Fuel 290 (2021) 119973

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Fuel
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Full Length Article

Influence of surface mineralogy on the activity of Halanaerobium sp. during

microbial enhanced oil recovery (MEOR)
Felix Kögler a, *, Nicole Dopffel b, Eva Mahler c, Fabian S.F. Hartmann d,
Dirk Schulze-Makuch e, f, g, Foppe Visser a, Bernd Frommherz a, Andrea Herold c, Hakan Alkan a
a
Wintershall Dea GmbH, 34119 Kassel, Germany
b
Norwegian Research Center NORCE, 5008 Bergen, Norway
c
BASF SE, 67056 Ludwigshafen, Germany
d
Department of Biotechnology and Biomedicine, Technical University of Denmark, 2800 Kgs. Lyngby, Denmark
e
Center of Astronomy & Astrophysics, Technische Universität Berlin, 10623 Berlin, Germany
f
Section Geomicrobiology, German Research Centre for Geosciences (GFZ), 14473 Potsdam, Germany
g
Department of Experimental Limnology, Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), 12587 Stechlin, Germany

A R T I C L E I N F O A B S T R A C T

Keywords: Microbial enhanced oil recovery (MEOR) is an economically attractive tertiary recovery technique and fermen­
Microbial enhanced oil recovery tative bacteria are frequently suggested for MEOR, partly because microbially produced organic acids have the
Carbonate dissolution potential for rock matrix dissolution.
Dynamic experiment
In this study, the metabolic activity and the community shift of a diverse microbiome of a high-salinity oilfield
Reservoir microbiology
upon supplying MEOR nutrients was investigated in dynamic sandpacks set-up with and without crude oil using
Halanaerobium
High salinity pure quartz sand and two types of reservoir rock. Geochemical characterization of the porous media included
specific surface area (SSA), X-ray diffraction (XRD) and X-ray photoelectron spectroscopy (XPS). During the exper­
iments, substrate and metabolites, incremental oil and differential pressure were monitored and the microbial
community shift was investigated via Illumina sequencing.
Fermentative Halanaerobiales outcompeted other microbes and led to an incremental oil recovery of 24.5 ±
9.6 %OOIP in reservoir rock. Microbial-induced dissolution of surface minerals was indicated by a decrease in SSA
and surface-bound ferrous iron and concluded to be an important MEOR mechanism. Fermentation of sucrose
was primarily limited by an insufficient acid neutralization capacity (ANC), but a carbonate content of 12%
sustainably buffered the pH in a favorable growth range. Even minor amounts of other non-inert minerals (1%
pyrite and calcite) facilitated microbial growth significantly, resulting in six-fold higher acetate production rates
compared to quartz sand. Besides emphasizing the relevance of accessory minerals in MEOR, our results imply
that the ANC could serve as potential screening parameter for predicting the performance of fermentation - based
MEOR in the field.

1. Introduction hand, detrimental effects include biodegradation of aliphatic hydro­

Oil reservoirs represent an extreme microbial habitat characterized
by high pressures, temperatures and salinities. Yet, diverse functional
microbial groups have adapted to these harsh conditions including
anaerobic hydrocarbon degraders, sulfate, nitrate and iron reducers,
acetogens, methanogens and also fermentative bacteria [1,2]. Over the
last years, the interest of the petroleum industry in reservoir microbi­
ology has increased because microbes can have a significant impact on
oil recovery and production operations in various ways. On the one
carbons and the activity of sulfate reducing microorganisms (SRM) which
leads to reservoir souring and microbial influenced corrosion [3–5]. On
the other hand, microorganisms can be used in tertiary oil recovery to
enhance oil production, a process referred to as microbial enhanced oil
recovery (MEOR). In situ MEOR describes the injection of nutrients into a
reservoir to stimulate the indigenous microbial community. Hereby,
several oil recovery mechanisms can be induced which include (i)
improved mobility ratios of fluids; (ii) wettability alteration; (iii) bio­
surfactant and emulsifier production; (iii) bioplugging of high-

* Corresponding author at: 1A Douro Place, W85PH, London, UK.

E-mail address: felix.koegler@rws.com (F. Kögler).

