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Emission of Volatile Organic Compounds and Greenhouse

Gases from the Anaerobic Bioremediation of SoilsContaminated with Diesel

Marcio Gonçalves Franco & Sergio Machado Corrêa &

Marcia Marques & Daniel Vidal Perez

Received: 12 June 2013 / Accepted: 15 January 2014 / Published online: 1 February 2014# Springer International Publishing Switzerland 2014

Abstract Bioremediation processes have been credited

for reducing high levels of organic contaminants from

soils. However, during the bioremediation of soils con-

taminated with diesel, the conversion of heavy mole-

cules to volatile organic compounds (VOCs) and green-

house gases (GHGs) and the volatilization of light mol-

ecules can occur. The ongoing construction of a large

petrochemical complex in Rio de Janeiro (COMPERJ)

and the transportation of large volumes of oil by-

products have raised serious concerns regarding

accidents that may result in soil contamination.

Bioremediation is a potential technique that can be

applied to minimize damage from such contamination.

The objective of this study was to characterize the

emission of GHGs and VOCs during the bioremediation

of soils contaminated with diesel oil. Soil samples

contaminated with 0.5, 2.0, and 4.0 w/w% diesel oil

were kept in glass rectors (2 L internal volume) for

3 months under anaerobic/anoxic conditions. The soil

moisture was kept at 80 % of the field capacity.

Bioremediation processes were investigated in regard

to nutrient adjustment (biostimulation), no adjustment

(natural attenuation), and sterilized soil (abiotic pro-

cess). The gases emitted from various reactors were

collected with coconut shell charcoal cartridges, and

the GHGs were collected in Tedlar bags. The chemical

analyses of GHGs and VOCs were performed using gas

chromatography. The results indicated that air samples

contained high concentrations of CO2, but low concen-

trations of CH4. Differences in the composition of the

gas emitted, regarding CO2, were not statistically sig-

nificant. Regarding VOC emissions, such as alkanes and

alkenes (both branched), cycloalkanes, and aromatic-

substituted compounds, the compounds with higher

emissions were cycloalkanes and branched alkanes.

Keywords Emissions . Diesel . Atmosphere .

Bioremediation . VOC . GHG

1 Introduction

Soil contamination is the result of the industrial progress

that society has experienced during the second half of

the last century as well as the rapid population and

economic growth in the present century. A list of USA

environmental national priorities from the mid-90s iden-

tified 1,200 contaminated areas with the potential of

Water Air Soil Pollut (2014) 225:1879

DOI 10.1007/s11270-014-1879-z

M. G. Franco : S. M. Corrêa (*)

Faculty of Technology, Rio de Janeiro State University-UERJ,

Rodovia Presidente Dutra, km 298, Resende, RJ 27537-000,

Brazil

e-mail: [email protected]

M. MarquesFaculty of Engineering, Rio de Janeiro State

University-UERJ,

Rua São Francisco Xavier,524, sala 5024E, Maracanã, Rio de

Janeiro, RJ 20559-900, Brazil


D. V. Perez

National Centre for Soil Research, Embrapa,

Rua Jardim Botânico 1024, Jardim Botânico, Rio de Janeiro,

RJ 22460-000, Brazil



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increasing to 32,000 sites, according to Singh and Ward

(2004). In the largest Brazilian cities, such as Rio de

Janeiro and São Paulo, environmental protection agen-

cies have reported several contaminated areas. The pe-

troleum industry introduces toxic pollutants into the

environment through several processes, such as explo-

ration, exploitation, transportation, storage, and refine-ment. While the environmental and health problems

resulting from the pollution of soil and water with

petroleum are well-known, the impacts on the atmo-

sphere are poorly studied. Large quantities of volatile

organic compounds (VOCs) are released into the atmo-

sphere during accidents, general operations, and during

treatment processes of contaminated soil and water. To

address the issue raised by remediation technologies and

their potential to release pollutants into the atmosphere,

the bioremediation technique and the soil from the re-

gion where the Petrochemical Complex of Rio deJaneiro (COMPERJ) has been constructed were chosen

for study. COMPERJ is a petrochemical complex being

built in the region of Itaboraí in the Rio de Janeiro

Metropolitan Area that primarily aims to increase the

domestic production of petrochemicals. COMPERJ will

be responsible for processing 450 thousand barrels per

day of crude oil with a high transportation flow of raw

materials as well as final products. Consequently, the

risk of pollution related to oil spills is expected to

increase considerably.

