Microaeration For Hydrogen Sulfide Removal During Anaerobic Treatment: A Review

Rev Environ Sci Biotechnol (2015) 14:703–725
DOI 10.1007/s11157-015-9386-2
REVIEW PAPER
Microaeration for hydrogen sulfide removal

during anaerobic treatment: a review
Lucie Krayzelova . Jan Bartacek . Israel Dı́az . David Jeison .
Eveline I. P. Volcke . Pavel Jenicek
Published online: 14 November 2015

Springer Science+Business Media Dordrecht 2015
Abstract High sulfide concentrations in biogas are a (microbiology, chemistry) of microaeration and the
major problem associated with the anaerobic treat- key technological factors influencing microaeration.
ment of sulfate-rich substrates. It causes the corrosion Other aspects such as process economy, mathematical
of concrete and steel, compromises the functions of modelling and control strategies are discussed as well.
cogeneration units, produces the emissions of unpleas- Besides its advantages, the limitations of microaera-
ant odors, and is toxic to humans. Microaeration, i.e. tion such as partial oxidation of soluble substrate,
the dosing of small amounts of air (oxygen) into an clogging the walls and pipes with elemental sulfur or
anaerobic digester, is a highly efficient, simple and toxicity to methanogens are pointed out as well. An
economically feasible technique for hydrogen sulfide integrated mathematical model describing microaera-
removal from biogas. Due to microaeration, sulfide is tion has not been developed so far and remains an
oxidized to elemental sulfur by the action of sulfide important research gap.
oxidizing bacteria. This process takes place directly in
the digester. This paper reviews the most important Keywords Anaerobic digestion Biogas Elemental
aspects and recent developments of microaeration sulfur Hydrogen sulfide removal Microaeration
technology. It describes the basic principles Sulfide oxidizing bacteria
L. Krayzelova (&) J. Bartacek P. Jenicek Abbreviations

Department of Water Technology and Environmental ABR Anaerobic baffled reactor
Engineering, University of Chemistry and Technology
Prague, Technicka 5, 166 28 Prague 6, Czech Republic BTF Biotrickling filter
e-mail: [email protected]; [email protected] CSTR Continuous stirred tank reactor
DO Dissolved oxygen
L. Krayzelova E. I. P. Volcke EGSB Expanded granular sludge bed
Department of Biosystems Engineering, Ghent
University, Coupure Links 653, 9000 Ghent, Belgium FBR Fluidized bed reactor
IC Internal circuit reactor
I. Dı́az MDU Microaerobic desulfurization unit
Department of Chemical Engineering and Environmental ORP Oxidation–reduction potential
Technology, University of Valladolid, Calle
Dr. Mergelina, 47011 Valladolid, Spain PID Proportional-integral-derivative
SCADA Supervisory control and data acquisition
D. Jeison SOB Sulfide-oxidizing bacteria
Departamento de Ingenierı́a Quı́mica, Universidad de La SOU Sulfide-oxidizing unit
Frontera, Casilla 54-D, Temuco, Chile
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704 Rev Environ Sci Biotechnol (2015) 14:703–725
SRB Sulfate-reducing bacteria demanding and expensive (Appels et al. 2008). In