https://doi.org/10.1016/j.fuel.2020.119973
Received 16 July 2020; Received in revised form 2 November 2020; Accepted 8 December 2020
Available online 24 December 2020
0016-2361/© 2020 Elsevier Ltd. All rights reserved.
F. Kögler et al.
permeability zones by microbes and associated conformance control and
(iv) permeability increase through organic acid induced rock dissolution
in reservoirs with non-inert minerals [6–8].
The latter two are of specific relevance in heterogenous oil reservoirs
which are not comprised exclusively of quartz. More than half of the
world’s conventional oil reserves are found in fractured carbonate res­
ervoirs [9–11] and pore cementation with reactive minerals like gyp­
sum, calcite and siderite is a frequent diagenetic process [12]. In fact, it
is estimated that 15% of global siliciclastic oil reservoirs contain
dominant rock grains which are chemically and physically unstable
(Davies, 1980) and even minor amounts of these minerals can make up
most of the pore-mineral contact boundary [13]. In such formations,
high specific surface area and high salinities with a significant concen­
tration of divalent cations represent a major challenge for conventional
chemical EOR, e.g. due to adsorption or crosslinking of polyacrylamide
(PAM) polymers and anionic surfactants [14–16]. Here, MEOR has a
particularly promising potential because certain microorganisms have
adapted to high salinities. In addition, the combination of conformance
control in high-permeability zones by bioplugging and a simultaneous
permeability increase by diversion of microbially produced organic
acids in low-permeable reservoir matrices might significantly improve
sweep efficiency and enhance production of remaining oil.
Fermentative bacteria, which quickly generate high cell densities
and form gases as well as organic acids when conditions are favorable,
appear to be predestinated MEOR candidate species in calciferous for­
mations. With terminal electron acceptors such as oxygen, nitrate or
oxidized metals being scarce under most reservoir conditions, fermen­
tation is the most probable metabolic pathway, if suitable electron do­
nors are provided. However, members belonging to the order of
Halanaerobiales have not been investigated for MEOR yet, although
they have been detected frequently in medium and high-salinity hy­
drocarbon reservoirs recently [17,18] and are known to ferment di­
saccharides to organic acids, alcohols and gases [19]. Yet, one of the
major constraints for sustaining continuous microbial fermentation is
the rapid decrease in ambient pH due to the acidification of the sur­
rounding medium. Although researchers have acknowledged microbial
sensitivity to environmental pH and the dependence of MEOR on
geochemical aspects [6,20], the pH-buffering potential of minerals
during microbial fermentation in a porous medium has not been taken
into consideration yet. In order to close the tremendous research gap
regarding biogeochemical interactions between acid-producing bacteria
and non-inert rocks such as carbonates or calcareous and ferruginous
sandstones., we performed anaerobic sandpack experiments with
different lithologies including quartz sand, two samples of reservoir
sandstone and crushed limestone. These were inoculated with an
oilfield-derived, halophilic microbial community and flooded with nu­
trients to investigate (i) how carbonate content and non-inert mineral
cements of a porous medium influence the microbial growth of
fermentative anaerobic bacteria of the order Halanaerobiales; (ii)
whether the geochemistry of the porous medium was altered by the
fermentative activity of Halanaerobiales and (iii) if the applied MEOR
approach resulted in incremental oil recovery.
2. Materials and methods
2.1. Rock used in sandpack experiments
Three different lithologies were used in sandpacks: Pure quartz sand
(QS, Nudersdorf, Germany) and two core samples from an Upper Val­
anginian oil reservoir (T = 37 ◦ C), selected as a pilot candidate for a
MEOR application [21–23]. The reservoir rock included a siderite-
cemented sandstone (SC) and an uncemented reservoir sandstone (RS)
with the non-quartz minerals of the reservoir rock mainly present as
carbonate pore cements [24]. For the use as porous medium in sand­
packs, reservoir rock samples SC and RS were crushed with a bead-mill
and only grain size fractions < 1000 µm were used. Quartz sand (QS)
2
Fuel 290 (2021) 119973
was suspended several times with 0.1 M HCl and decanted to remove
fines and contaminants and dried (60 ◦ C, p = 0 bar). For X-ray diffraction
(XRD), X-ray fluorescence (XRF), X-ray photoelectron spectroscopy (XPS),
Specific surface area (SSA) measurements, samples were Soxhlet -
cleaned from residual oil for several hours until the condensing solvent
was clear (60:40%-v/v cyclohexane:ethanol, T = 130 ◦ C). After solvent
evaporation, oil-free samples were rinsed with ddH2O and dried (60 ◦ C,
p = 0 bar). Mineral phases were identified via XRD (D8 Advance with Cu
target tube at 40 kV and 40 mA, Bruker, USA) and cross-correlated to
XRF results (Xepos EDXRF, Spectro Analytical Instruments GmbH,
Germany). pH of the rock samples was determined as the active pH by
suspending 10 g of sample in 25 mL ddH2O (double pore slim electrode,
Hamilton, USA). Subsequently, the acid neutralization capacity (ANC)
was determined via step-wise addition of 0.5 M HCl until pH = 7.0 was
reached (equilibrium for 30 min). Specific surface area (SSA) was
measured via nitrogen adsorption (Autosorb 6, Anton Paar, Austria) and
calculated according to the BET model [25]. Particle size distribution
(PSD) was measured via laser diffraction in ddH2O (Mastersizer 3000
with Hydro EV dispersion unit, Malvern, UK). A few drops of iso-prop­
anol were added as dispersant to facilitate the separation of agglomer­
ated oil-wet reservoir rock grains. Because the iron-bearing minerals
siderite and pyrite were identified as major leachable components in
reservoir rock samples via XRD-XRF, iron content was measured in RS
and SC with both a photometric assay according to Klueglein and Kap­
pler [26] and XPS, a surface-sensitive analysis with penetration depths
~ 10 nm. For the photometric assay, 500 mg of rock sample was incu­
bated under anaerobic conditions in 6 M HCl (60 ◦ C, 24 hrs) and the
absorbance of the 0.2 µm-filtrated supernatant was measured after the
addition of ferrozin at λ = 562 nm. Increase in pore volume (PV) due to
dissolution of Fe-bearing minerals in reservoir rock sandpacks was
calculated from the iron mass balance.
2.2. Fluids, nutrients and microorganisms
Injection water and crude oil (µ = 43.4 ± 1.8 mPas at 37 ◦ C, MCR
301, Anton Paar, Austria) for the sandpack experiments were obtained
from the same oilfield as the rock samples. All aqueous fluids were
handled anoxically in a glove box (N2:H2-97:3 vol-%, Coy, USA). In­