According to Militon et al. (2010) and Jϕrgensen(2011), bioremediation processes are influenced by

physical and chemical conditions, including nutrient

ratios related to the organic carbon and type of micro-

organisms. The more important nutrients are nitrogen

and phosphorous (in regard to microbiology activity and

cell growth). As stated by Militon et al. (2010), the

adjustment of carbon:nitrogen ratio in petroleum-

contaminated soils can increase cell growth rate, de-

crease the microbial lag phase, help to maintain micro-

bial populations at high activity levels, and increase the

rate of hydrocarbon degradation. Jϕrgensen (2011) alsosuggested using nitrogen levels lower than 100 mg kg−1

for the biodegradation of petroleum hydrocarbons,

but depending on organic carbon concentr ation.

Temperature also plays an important role in the mecha-

nism of bioremediation. Jϕrgensen (2011) and Nester

et al. (2001) highlighted that the speed of enzymatic

reactions in the cell doubles for each 10 °C rise in

temperature. In this case, controlling temperature is very

important for the optimization of the bioremediation

process. In some cases, high temperatures could inacti-

vate bacterial metabolism and, therefore, interrupt the

treatment. According to Jϕrgensen (2011), the use of

high temperatures is appropriate only in the presence of

thermophilic microorganisms, as the temperature acti-

vation is close to 60 °C. Perfumo et al. (2007) suggested

the intrinsic potential for natural attenuation in cool soilsthrough thermally enhanced bioremediation techniques.

In terms of the compounds produced by remediation

processes, emission to the air have been studied by

many authors, such as Pasumarthi et al. (2013),

Mumford et al. (2013), and Karamallidis et al. (2010).

In a specific case of anaerobic processes, Rodrigues

et al. (2013), Da Cruz et al. (2011), Barret et al.

(2010), Diplock (2009), Haritash and Kaushik (2009),

Gan et al. (2009),Li et al. (2010), Eibes et al. (2006), Yu

et al. (2005), and Díaz (2004) registered no significant

variation in temperature during the treatments, different-ly from aerobic processes. Some gases are formed by

both anaerobic and aerobic processes, including carbon

dioxide (CO2), methane (CH4), and nitrous oxide

(N2O), but only under anaerobic conditions that methan-

ogenic reactions are observed in large scale (Díaz 2004).

The bioremediation of oil-contaminated soils has

shown to be highly efficient; the microorganisms typi-

cally receive all of the credit for the removal efficiency.

Losses due to volatilization or breakages of contami-

nants into lighter molecules with subsequent volatiliza-

tion with no interference from microorganisms have not been estimated. According to Solomons and Fryhle

(2011), breaking down hydrocarbons into smaller mol-

ecules is simple but requires the availability of metals

such as iron, nickel, or aluminum in the soil. According

to EMBRAPA (1997), most soils contain these metals,

and reactions catalyzed by these metals are possible.

Environmental problems related to the emissions of

VOCs and greenhouse gases (GHGs) are known to

occur. The major problems associated with these emis-

sions are the quantities of the emitted gases into the

atmosphere and the impact of the Greenhouse effect.There is a direct link between GHG and VOC emissions

and the Greenhouse effect, as described by Giostra et al.

(2011), He et al. (2012) and Koornenerf et al. (2012)

which is considered to be one of the most serious

problems facing the society today.

With the fast development of environmental prob-

lems related to the emissions of VOCs and GHGs, few

studies assessing this aspect have been completed.

According to Tammadoni et al. (2013) and Zou et al.

1879, Page 2 of 9 Water Air Soil Pollut (2014) 225:1879


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(2003), many VOCs (hydrocarbons) are released using

energy. In case of storage of waste for energy genera-

tion, some authors such as Hafner et al. ( 2013),

Koornenerf et al. (2012), He et al. (2012), and Chiriac

et al. (2011) mentioned that VOCs released include not

only hydrocarbons, but also compounds such as alco-

hols, ketones, esters, benzene, cyclic compounds, andterpenes. These studies quantified VOCs and found

alarming emission values during the storage (high con-

centrations of CH4 and CO2 and CO emissions).