TN Total nitrogen contrast, biological methods based on the biochemical
UAF Up-flow anaerobic filter oxidation of sulfide to sulfate, thiosulfate and elemen-
UASB Up-flow anaerobic sludge blanket reactor tal sulfur involve lower operational costs with lower or
VFA Volatile fatty acid no need for chemical addition (Buisman et al. 1989;
Syed et al. 2006). Biological removal of H2S from
biogas in closed anaerobic reactor (or digester)
requires an electron acceptor. Therefore, a small
amount of pure oxygen or air must be provided into
the reactors for biological desulfurization.
1 Introduction Among the biological desulfurization methods,
microaeration has recently gained growing attention.
Under anaerobic conditions, dissimilatory sulfate- With microaeration, most authors refer to controlled
reducing bacteria (SRB) use sulfate as the terminal dosing of small amount of air/oxygen into the liquid or
electron acceptor for the degradation of organic gaseous phase of anaerobic digesters (Fig. 1). This
compounds while producing hydrogen sulfide (H2S). method is reliable, simple and economically efficient.
H2S ends up in both the liquid effluent and biogas However, it has also some potential drawbacks such as
formed through the anaerobic digestion of organic partial oxidation of soluble substrate or clogging the
material. High concentrations of hydrogen sulfide in walls and pipes with elemental sulfur which are
biogas reduce its quality, since it causes corrosion of discussed later in this manuscript. This contribution
concrete and steel, compromises the functions of reviews the important aspects of biological removal of
cogeneration units, produces emissions of unpleasant sulfide during anaerobic treatment. Particular attention
odors, is toxic to humans and generates emissions of is paid both to the basic principles of sulfide oxidation
sulfur dioxide during combustion. In addition, the (microbiology, chemistry) and the technological factors
presence of sulfide in the liquid phase causes corrosion influencing this process. The need for further develop-
of water transport systems and the accumulation of ments of microaeration, such as mathematical model-
inert material in the sludge (e.g. metal sulfides). ing, is discussed as well. Furthermore, the challenges
Moreover, sulfide is toxic to methanogens (already at and advantages of biological oxidation of sulfide are
concentrations above 50 mg L-1) and may cause the described, including economic considerations.
inhibition of anaerobic processes (Buisman et al.
1990a; Hao et al. 1996; Hulshoff Pol et al. 1998;
Khanal and Huang 2003b; Stucki et al. 1993; Zhou
et al. 2007). For all of these reasons, the production of 2 Terminology
sulfide is a major problem associated with the
anaerobic treatment of sulfate-rich wastewater and The action of dosing small quantities of air into the
organic wastes. bioreactor is referred to by different terms in literature,
Available methods for sulfide removal from biogas such as ‘‘microaeration’’ (Duangmanee et al. 2007;
can be classified into physico-chemical and biological Jenicek et al. 2008, 2010, 2013; 2014; Krayzelova
methods, as summarized in Table 1. Many commer- et al. 2014a; Tang et al. 2004; Tartakovsky et al.
cial technologies are available on the market, such as 2011), ‘‘limited aeration’’ (Zhou et al. 2007; Zitomer
SulfaTreat (solid scavenger, iron sponge technol- and Shrout 2000), ‘‘aeration’’ (Bekmezci et al. 2011;
ogy), SOXSIA (sulfur oxidation and siloxane Ikbal et al. 2003; Lohwacharin and Annachhatre
adsorption), THIOPAQ (physical–chemical absorp- 2010), ‘‘microoxygenation’’ (Dı́az and Fdz-Polanco
tion with biological regeneration), DMT Sulfurex 2012; Dı́az et al. 2011a, b; Fdz-Polanco et al. 2009;
(water scrubber), Sulfur-rite (iron sponge technol- Ramos et al. 2012; Ramos and Fdz-Polanco 2013,
ogy), and Media-G2 (iron sponge technology). 2014; Ramos et al. 2013, 2014b, c), ‘‘oxygenation’’
Operation at high temperature and pressure, as well (Khanal and Huang 2003a, b; 2006; Khanal et al.
as the need for additional equipment and chemicals, 2003) or ‘‘moderate oxygenation’’ (van der Zee et al.
make physico-chemical methods energetically 2007).
123
Table 1 The summary of physico-chemical and biological desulfurization methods others than microaeration
Physico- Reagent Parameters Situation Additional comments References
chemical
methods
Precipitation Iron chloride solution Small scale anaerobic digester For liquid sulfide Kapdi et al. (2005)
Petersson and Wellinger (2009)
Scrubbing Sodium hydroxide High pressure drop (high contact Lab-scale two-stage co-current For gaseous H2S Couvert et al. (2008)
surface), long residence times contactor (scrubber) Large volume contactors
Physical Water Pressurizing of biogas Counter-current packed column High water consumpion Kapdi et al. (2005)
absorption For simultaneous removal of Wellinger and Lindberg (1999)
H2S and CO2
Chemical Iron-chelated Room temperature Lab-scale counter-current gas–liquid For gaseous H2S Horikawa et al. (2004)
absorption solutions Low gas pressure 1.2–2.2 bar contactor
Sodium hydroxide For gaseous H2S Petersson and Wellinger (2009)
For very large gas volumes or