jection water was passed through a sterilized 10–15 µm filter prior to
use. Water salinity is 168.3 ± 3.0 g*L-1 Total Dissolved Solids (TDS) with
an average pH ~ 6.3 and an ionic strength of 3.4 M (see Table S1 for the
ionic composition).
The injection water was also used as microbial inoculum for all ex­
periments and comprises, among others, fermentative bacteria of the
order Halanaerobiales. These were identified as potentially beneficial
for oil recovery in the studied oilfield [21] and perform mixed-acid
fermentation of low-molecule carbohydrates to acetate, lactate, carbon
dioxide, hydrogen and, to a lesser extent, formate. Although Halaner­
obium sp. present in our system did not show any sulfidogenic or cor­
rosive capacity as recently reported [27,28], sulfate-reducing bacteria
(SRB) potentially were potentially able to grow on metabolites produced
by Halanerobium sp. [29,30]. Hence, molybdate was used preventively
as a specific SRB inhibitor. The nutrient solution was prepared as 100x
stock in ddH2O and contained sucrose (technical grade, Südzucker,
Germany), dried yeast extract (technical grade, Springer, Germany), and
molybdate (Na2MoO4, Sigma-Aldrich, Germany) to a final concentration
of 5 g*L-1, 1 g*L-1 and 0.5 mM, respectively. All experiments were per­
formed at reservoir temperature (37 ◦ C). Nutrient stock solutions and
MES buffer were deprived of oxygen by nitrogen purging (30 min) or
degassing under vacuum.
2.3. Preparation of sandpacks and experimental procedure
The sandpack experiments were set up and sterilized as described in
[31]. All experiments were conducted under anaerobic conditions under
near-atmospheric pressure (~500 mbar; back pressure regulator: BOLA,
F. Kögler et al.
Germany). Initial growth experiments were performed without oil in
sandpacks with quartz sand (QS) and reservoir rock (1:1 wt% mixture of
SC and RS, labeled SC-RS). After inoculation with injection water, nu­
trients were injected with a piston or a HPLC pump (Labotron, Wagner,
Germany) for 7–10 days with a constant, reservoir-representative
interstitial velocity (~0.5–0.8 m*d-1 ~ 3–4 PV*d-1, Fig. 1, Figure S2).
MEOR two-phase experiments were conducted in duplicates with SC and
RS as porous media. Here, nutrients were injected continuously at
remaining oil saturation after waterflooding with flow rate similar to the
growth experiments (0.5–0.8 m*d-1, Fig. 1).
Differential pressure was monitored along the length of the sand­
packs (Aplisens, Poland) and volumes of produced oil and gas were
measured with a modified burette (WITEG, Germany; ± 0.05 mL,
Figure S2). The bulk volume of produced oil was also measured photo­
metrically by dissolving the oil sample in a known volume of cyclo­
hexane (ratio towards oil ≥ 10:1) and measuring the absorbance of the
resulting solution at a wavelength of 780 nm with a spectrophotometer
(Infinite M1000 luminometer, Tecan, Switzerland) versus a calibration
curve. Permeability was calculated according to the Darcy equation for
laminar and linear flow (Eq. 1) where q is the volumetric flow rate
[ml*sec-1], µ is the dynamic fluid viscosity [cP], A is the cross-sectional
area [cm2], Δp the differential pressure [atm], Δl is the length along the
differential pressure Δp [cm] and k the Permeability in [D].
qμΔl
k=
AΔp
the permeability reduction factor (PRF́ ) as an indication for bio­
plugging was calculated from the effective water permeability before
and after microbial stimulation, kW [D and kWF [D]; water saturation
after nutrient stimulation, SWF [%], was normalized to SW [%] before
nutrient stimulation to minimize the change in water saturation during
MEOR experiments (Eq. 2).
kW SWF
PRF‘ = * (2)
kWF SW
Correlation coefficients ρX,Y were calculated according to Pearson
(Eq. 3) and corresponding determination coefficients (R2) were obtained
by method of least squares. x‾ and y‾ donate mean values of the cor­
responding variable.
∑
(x − x)(y − y)
ρX,Y = √̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅
̅ (3)
∑ ∑
(x − x)2 (y − y)2
Fig. 1. Experimental procedure of growth experiments (green arrows; QS and SC-RS) and MEOR two-phase experiments with remaining oil (black arrows; RS and
SC). The injected volume is given in pore volumes (PV); duration [d] and injection velocity [m*d-1] of the experimental steps is given in brackets. (For interpretation
of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fuel 290 (2021) 119973
2.4. Chemical and microbiological analysis
Gaseous metabolites produced in the sandpacks were collected in the
outflow (Figure S1) and analyzed via GC (490 Micro GC, Agilent, USA).
Filtered liquid samples (0.22 µm, Millex, Millipore, USA) were analyzed
for organic acids, alcohols and substrate concentration via HPLC (pre-
column: Cation H; column: Aminex HPX-87H, 300 × 7.8 mm (Biorad);
eluent 5 mM H2SO4). The microbial community was identified via Illu­
mina MiSeq with universal primers covering the 16S rRNA gene of both
bacteria and archaea. Operational taxonomical units (OTUs) were binned
at a 97% identity cut-off. Samples for DNA isolation (Fast DNA spin kit
for soil, MP Biomedicals, USA) were taken after the experiments directly
from the porous medium either near the inlet and the outlet (comple­
mentary denaturating gradient gel electrophoresis, DGGE) or from the
central parts of the sandpacks (Illumina) and compared to liquid samples
from injection water or batch experiments. For DGGE, DNA was
amplified by PCR using universal primers targeting the 16 s rRNA gene
and amplicons were separated according to their base sequences on
polyacrylamide gels with a chemical gradient of 30–70% urea [32],
sequenced via Sanger-sequencing and aligned using the BLAST algo­
rithm and the NCBI database [33,34].
3. Results
(1) 3.1. Geochemical and petrophysical characteristics of sandpacks before
MEOR
Reservoir sandstone (RS) and quartz sand (QS) samples differed only in
their accessory mineral composition with QS containing mainly oxides
and feldspar whereas RS contained sulfates (gypsum, CaSO4), carbon­
ates (calcite and siderite) and sulfides (pyrite) (Table 1). The main
carbonate phase in siderite-cemented reservoir sandstone (SC) sandpacks
was siderite (FeCO3). Concentration of surface iron measured by XPS
was approximately 1.5 - fold and 10 - fold higher in SC samples and RS
samples, respectively, compared to their bulk iron content (Fig. 5).
Specific surface area (SSA) correlated positively with cumulative car­
bonate and sulfide content with ρ = 0.90 (R2 = 0.81) whereas the cor­
relation between SSA and clay mineral content was minor (ρ = 0.59, R2
= 0.35).
3.2. Fermentative microbial growth in sandpacks
Sucrose consumption and acetate production as well as petrophysical
parameters after microbial growth and / or MEOR are summarized in
Table 2. The permeability reduction factor ́ (PRF́ ) suggested a permeability
3
F. Kögler et al. Fuel 290 (2021) 119973