Likewise, the present study seeks to quantify the

VOCs and GHGs released during the anaerobic biore-

mediation process of soils contaminated with diesel oil.

The specific objectives of this study are as follows: (i) to

assess the conversion of heavy into lighter hydrocarbons

under three different microbiological conditions (abiotic

processes, natural attenuation, and biostimulation); (ii)

to characterize the emission patterns and quantify VOCsand GHGs during the treatment period; and (iii) to check

the residual contaminants in the soil after treatment.

2 Methodology

2.1 Soil Sampling and Site Description

The soil used in the study was collected at the

COMPERJ region (located at Rodovia Estadual RJ

116 km 5 Itaboraí — RJ, Brazil at 22°41′22″S and42°49′47″W ) . T h e s o i l w a s c h a r a c t e r i z e d b y

EMBRAPA as a Cambisol (Inceptisol by USA soil

classification). Ten soil samples were collected with a

cleaned shovel at an average depth of 10 cm in a

randomized sampling design in an area of approximate-

ly 1,000 m2. At the laboratory, the samples were ho-

mogenized and a composite soil sample of approximate-

ly 60 kg was oven-dried at 40°C±2°C, passed through a

2 mm mesh sieve, stocked in a polyethylene bag, and

stored in a temperature-controlled room (±25 °C). The

characterization was made according to EMBRAPA(1997), Bertrand (1965), Bohn et al. (1979), and

Brener and Jackson (1970).

2.2 Experimental Setup

To assess air emissions from soils contaminated with

diesel without the interference of microorganisms (abi-

otic processes — AB), under natural conditions (natural

attenuation — NA), and with the stimulation of the

indigenous microorganisms (biostimulation — BI),

three different setups (AB, NA, and BI) were prepared

as described below.

Abiotic Processes (AB): To assess the emissions from

soil samples with no microbial activity, the soil pH was

adjusted to neutrality (approximately 7.0), as describedin the literature (U.S. EPA 1996; Sarkar et al. 2005). The

soil was then subjected to sodium azide (5 % w/w) for

1 h and autoclaved for 2 h. The water used for moisture

adjustment was also autoclaved.

Natural Attenuation (NA): To assess the degradation

processes with no interference, the soil was tested with-

out any chemical or thermal sterilization. The pH was

not adjusted and no sodium azide or thermic sterilization

was applied. Only moisture and nutrient ratio were

controlled.

Biostimulation (BI): To enhance microbial activity, the

soil pH was adjusted to neutrality (approximately 7.0),

as described in the literature (U.S. EPA 1996; Sarkar

e t a l . 2005) ; n o s t e r i l i z a t i o n w a s p e r f o r m e d .

Phosphorous (sodium phosphate — Na 3PO4) and nitro-

gen (urea — C(NH2)2O) were added according to the

literature. Some authors (Ausma et al. 2002; Liebeg and

Cutright 1999) suggest a C:N:P ratio of 100:5:1 per

100 g of soil while others (Colla et al. 2013) suggest 100:10:1. With the addition of diesel B5, the total or-

ganic content increased according to the amount added

(5.0, 20, or 40 g per kg of soil). The initial C:N:P ratio in

all experimental units was adjusted to achieve a ratio of

about 100:5:1, adding 0.42 g of P and 0.084 g of N to the

original soil with 8.4 g of C per kilogram of soil.