high H2S concentrations
Chemical Iron oxides, iron Temperature 25 C Lab-scale upward or downward flow For gaseous H2S Kohl and Nielsen (1997)
‘‘dry’’ sponge Pressure less than 2 kPa gas–solid contactors (semi-batch) limited regeneration McKinsey Zicari (2003)
adsorption (19 - 29)
Temperature 40 C Usually two reaction beds Capacity 1000 Nm3 gas h-1 Petersson and Wellinger (2009)
Atmospheric pressure Limited regeneration Wellinger and Lindberg (1999)
Activated carbon Temperature 50–70 C Usually two vessels for continuous For gaseous H2S Bandosz (2002)
(AC) Pressure 7–8 bar system Limited regeneration Wellinger and Lindberg (1999)
300 mg H2S per 1 g of AC Impregnation of AC needed
Biological Electron acceptor Dominant microorganisms Situation Additional comments References

methods
Biochemical Oxygen (pure O2 or SOB such as Thiobacillus sp., Digester For gaseous and liquid H2S Petersson and Wellinger (2009)
oxidation air) Sulfolobus sp.
SOB such as Thiobacillus sp., Trickling filter with packing material For gaseous H2S Petersson and Wellinger (2009)
Sulfolobus sp.
Thiobacillus sp. Biological filter (combination of water For gaseous H2S Wellinger and Lindberg (1999)
scrubbing and biological oxidation)
Thiobacillus sp. Lab-scale fixed-film bioreactors For gaseous and liquid H2S Gadre (1989)
Jensen and Webb (1995)
Nitrite Lab-scale batch bioreactor For liquid sulfide Mahmood et al. (2007)
Nitrite Chemolitotrophic enrichment Lab-scale batch bioreactor For liquid sulfide Cardoso et al. (2006)
culture
Pure culture of Thiomicrospira sp. Lab-scale batch and continuous For liquid sulfide Gadekar et al. (2006)
CVO bioreactor
705
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In this paper, the process of biological oxidation of