Table 1 microbially produced acids, as the addition of a pH buffer in QS sand­

Initial properties of sandpacks. Errors represent the range between independent packs led to a complete metabolization of the provided sucrose (Fig. 2).
duplicate experiments. Mineralogical components represent mean values from In contrast, a pH ≥ 5.3 was maintained for 30 PV injected nutrients
triplicate XRD-XRF measurements. BDL: Below detection limit. SC: Siderite- with continuous acetate production in SC-RS and SC sandpacks and even
cemented reservoir sandstone. SC-RS: Mixture of RS and SC (1:1- wt%). RS: a cumulative production of 184.8 mmolAcetate*kg-1 Rock did not exceed the
Reservoir sandstone. QS: Quartz sand.
acid neutralization capacity ANC in SC-RS sandpacks (Fig. 3). Once the
SC SC-RS RS QS ANC of 1.0 ± 0.0 mmolH+*kg− 1 and 4.5 ± 0.5 mmolH+*kg− 1 was
Quartz, wt-% 62.6 ± 9.4 81 ± 2.0 96.6 ± 2.1 92.7 ± 5.9 exceeded, pH decreased drastically in sandpacks QS and RS, respectively
Oxides, wt-% 0.7 ± 0.1 0.9 ± 0.1 BDL 4.2 ± 0.3 (Fig. 3). In RS sandpacks, fermentative activity as indicated by elevated
Clay Minerals, wt-% 6.3 ± 0.3 3.8 ± 0.5 2.0 ± 1.8 0.8 ± 1.4 CO2 production rates still remained high for more than 10 IPV of nu­
Carbonates, wt-% 22.0 ± 3.3 11.7 ± 1.0 0.6 ± 0.1 BDL
trients, before the low pH inhibited microbial activity as indicated by a
Feldspar, wt-% 2.9 ± 1.4 2.0 ± 0.7 BDL5 2.8 ± 4.9
Sulfides, wt-% 0.9 ± 0.3 0.6 ± 0.2 0.6 ± 0.3 BDL buildup of effluent sucrose (IPV 23–36, Fig. 4).
Sulfates, wt-% 0.3 ± 0.6 0.3 ± 0.0 0.3 ± 0.6 BDL
Other, wt-% BDL5 BDL5 BDL5 0.7 ± 0.2
Permeability k, mD 945 ± 219 2466 ± 907 10,250 ± 354 5138 ± 1482 3.3. MEOR in sandpacks and mineral dissolution porous media
Porosity Φ, % 36.1 ± 4.6 37.3 ± 3.6 40.9 ± 5.5 42.6 ± 0.4
Pore Volume, mL 35.4 ± 4.5 36.6 ± 3.5 40.1 ± 5.4 41.8 ± 0.4
Because of the low microbial activity in the QS sandpacks without an
SSA1, m2*g− 1 5.8 ± 1.4 4.3 ± 1.0 2.0 ± 0.6 0.6 ± 0.0
dv502, µm 244 212 180 180 additional pH buffer, only RS and SC were considered for further MEOR
dv102, µm 15 10 5 100 experiments. Due to slightly different growth dynamics, exemplary ex­
SOI6, % 67.0 ± 9.1 n.a.4 88.4 ± 1.3 n.a.4 periments are shown in Fig. 4. Increased CO2 production and depletion
ROS7, % 38.6 ± 2.6 n.a.4 39.4 ± 2.5 n.a.4 in effluent sucrose indicate the activity of fermentative bacteria. Overall
FOS3, % 24.1 ± 1.5 n.a.4 17.8 ± 10.7 n.a.4
trends with respect to incremental oil, permeability reduction PRF́ and
1
Specific Surface Area. sucrose consumption rate qS are still comparable for each porous me­
2
10% / 50% of particles are below the given equivalent diameter. dium as seen in Table 2.
3
Final oil saturation after MEOR. Most significant incremental oil recovery from sandpacks SC and RS
4
n.a.: Not applicable (experiments without oil). was observed during the early MEOR or nutrient injection phase be­
5
Below detection limit in all measurements.
6 tween 10 and 20 injected pore volumes (IPV, Fig. 4). At that point, only
Initial oil saturation after oil flooding.
7 little amounts of sucrose were metabolized and bacterial activity is
Remaining oil saturation after water flooding.
mainly indicated by a pH decrease and accompanied by a slight decrease
in relative water permeability. In RS sandpacks with a permeability of
Table 2 10.3 ± 0.3 D, the continuous consumption of sucrose resulted in CO2
Sandpack parameters after microbial growth. If given, errors represent the mean production rates up to 10.9 mmolCO2*d-1 and a parallel reduction in
values of independent duplicate experiments. n.d.: Not determined. n.a.: Not water permeability was observed (26–30 IPV, Fig. 4), potentially
applicable. induced by multi-phase flow of water, oil and gas. In contrast, decrease
SC5 SC-RS RS5 QS Batch1 in relative water permeability and complete metabolization of influent
sucrose did not occur simultaneously in the lower-permeable SC sand­
Injected nutrients, 11–40 26 24–38 25 n.a.
PV packs with k = 0.9 ± 0.2 D: After a “chemostat”-like phase between
Incubation time, d 8–10 8–10 8–10 8 7 IPV 18–38 characterized by constant pH, sucrose concentration and
qS6, mMSucrose*d-1 4.5 ± 0.3 4.5 ± 1.6 3.7 ± 2.2 0.6 2.5 water permeability, a sudden decrease in water permeability was
q7A, mMAcetate*d-1 25.9 ± 6.3 23.5 ± 18.8 ± 4.3 10 observed approximately 1.5 d before most of the provided sucrose is
3.8 12.7
PRF́ 3, - 3.1 ± 0.0 2.6 ± 0.1 1.0 ± 0.2 1.1 n.a.
consumed after 44 IPV. This erratic permeability decrease correlated
IRFOOIP2, % 21.9 ± 4.7 n.a. 24.5 ± 9.6 n.a. n.a. with the production of minor amounts of incremental oil.
Decrease in SSA, % 43 ± 16 n.d. 17 ± 7 2±1 n.a. The net amount of dissolved ferrous iron during MEOR experiments
PV increase5, % 0.42 ± 0.26 ± 0.13 ± n.d. / n. n.a. increased with the cumulative amount of microbially produced acetate
0.16 0.11 0.02 a..
which suggests the dissolution of Fe-bearing minerals (Figure S2).
q7Acetate: Maximum acetate production rate. Dissolution rates were highest at the beginning of the nutrient injections
and the dissolution of 1–2 * 10-2 mmolFe * g-1Rock also led to a significant
1
Static and anaerobic conditions with 100 mL nutrient solution MES as pH
buffer, no solid phase. mobilization of 10–20 %OOIP remaining oil in MEOR experiments. At
2
Recovery factor with respect to the original oil in place. that point, ~ 9 g acetate were cumulatively produced per liter pore
3
Permeability reduction factor, kW/kWF.
5
volume (Figure S2). Iron removal from the porous medium was further
Multiphase MEOR experiments with crude oil.
6 confirmed by measuring the superficial iron content after the MEOR
qSucrose: Maximum sucrose consumption rate.
experiments by XPS (Fig. 5). In RS sandpacks, both bulk and surface iron

