS/X

: Substrate-biomass yield coefficient (mg-sulfate/mg-biomass)

YP/X

: Product-biomass yield (mg-sulfide/mg-biomass)

: Exponential term for Luong model

: Exponential term for Moser model

: Exponential term for EPS model

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