sulfide is called ‘‘microaeration’’ if air was used for the
oxidation of sulfide and ‘‘microoxygenation’’ if pure
oxygen was used instead. As for the amount of air/
oxygen dosed, we follow the criteria shown in Fig. 2.
The term ‘‘microaerophilic’’ is used only to refer to
microorganisms.
The concentration of dissolved oxygen (DO) is not
a good control parameter for the microaeration process
since the formation of elemental sulfur or sulfate
proceeds at DO concentrations below 0.1 mg L-1,
which is the lowest detection limit of commonly
available oxygen electrodes (Janssen et al. 1995). The
Fig. 1 The scheme of possible application of microaeration in oxidation–reduction potential (ORP) could make up a
anaerobic digesters with biogas and sludge recirculation: better control parameter to characterize microaerobic
A dosage in the liquid phase, B dosage in the gas phase, systems. However, a wide range of ORP values have
C dosage in the biogas recirculation been reported during microaeration: lower than
-460 mV (Duangmanee et al. 2007); -320 to
The terms ‘‘microaeration’’ or ‘‘microoxygenation’’ -270 mV (Nghiem et al. 2014); -265 mV (Khanal
reflect (in most cases) the gas used. I.e. when air is and Huang 2003b, 2006; Khanal et al. 2003); -230 to
dosed into the anaerobic reactor, the process has been -180 mV (Khanal and Huang 2003a); 0 to -200 mV
called ‘‘microaeration’’, and when pure oxygen is (Kobayashi et al. 2012); and higher than -150 mV
used, the term ‘‘microoxygenation’’ has been applied. (Xu et al. 2012). This large variation is probably
However, this has not been a strict rule and not all caused by the uniqueness of each system and its
authors follow it. operational conditions. Moreover, it is often not clear
Besides, it should be noted that the terms ‘‘mi- whether the results are expressed as ORPH (with
croaerobic’’ (Dı́az and Fdz-Polanco 2012; Dı́az et al. hydrogen electrode as reference) or as ORPAg (with
2011a, b; Ramos et al. 2012, 2014b, c; Ramos and Fdz- argent chloride electrode as reference).
Polanco 2013, 2014) or ‘‘microaerophilic’’ (Fdz-
Polanco et al. 2009; Chu et al. 2005) are also applied
to denote the reactor conditions (bulk liquid oxygen 3 Principles of microaeration
concentrations) as such, and at the same time referring
to the act of oxygen dosage as ‘‘microoxygenation’’. To understand the effect of oxygen dosage, it is
When referring to microaeration, the amount of necessary to understand the nature of both biological
oxygen is crucial. Several terms have been used when and chemical oxidation of sulfide. The most important
referring to the action of dosing oxygen to a culture. bioconversions involved in aerobic sulfide removal are
Authors were using the term ‘‘aeration/oxygenation’’ (Buisman et al. 1990b; Chen and Morris 1972; Janssen
if the dose of oxygen was as high as 102–218 et al. 1995; Kuenen 1975):
L O2 L-1 feed (Bekmezci et al. 2011). For the amount
of oxygen between 2.6 and 6.4 L O2 L-1 feed
(Lohwacharin and Annachhatre 2010) or 5.1 (Zhou
et al. 2007), the authors used prefix ‘‘limited’’. Prefix
‘‘micro’’ was used when the amount of oxygen was
0.03–1.27 L O2 L-1 feed (Dı́az and Fdz-Polanco
2012; Dı́az et al. 2010, 2011a, b; Fdz-Polanco et al.
2009; Jenicek et al. 2014; Krayzelova et al. 2014a;
Rodriguez et al. 2012). However, van der Zee et al.
(2007) used the prefix ‘‘moderate’’ for 0.74–0.94 Fig. 2 The terminology for air/oxygen dosing based on the
L O2 L-1 feed. amount of oxygen dosed
123
Rev Environ Sci Biotechnol (2015) 14:703–725 707
2HS þ O2 ! 2S0 þ 2OH increased up to 2, sulfide was completely oxidized to