reduction in SC and SC-RS sandpacks with a permeability < 3 D while

7 6
significant permeability change was observed for QS and RS sandpacks
Effluent Sucrose [g/L]

with a permeability greater than 5 D (Table 2).

Effluent pH

4
Despite their different carbonate content of 22.0 ± 3.3% and 11.7 ± 5
1.0%, microbial growth as indicated by maximum sucrose consumption 2
(qSucrose) and acetate production rates (qAcetate) was highest in sandpacks
with reservoir rock SC and SC-RS, respectively. qSucrose in QS sandpacks 3 0
with pure quartz sand was 7–8 ten times lower, only 0.6 mMSucrose*d-1. 0.0 10.0 20.0 30.0 40.0 50.0
Injected Volume [PV]
Despite the similar bulk mineralogy between QS and RS sandpacks,
QS, pH SC-RS, pH Start nutrient injection
sucrose consumption rates in RS sandpacks with only accessory amounts Addition pH buffer QS, Sucrose SC-RS, Sucrose
of pyrite and calcite was still six times higher at 3.7 ± 2.2 mMSucrose*d-1
compared to QS sandpacks (Table 2). In QS sandpacks, continuous Fig. 2. Sucrose consumption and pH in a sandpack with quartz sand (QS, k ~
fermentative growth was likely inhibited by the pH drop induced by 4.5 D) and crushed reservoir rock (SC-RS, k ~ 3.5 D). One-phase growth ex­
periments (no oil phase). Interstitial velocity ~ 0.5 m*d-1 or ~ 2.5 PV*d-1.

4
F. Kögler et al. Fuel 290 (2021) 119973

7
ANC1 pHRock2 pHEnd3

RS 44.5 ± 0.5 8.5 ± 0.1 4.3

SC 325.0 ± 0.0 7.7 ± 0.1 5.4

pH

5 QS 1.0 ± 0.0 6.8 ± 0.8 4.0

SC-RS 184.8 ± 0.3 8.1 ± 0.1 5.2

4
0 30 60 90 120 150 180
Cumulative Acetate [mmol*kgRock-1]

Fig. 3. Outflow pH plotted against the total amount of acetate produced during microbial fermentation in sandpacks. In total, ~ 30 PV nutrients were injected. 1Acid
neutralization capacity (ANC) in [mmolH+*kg-1 2 3
Rock]. pHRock: Initial pH of the corresponding material. pHEnd: Final outflow pH.