The emissions of VOCs and GHGs from bioremedi-

ation processes were studied using 2-L glass reactors

coupled with coconut shell charcoal (CSC double bed

400/200 mg — Supelco ORBO 32) cartridges (NIOSH

2003; U.S. EPA 1984) and 3-L Tedlar bags in series(Fig. 1). The emissions were measured during the treat-

ment of 1.0 kg of soil artificially contaminated with

commercial diesel oil. The commercial diesel oil (with

5 % biodiesel) was chosen to reflect the current use of

B5 diesel in Brazil and the subsequent increased poten-

tial for accidents during the first year of COMPERJ’s

operation. The B5 diesel concentrations in the treated

soil samples were 0.5 %, 2.0 %, and 4.0 % w/w. Each

treatment (AB, NA, and BI) in three levels of

Water Air Soil Pollut (2014) 225:1879 Page 3 of 9, 1879


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contaminants (0.5, 2.0, and 4.0 % w/w) was made in

triplicate resulting in 27 reactors or experimental units

monitored for 3 months. Soil humidity was controlled

throughout the experiment to 80 % of its field capacity

using the gravimetric method. The reactors were

weighed each week, and the water content was adjusted

by adding fresh distilled water to its top. The reactorswere kept in the same room throughout all of the exper-

iments at an ambient temperature of 20 °C and without

sunlight.

2.3 Emissions Sampling

The CSC cartridges were changed after 30, 60, and

90 days and analyzed for light VOCs (adsorbed on the

CSC cartridges). The gases retained in the cartridges

were extracted with 1.0 mL of dichloromethane in an

ultrasound bath for 10 min. GHGs stored in the Tedlar

bags were sampled with a 10-mL gastight syringe and

analyzed on the same day immediately after the collec-

tion. The volume collected by each bag was measured

using a 250-mL polypropylene syringe. The gas was

measured once a month. After 90 days, the remaininghydrocarbons in the contaminated soils were extracted

using cyclohexane in a Soxhlet extractor for 4 h and

analyzed.

2.4 Analysis of Fungi and Bacteria

Microbiological analyses were made at the beginning

of the treatment. The methodology was performed

using Petri plates and vials sterilized in autoclave

NOVATECNICA model NT 713. Culture medium was

prepared with Sabouraud (64 mg L−1), agar solution

(2.5 mg L−1), and NaCl solution (0.085 % w/v). The

soil – saline solution was prepared with 9.0 mL NaCl

solution added to 1 g of soil. After that, different dilu-

tions were made: 1:1000 for BI and 1:100 for AB and

NA reactors. Then, the mixture was poured in the cul-

ture medium in Petri plates (inert atmosphere). The

incubation temperature was 28 °C during 48 h. After

incubation, colonies were counted in QUIMIS model

295 counter.

2.5 Chemical Analyses

VOC analyses on samples obtained with CSC cartridges

and n-alkanes from the soil were performed using a

Varian 450 Gas Chromatograph coupled to a Varian

220 Mass Spectrometer (ion trap) under the following

conditions: injector at 120 °C; mobile phase He

1.0 mL min−1; VF5MS column 30 m×0.25 mm×

0.25 μ m; column temperature of 40 °C for 4 min,

followed by heating at 10 °C min−1 to 200 °C and

stabilizing for 10 min; and 1.0 μ L splitless injection.The mass spectrometer was operated in SCAN mode

(45 – 360 m/z), with a trap temperature at 250 °C, transfer

line at 280 °C, and manifold at 40 °C. Quantification

was performed by the external standard method using a

ChemService TPH-6JM standard (Diesel Range

Organics Mixture #2). Calibration curves with five

levels in triplicate were used, ranging from 0.5 to

10.0 mg L−1 of each compound; the coefficient correla-

tions were greater than 0.98.

Fig. 1 Scheme of the reactor used in the experiments



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For GHGs, chemical analyses were performed using

an Agilent 7890A Gas Chromatograph with three de-

tectors: a thermal conductivity detector (TCD) to mea-

sure CO2 at high levels as well as molecular oxygen and

nitrogen, an electron capture detector (ECD) to measure

N2O, and a flame ionization detector (FID) to measure

CH4 and CO2 at low levels.The developed chromatograph system uses two sep-

arated channels with 1/8″ packed columns (HayeSep

Q80/100). The first channel uses two valves for the

TCD and FID, arranged in series to measure CO2 using

a metanizer to convert CO2 to CH4. The other channel

with two valves is used to measure N2O on the micro

ECD. Two pre-columns are used to retain heavier com-

pounds and send oxygen and water to vent. A 1.0 mL

sampling loop is used, columns are kept at 60 °C, and

valves are kept at 100 °C. The FID is operated at 250 °C,

the ECD at 350 °C, and the TCD at 200 °C. Helium 5.0is used as the mobile phase at 21 mL min−1. The cali-

bration was performed using five standards (from Linde

Gas) with GHG concentrations ranging from 351 to

451 μ mol mol−1 of CO2, 1.510 to 2.010 μ mol mol−1

of CH4, and 0.250 to 0.350 μ mol mol−1 of N2O. The

correlation coefficients (R 2) for the calibration curves in

triplicates were higher than 0.99 for CO2 and CH4 and

0.98 for N2O.