ð1Þ sulfate. At O2/S2- as low as 0.15 mol/mol, the activity
DG ¼ 169:35 KJ mol1
of sulfide-oxidizing severely decreased. According to
2HS þ 4O2 ! 2SO2 þ the authors, it was probably related to an oxygen
4 þ 2H
1 ð2Þ limitation in the culture which promoted sulfide
DG ¼ 732:58 KJ mol
accumulation in the reactor (Alcántara et al. 2004).
2HS þ 2O2 ! S2 O2 At the ratios between 0.25 and 0.35 thiosulfate was
3 þ H2 O
ð3Þ detected in the culture. On the other hand, Dı́az et al.
DG ¼ 387:35 KJ mol1
(2011a) observed an increase in S2O32- concentration
The biological removal of hydrogen sulfide (H2S) is when increasing oxygen rate from 9.3 to
based on the biochemical oxidation of sulfide to 14.1 L day-1. This indicated a slight overdose of
elemental sulfur (S0) or/and sulfate (SO42-). Some oxygen.
authors (Dı́az et al. 2011b; van den Ende and van Munz et al. (2009) observed that in some cases,
Gemerden 1993) have also reported the production of there is less than 0.5 mol O2/mol S2- necessary for
thiosulfate (S2O32-). Sulfide serves as the electron successful oxidation of sulfide to elemental sulfur.
donor while oxygen serves as the terminal electron Authors observed 91, 87, and 85 % of sulfide being
acceptor. Under oxygen limiting (microaerobic) con- converted to elemental sulfur at O2/S2- ratio of 0.015,
ditions, at oxygen concentrations below 0.1 mg L-1, 0.005, and 0.03 mol/mol, respectively. Also, they
sulfur is the major end-product of the sulfide oxidation observed a strong effect of pH on the sulfide oxidation.
(Eq. 1), with a partial oxidation to thiosulfate (van den The maximum elemental sulfur production decreased
Ende and van Gemerden 1993). Sulfate is formed with increasing pH (from 85–91 to 53–59 % at pH 8
under sulfide limiting conditions and implies higher and 9, respectively).
oxygen consumption per mole of sulfide (Eq. 2). According to Klok et al. (2013) biological oxida-
Chemical oxidation of sulfide, resulting in the formation of sulfide significantly depends on the concentra-
tion of mainly thiosulfate (Eq. 3) (Janssen et al. 1995) tion of sulfide. Sulfide oxidizing activity increased at
becomes important when biological activity of sulfide sulfide concentrations from 0 to 0.15 mmoL L-1. At
oxidizing bacteria is limited. This is the case espe- concentrations from 0.3 to 1.0 mmoL L-1, biological
cially in bioreactors highly loaded with sulfide. In such activity gradually decreased and increased again at
cases when oxygen is not consumed fast enough by sulfide concentrations from 1.0 to 5.0 mmoL L-1.
sulfide oxidizing bacteria, the chemical oxidation of This was most likely the result of bacteria adaptation
sulfide to thiosulfate becomes significant. From the to high sulfide concentrations. Buisman et al. (1990a)
economical point of view, sulfur formation is pre- observed that the contribution of chemical oxidation
ferred, since it can potentially be recovered. Besides, of sulfide was larger when sulfur loading rate
the lower amount of oxygen needed for the oxidation increased.
to sulfur compared to sulfate implies lower energy
consumption.
The formation of sulfur and sulfate can be con- 4 Microorganisms involved in microaeration
trolled by the amount of oxygen supplied (Janssen
et al. 1995). Theoretically, 0.5 mol O2/mol S2- is Sulfide-oxidizing bacteria (SOB) are the main group
necessary for the oxidation of sulfide to elemental involved in sulfide oxidation under microaerobic
sulfur (Eq. 1). According to Janssen et al. (1995) a conditions. In general, SOB are photoautotrophs or
maximal sulfur production of 73 ± 10 % occurred at chemolithotrophs. Photoautotrophs use CO2 as the
an O2/S2- consumption ratio in the range of 0.6–1.0 terminal electron acceptor while chemolithotrophs use
(mol L-1 h-1)/(mol L-1 h-1) with 0.7 as the opti- oxygen (aerobic species) or nitrate and nitrite (anaer-
mum. According to Alcántara et al. (2004), sulfur- obic species). As microaeration always takes place in
producing steady states were achieved at O2/S2- ratio dark anaerobic fermenters, photoautotrophs cannot be
ranging from 0.5 to 1.5. The maximum elemental involved in the process. Also, present paper focus on
sulfur formation (85 % of the total influent sulfur) the dosing of limited amount of air or oxygen into an
occurred at the ratio of 0.5. When the ratio was anaerobic reactor, therefore, chemolithotrophs using
123
nitrite or nitrate as an electron acceptor will not be to participate on the oxidation of sulfide were of genus
discussed. Thiomicrospira (Gadekar et al. 2006), Thiomonas (Ng
In terms of energy and carbon sources, SOB can be et al. 2004), Thiothrix (Cytryn et al. 2005; Maestre
classified into four groups: (1) obligate chemolitho- et al. 2010) with the specific species of Thiothrix nivea