RS 12 7.0 100 6 7.0 100

SC

CO2 Production [mmol*d-1]

CO2 Production [mmol*d-1]

(A) 10 6.5 80 (A) 5 6.5 80

Sucrose [%-IF]
Sucrose [%-IF]
8 6.0 4 6.0
60 60

pH
6 3 5.5
pH

5.5
40 40
4 5.0 2 5.0
20 1 4.5 20
2 4.5
0 4.0 0 0 4.0 0
0 10 20 30 40 50 60 0 10 20 30 40 50 60
80 1E+01 (B) 80 1E+01

Water Permeability kW/k [-]

(B)
Water Permeability kW/k [-]
Oil Saturation [%]

60 60
Oil Saturation [%]

1E+00 1E+00

40 40

1E-01 1E-01
20 20

0 1E-02
0 1E-02
0 10 20 30 40 50 60
0 10 20 30 40 50 60
IPV
IPV
Oil Saturation Water Permeability Oil Saturation dp -HI- Water Permeability
CO2 Production Sucrose pH CO2 production Sucrose pH

Fig. 4. MEOR sandpack experiments with crushed reservoir sandstone (RS, grey, upper left), reservoir sandstone with siderite cement (SC, red, upper right). The
highlighted background marks sucrose injection phases which are preceded and followed by waterflooding. Differential pressure above the measuring range of the
transmitters is indicated with dashed lines (dp -HI-). Interstitial velocity was ~ 0.7 m/d (3 PV/d). Representative single experiments are shown. (For interpretation of
the references to colour in this figure legend, the reader is referred to the web version of this article.)

content decreased only insignificantly after MEOR and a change in bulk the families Deferribacteraceae and Desulfohalobiaceae, respectively
iron could not be detected (Fig. 5). However, XPS measurements in SC (Fig. 6). The target microorganisms for MEOR, phylogenetically affili­
sandpacks with considerable siderite cement clearly revealed significant ated to the Halanaerobiaceae and Halobacteroidaceae, represented ~ 25%
dissolution of superficial iron minerals, as the surface iron content of detected sequences. After the MEOR experiments, overall species
decreased by the factor of two after the experiments (Fig. 5). Similar to richness in SC and RS sandpacks decreased significantly and relative
the RS sandpacks, this drastic change of pore surface mineralogy could abundances of Halanaerobiales increased to ≥ 85%. The relative
not be resolved by bulk iron measurements. These results are in line with abundance of all other taxa declined, except for Oceanospirillales
the decrease in SSA after microbial growth in sandpacks which ranged –related sequences making up 9.8% in RS and 2.9% in SC sandpacks
from no significant decrease in SSA in QS (2.2 ± 1.3%) to 43 ± 16% in (Fig. 6). Taxonomic differences between low-permeable SC sandpacks
SC sandpacks (Table 2). The calculated pore volume increase due to and high-permeable RS sandpacks were observed on a family level:
dissolution of iron minerals was calculated to be 0.13 ± 0.02, 0.26 ± 45.4% of sequence reads found in the SC sandpacks were assigned to the
0.11 and 0.42 ± 0.16% for sandpacks RS, SC-RS and SC, respectively. Halobacteroidaceae which made up only 9.8% of the total community in
RS sandpacks (Fig. 6).
Complementary DGGE analysis yielded congruent results: Hala­
3.4. Microbial community shift after MEOR
naerobiaceae genes were found in both sandpacks whereas Halobacter­
oidaceae specific sequences were found only near the inlet region of the
Illumina sequencing of 16 s rRNA genes isolated from the injection
low-permeable SC sandpacks. These were assigned to Orenia salinaria,
water revealed a diverse halophilic microbial community of archaea
exclusively (99% similarity at 398 bp read length). DGGE also indicated
(Methanosarcinaceae) as well as iron- and sulfate-reducing bacteria of

5
F. Kögler et al. Fuel 290 (2021) 119973

SC 25.0 RS 5.0
20.0 4.0

Fe, wt-%
Fe, wt-%
15.0 3.0
10.0 2.0
5.0 1.0
0.0 0.0
before before
after MEOR after MEOR
MEOR MEOR
XRD (bulk) 6.8 ± 1.6 n.d. XRD (bulk) 0.3 ± 0.1 n.d.
Photometric (bulk) 6.7 ± 0.6 6.5 ± 0.6 Photometric (bulk) 0.3 ± 0.1 0.3 ± 0.1
XPS (surf.) 10.6 ± 0.4 5.7 ± 0.5 XPS (surf.) 4.1 ± 0.6 3.4 ± 1.0

Fig. 5. Superficial (XPS, grey) and bulk (XRD, blue; photometric, orange) iron content (Fe) of sandpacks with crushed siderite-cemented reservoir sandstone (SC,
left) and crushed non-cemented reservoir sandstone (RS, right) before and after MEOR. Iron content from XRD data was calculated from FeS2 and FeCO3 only since
these were identified as the dominant Fe-bearing mineral phases. Analysis were performed in triplicates. n.d.: Not determined. (For interpretation of the references to
colour in this figure legend, the reader is referred to the web version of this article.)