3 Results and Discussion

3.1 Soil Characterization

Soil from the COMPERJ site has a sandy loam texture,

with 120 g kg−1 of clay and 798 g kg−1 of sand. Low

clay content is a positive characteristic for bioremedia-

tion purposes. Elemental analysis of this soil indicated a

low content of organic carbon (8.4 g kg−1) and a C/N

ratio (10) consistent with a well-humidified organic

matter. Therefore, the contaminant will be the main

carbon source for microorganism’s growth. The acidic pH (5.3), low base saturation (8 %), high aluminum

saturation (58 %), and low content of phosphorus are

consistent with tropical soil conditions. Such low pH

required adjustment to a value around 7.0 to optimize

microbiota (particularly bacteria) metabolism. In this

context, the high amount of aluminum found in the soil

sample (0.7 cmolc kg−1) can facilitate biodegradation, as

this metal can act as an electron acceptor. Regarding the

extraction of other metals by Mehlich 1 solution (HCl

0.05+H2SO4 0.0125 mol L−1), the levels of Fe, Mn, Zn,

and Cu were within the range found in Rio de Janeiro

State (Palmieri et al. 2003). The levels of Cr, Cd,

and Pb were within the normal range in Brazilian

soils. Co and Ni were below the detection limit of

the technique (ICP-AES).

3.2 Temperature

The temperatures reached by the soil mass during vari-

ous treatments showed negligible variation. According

to Jacques and Seminoti (2006), in anaerobic systems,

electron transfer reactions occur with a low energy

release. No supply of oxygen was available throughout

the 90 days that the samples were in the locked reactors,

aiming to establish an anaerobic environment. The

highest temperature observed in the biostimulation re-

actors occurred at the end of the experiment, but did not exceed 23 °C. In the other reactors, the temperature did

not exceed 22 °C.

3.3 GHG Emissions

High GHG concentrations (CH4, CO2, and N2O) were

observed even after 90 days of treatment as shown in

Figs 2, 3, and 4.

CH 4: Different treatments (AB, NA, and BI) resulted inless variation regarding methane concentration in sam-

ples obtained after 30, 60, and 90 days from reactors

containing soil with high contamination (4 % B5 diesel)

compared to those from reactors with soils with lower

contamination (0.5 % B5 diesel). Samples collected in

the ambient air of the experiment room displayed

1

2

3

30 days 60 days 90 days

p p m C

H 4

AB 0.5%

AB 2.0%

AB 4.0%

NA 0.5%

NA 2.0%

NA 4.0%

BI 0.5%

BI 2.0%

BI 4.0%

Fig. 2 CH4 concentration from reactors with soil contaminated

with0.5%, 2.0 %,and 4.0 % dieselB5 after 30, 60, and90 daysof

treatment by AB, NA, and BI



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methane values ranging from 1.3 to 1.7 ppm, indicating

t h a t t h e m e t h a n e w a s e m i t t e d f r o m a l l o f t h e

experiments.

CO2: The concentrations of CO2 emitted from all treat-

ment are shown in Fig 3. A trend towards reduction in

the CO2 emitted throughout the days of the experiment

in all of the reactors, regardless of the initial concentra-

tion of the soil contaminant and the treatment applied,

was observed. A higher initial B5 diesel concentration in

the soil led to a higher concentration observed after 30

and 60 days of treatment. However, by the end of the

experiment, all treatments were releasing approximately

450 ppm CO2. The ambient air of the experiment room

revealed values ranging from 380 to 410 ppm of CO2,

indicating that the emissions from the reactors are

considerable.