4.1. Shift of the microbial community after MEOR

Halanaerobiales: Halobacteroidaceae*
100%
Isolated 16S rRNA genes from the injected water and from sandpacks
Halanaerobiales: Halanaerobiaceae*

Desulfovibrionales: Desulfohalobiaceae
after MEOR imply that the microbial community drastically changed
Deferribacterales Deferribacteraceae due to the injection of nutrients. Halanaerobiales dominated the com­
80%
Oceanospirillales: Alteromonaceae, munity with more than 85% relative abundance, compared to 25% in
the injection water. As fermentation is a very fast and productive process
Halomonadaceae
Spirochaetes

Pseudomonadaceae [35], other microorganisms with slower non-fermentative metabolic

60% pathways present in the injection water, such as methanogenic archaea
Comamonadaceae
and iron-reducing bacteria, were apparently vastly outcompeted. The
Burkholderiales
reasons for the slight enrichment of Oceanospirillales including Hal­
Staphylococcaceae
40% omonas taeanensis remain speculative: H. taenensis is described as a
Bacillaceae
motile bacterium growing under aerobic conditions and able to utilize
Cyanobacteria nitrate [36]; other Halomonas species were also shown to degrade hy­
20% Ectothiorhodospiraceae drocarbons [37]. Chemotaxis might have been an advantage compared
Gammaproteobacteria to the non-motile Halanaerobium sp. in sandpacks, because it would
Thermotogales Thermotogaceae allow H. taenensis to actively move to regions with potential nutrients
0% Clostridiales and electron acceptors (i.e. crude oil, traces of oxygen or nitrate). The
Injection RS SC Archaea: Methanosarcinaceae
carbonate-rich and “low permeable” SC and carbonate-lacking and high-
Water permeable RS sandpacks were similar on an order level, indicating that
Other
fermentative activity of the Halanaerobiales is not directly susceptible to
Fig. 6. Relative microbial abundance [%] as determined by Illumina the carbonate content, but only to the resulting equilibrium pH in the
sequencing before (Injection Water) and after MEOR (RS, SC). Taxa containing pores. However, slight differences on a family level could imply addi­
the MEOR target species stimulated by the injected nutrient are marked with an tional links to geochemistry or permeability: Orenia salinaria specific
asterisk (*). Other: OTUs with a relative abundance < 1%. SC: Reservoir DNA sequences were only found near the injection vicinity of the lower-
sandstone with siderite cement; RS: Non-cemented reservoir sandstone after permeable SC sandpacks (k ~ 1 D). Because it is both relatively large
microbial stimulation in sandpack experiments.
6–10 µm and susceptible to a pH < 5.5 [38], growth in RS sandpacks and
distant parts of the SC sandpacks was potentially prevented by the low
the presence of Halomonas taeanensis in the RS sandpacks. Halomonas sp. pH (RS) or insufficient propagation (SC).
belong to the Oceanospirillales which were also detected in these sand­
packs via Illumina sequencing. The other sequences retrieved by DGGE
could be assigned to Halanaerobium praevalens (99% similarity at 389 bp 4.2. Mineral dissolution by microbially produced acids
read length) and Halanaerobium saccharolyticum (99% similarity at 456
bp read length). Minor Illumina reads were assigned to sequences spe­ The decrease in SSA in sandpacks RS and SC in conjunction with the
cific to Deferribacteraceae (~0.2% in both sandpacks) and Ectothio­ observed production of organic acids strongly suggests mineral disso­
rhodospiraceae (0.1–0.8%). lution. Clay minerals found in each rock type typically exhibit a very
high SSA and readily interact with microbes: Microbially produced
4. Discussion organic acids are known to enhance mineral weathering rates [39] and
Deferribacteraceae found in RS and SC sandpacks comprise several spe­
The growth of a halophilic microbial oil reservoir community was cies of iron-reducing bacteria known to interact with iron-bearing clay
triggered by the injection of sucrose-amended injection water into minerals [40]. However, we have no evidence for a significant impact of
sandpacks set up with quartz sand (QS) and a mixture of two reservoir microbial growth on clay minerals as no change in permeability or
lithologies. In addition, MEOR experiments at remaining oil saturation specific surface was observed for QS sandpacks with a clay content of
were performed with the reservoir lithologies SC and RS. 0.8 ± 1.4%. The increase in ferrous iron with cumulative acetate pro­
duction rather suggests a “leaching” of siderite and pyrite in RS and SC
sandpacks. The strong correlation between SSA decrease and cumulative
carbonate / sulfide content indicates that these reactive minerals

6
F. Kögler et al.
provided the main mineral-pore contact boundaries during the experi­
ments. It is known that such accessory minerals can provide most of the
fluid-rock contact [13]. The decrease in iron dissolution rates with
progressing experiment time and cumulatively produced acetate might
imply the loss of these reactive surfaces [41], further indicating super­
ficial mineral dissolution. Finally, this conclusion is supported by the
decrease of surface iron content after MEOR experiments measured by
XPS. These dissolution processes could not be resolved via the change in
bulk mineral content which underlines that knowledge of the spatial
mineral distribution is important when pore-fluid interactions are to be
investigated.
The highest iron dissolution rates coincided with the major amount
of incremental oil production during the early tertiary phase of the
nutrient injection. Oil production was negligible once 9 gAcetate per liter
pore volume were cumulatively produced (Figure S2). This corresponds
to a complete turnover of 8 PV of nutrients for the maximum MEOR
effect, much less than the total volume of nutrient volume injected into
the sandpacks. Similarly, recent results from Chinese field trials reported
that small slug sizes of 0.1 PV were sufficient for successful MEOR [42].
Compared to conventional acid treatments commonly used to improve
near-wellbore oil and gas flow [43], weak organic acids such as acetate
have the additional advantage of longer reaction times, thus allowing
deeper propagation into the reservoir [44]. Although the mineral sur­
face of reservoir rock samples was partly oxidized, restoration protocols
were deliberately not applied, because these can alter the geochemistry
to even less reservoir-representative conditions [45]. Instead, “fresh”
mineral surfaces were exposed by crushing the samples. Yet, the
resulting surface areas is higher than in the original sample and the
pore – solid contact of minor mineral components can be unrepre­
sentatively increased. This could lead to potential overestimations of
reaction rates and also, incremental oil recovery.
4.3. Relevance of mineral dissolution and buffering minerals for
fermentation-Based MEOR
If mineral dissolution is one of the main MEOR mechanisms, oil
would be mobilized via i) an increase of the pore throat radii (likely to be
a relevant process in water-wet porous media where oil is trapped in
larger pore bodies) or ii) by a wettability alteration due to dissolution of
pore surface minerals (more likely in oil-wet reservoirs where residual
oil adheres to the rock surface). The calculated porosity increase was
highest for SC sandpacks with 0.42% after MEOR. Such relatively small
changes in porosity can significantly change fluid flow through porous
media. For example, Zhu, Carlson and Coates [46] demonstrated the
potential of microbially induced mineral precipitation for MEOR in a
dual-permeability column system with nitrate-reducing Fe2+-oxidizing
bacteria. A porosity decrease of 0.9–1.4% was sufficient to produce
significant incremental oil. However, the porosity change was not
spread over the whole column but predominantly plugged the inlet. In
our sandpacks, dissolvable minerals were evenly distributed. In partic­
ular for the RS sandpacks with 98% quartz, the calculated porosity in­
crease of 0.13% would translate only into a marginal increase of the pore
throat radii would. Therefore, wettability alteration seems to be the
more plausible mechanism, especially considering that wettability
alteration after the growth of Halanerobium sp. was detected within this
project [47]. Furthermore, relative permeability curves obtained from
sandpacks also indicate wettability alteration towards more water-wet
conditions [31]. Time-resolved visualization of surface dissolution on
the pore scale could further fortify this conclusion, e.g. by using non-
inert calcite micromodels [48,49].
Lazar [50] already considered the presence of carbonates as essential
for successful MEOR and our data strongly support this hypothesis:
Although the mineral content of carbonates and sulfides was only 1.2%
in RS sandpacks, sucrose consumption rates were only insignificantly
lower compared to SC and SC-RS sandpacks, but six times higher than in
QS sandpacks without carbonate. In our study, 17 PV of nutrients were
7
Fuel 290 (2021) 119973
injected before the acid neutralization capacity (ANC) of 44.5 mmolH+ *
kg− 1 (~120 mmolH+ * L-Rock1) in RS sandpacks was reached. This cor­
responds to the amount of acetate needed in this study for significant
incremental recovery (~150 mmolAcetate or 9 gAcetate*L-1 PV). Within a pH
range of 4–8.5, approx. 1.5–2 mol protons are released for each mole of
fermented sucrose yyyy[51]. Hence, comparing the ANC of a given
reservoir rock to the expected proton production during fermentation -
based MEOR might provide an additional screening parameter to better
predict its feasibility. Our findings suggest that only very little amounts
of pH buffering minerals are needed in a reservoir rock to sustain long-
lasting fermentative growth on a field scale. Yet, these must be
accounted for in laboratory experiments, as seen by the QS sandpacks.
These represented a very poor reservoir analogue for studying
fermentation-based MEOR for two main reasons: Firstly, dissolution of
pore surfaces as a potential mechanism for incremental oil cannot be
accounted for. Secondly, fermentative microbial growth could not be
sustained due to the rapid pH drop.
5. Conclusion
Our findings suggest that successful MEOR is highly dependent on
the mineralogy of the reservoir and that a critical amount of pH-
buffering minerals should be present during fermentation-based
MEOR. These minerals include, but are not limited to, carbonates and
sulfides. In dynamic sandpack experiments, a cumulative amount of
only 1% calcite and pyrite was sufficient to buffer the pH during mi­
crobial fermentation and resulted in sucrose consumption and acetate
production rates which were almost two-fold higher compared to batch
incubations and six times higher than in quartz sand sandpacks. A car­
bonate content of ~ 12% proved sufficient to maintain a favorable pH
for the continuous growth of fermentative bacteria over at least 30 pore
volumes of injected nutrients or 180 mmolAcetate*kg-1 Rock. The ~
16–25 %OOIP incremental oil produced from sandpacks with crushed
reservoir rock were partly attributed to superficial mineral dissolution.
Quartz sand proved to be a very poor analogue to crushed reservoir rock
because the growth of acid-producing bacteria was inhibited by a
massive pH drop. Therefore, experimental results obtained with lithol­
ogies differing from the reservoir composition must cautiously be
transferred to oil field conditions. Our results suggest that fermentation-
based MEOR can be an efficient tertiary oil recovery technology in
reservoirs containing non-inert minerals. However, the presence of pH-
buffering minerals can be considered as a prerequisite for a successful
application and can be assessed by the acid neutralization capacity of
the rock as an additional screening parameter for MEOR.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
We appreciate the funding and permission of Wintershall Dea to
conductand publish this project. The authors would like to thank Sab­
rina Reimann and Sabine Schatzmann and their respective colleagues
from Wintershall Dea in Barnstorf for supplying reservoir rock und fluid
samples. Special thanks go to for providing reservoir fluids. Philipp
Aurin is thankfully mentioned for the XRD and XRF analysis. The BASF
analytics laboratory is acknowledged for HPLC analysis and SSA mea­
surements. Holger Hartmann is acknowledged for bioinformatics. The
BASF surface physics department is thankfully mentioned for XPS
analysis, especially Sabine Hirth and Roelf-Peter Baumann.
F. Kögler et al.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.fuel.2020.119973.
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