N 2O: Regardless of the treatment applied (AB, NA or

BI) or the initial concentration of the contaminant in the

soil, after 30 days of treatment, the concentration in the

sample was approximately 20 % higher than that mea-

sured after 60 and 90 days of treatment. A plateau of

N2O concentration approximately 300 ppb was reached

in samples obtained after 60 and 90 days of experimen-

tation. The ambient air of the experiment room present-

ed N2O values ranging from 295 to 310 ppb, indicatinga small emission of this GHG after 60 and 90 days of

experimentation.

The results suggest that the studied gases were gen-

erated by anaerobic processes. According to Díaz

(2004), the generation of CH4 and CO2 is a common

process in which oxygen is not necessary. The steps of

these processes are described by reactions presented by

Díaz (2004):

Cn

Hm HC aromaticð Þ

þ organic material þ initial carbon

→organic acids þ H−

ð1Þ

Organic acids þ H−→CH4 þ H2 þ CO2 excessð Þ ð2Þ

Despite these aspects, the possibility that CHG was

formed by chemical reactions (transformation of heavy

hydrocarbons into lighter molecules such as CH4 and

CO2) should be considered; however, this discussion

will be completed in another paper. A simple example

of this kind of reaction is that shown in Eq. 3, but in

presence of catalysts such as nickel and iron (Solomons

and Fryhle 2011):

CnHm HC aliphatic – heavy moleculesð Þ

→CnHm HC aliphatic – light molecules−COVð Þ

ð3Þ

3.4 Remaining Contamination in Soil

Figure 5 shows concentrations of several remaining n-

alkanes that were extracted from the soil originallycontaminated with 2 % of diesel B5 and after 0 days

of treatment in different reactors. Although the relative

abundance of each remaining compound is maintained

in all treatments, the soil that underwent biostimulation

(reactors BI) showed consistently less remaining n-al-

kanes than the soils treated by from the natural attenu-

ation reactor (NA) and abiotic processes (AB), suggest-

ing that higher degradation occurred in BI and to a lesser

extent in the NA process. A more detailed observation

300

350

400

450

500

550

600


p p m C

O 2

AB 0.5%

AB 2.0%

AB 4.0%

NA 0.5%

NA 2.0%

NA 4.0%

BI 0.5%

BI 2.0%

BI 4.0%

Fig. 3 CO2 concentration from reactors with soil contaminated

with0.5%, 2.0 %,and 4.0 % dieselB5 after 30, 60, and90 daysof

treatment by AB, NA, and BI

0

50

100

150

200

250

300

350

400

450


p p b N 2 O

AB 0.5%

AB 2.0%

AB 4.0%

NA 0.5%

NA 2.0%

NA 4.0%

BI 0.5%

BI 2.0%

BI 4.0%

Fig. 4 N2O from reactors with soil contaminated with 0.5 %,

2.0 %, and 4.0 % diesel B5 after 30, 60, and 90 days of treatment

by AB, NA, and BI



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of one group of hydrocarbons with 10 carbons (decane),

for instance, reveals that the concentration of decane in

the soil after the experiment is


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4 Conclusions

This investigation demonstrated that emissions of VOCs

occur under anoxic/anaerobic conditions. The possibil-

ity of the conversion of larger hydrocarbons into smaller

ones during the experiment should be considered.

Further studies should be conducted to confirm theabsence of active microbiota in sterilized soils.

Regarding GHG emissions, it is not possible to assume

that the entire content of generated gas comes from

biological processes. It is more likely that a different

population of microorganisms colonize the soil after

sterilization takes place due to the low residual effec-

tiveness of the applied sterilization procedures. There is

no doubt, however, that the contribution of GHGs from

the bioremediation processes is not negligible and it

should be measured or at least estimated in full-scale

treatment plants.

Acknowledgments The financial support from the Rio de

Janeiro Foundation for Research Assistance (FAPERJ) as well

as the Brazilian National Council for Scientific and Technological

Development (CNPq) is acknowledged. The support for interna-

tional exchange from the Swedish Foundation of International

Cooperation in Research and Higher Education (STINT) was also

appreciated.

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