trophs, (2) facultative chemolithotrophs, (3) (Prescott et al. 2002), Sulfurimonas with the specific
chemolithoheterotrophs, and (4) chemoorganohetero- species of Sulfurimonas denitrificans (Maestre et al.
trophs (Tang et al. 2009). Obligate chemolithotrophs 2010), and Acidithiobacillus with the specific species
need CO2 as carbon source and an inorganic energy of Acidithiobacillus thiooxidans (Lee et al. 2006).
source. All known Thiomicrospira sp., many
Thiobacillus sp., and at least one Sulfolobus sp. belong 4.1 SOB found in anaerobic reactors subjected
to this category (Kuenen and Veldkamp 1973; Matin to microaeration
1978). Facultative chemolithotrophs can grow either
chemolithoautotrophically with an inorganic energy Most of SOB found in microaerobic reactors for
source and CO2 as carbon source, or heterotrophically biogas production belong to phylum Proteobacteria
with organic compounds as carbon and energy source. or, exceptionally to phylum Actinobacteria. Haloth-
Some Thiobacilli sp., certain Beggiatoa, Thiosphaera iobacillus sp., Acidithiobacillus sp., and Sulfuri-
pantotropha, and Paracoccus denitrificans are typical curvum sp. were the most frequently cited species
examples of facultative chemolithotrophic SOB (Frie- (Table 2). SOB were found almost exclusively in the
drich and Mitrenga 1981; Nelson and Jannasch 1983). headspace of the reactors or in the gas–liquid inter-
Chemolithoheterotrophs such as a few Thiobacillus phase suggesting that sulfide oxidation took place
sp. and some Beggiatoa strains generate energy from there.
oxidation of reduced sulfur compounds. Che- Tang et al. (2004) observed a shift in the archaea
moorganoheterotrophs can oxidize reduced sulfur population as the consequence of the introduction of
compounds without deriving energy from them. microaeration. The size of Methanosarcina sp. pop-
Thiobacterium, Thiothrix, and some Beggiatoa sp. ulation was reduced, while the size of Methanoculleus
belong to this last group (Larkin and Strohl 1983). sp. population increased. In contrast, Ramos et al.
As far as pH and temperature are concerned, the (2014c) did not observe any particular impact on any
requirements of various SOB species are diverse. of the archaeal populations while changing from
Growth at pH values in the range 1–9 and temperatures anaerobic to microaerobic environment.
ranging from 4 to 90 C have been reported (Tang
et al. 2009). The majority of known chemolithotrophic
SOB are mesophilic, Thiobacillus being the only 5 Technological and physical factors influencing
genera encompassing both mesophilic and ther- microaeration
mophilic environments. Other important thermophilic
genera are Sulfolobus and Thermothrix. 5.1 Oxygen dosing point and mixing method
The most cited species of SOB found for the
oxidation of sulfide was Thiobacillus sp. (Alcántara 5.1.1 Air dosing point
et al. 2004; Annachhatre and Suktrakoolvait 2001;
Maestre et al. 2010; Ravichandra et al. 2006) of Number of authors compared the efficiency of
Hydrogenophilaceae family (Luo et al. 2011), specif- microaeration when air is dosed into the headspace
ically Thiobacillus denitrificans (Krishnakumar et al. or into the liquid phase of anaerobic digesters (Fig. 1).
2005; Lee and Sublette 1993; Ma et al. 2006; When dosed into the headspace, oxygen can directly
Ongcharit et al. 1990), Thiobacillus nivellus (Myung react with gaseous hydrogen sulfide and, therefore, the
Cha et al. 1999), Thiobacillus baregensis (Vannini amount of air needed per given amount of hydrogen
et al. 2008), Thiobacillus thiooxidans (Takano et al. sulfide is minimized (Dı́az et al. 2011b; Ramos et al.
1997) and Thiobacillus thioparus (Vlasceanu et al. 2012). This is important, because dosing lower amount
1997). SOB of Halothiobacillaceae family were of air induce lower contamination of biogas by
observed by Vannini et al. (2008) (Halothiobacillus nitrogen. On the other hand, when air is overdosed
neapolitanus) and Luo et al. (2011). Other SOB found in order to assure complete H2S removal, the excess
123
Table 2 Sulfide oxidizing bacteria found in anaerobic reactors subjected to microaeration

Genus Phylum Location Aeration References
gas
Acidithiobacillus thiooxidans Proteobacteria Bottom of biotrickling filter Air de Arespacochaga

et al. (2014)
Arcobacter, Sulfuricurvum e-Proteobacteria Headspace, liquid O2 Ramos et al. (2014a)
Acidithiobacillus c-Proteobacteria interphase
Acinetobacter c-Proteobacteria Headspace
Rhodococcus Actinobacteria
Acinetobacter, Arcobacter, Proteobacteria Microaerobic O2 Ramos et al. (2013)
Sulfuricurvum desulfurization unit
Halothiobacillus neapolitanus, Proteobacteria Headspace Air Kobayashi et al.
Sulfurimonas denitrificans (2012)
Halothiobacillus, Thiofaba c-Proteobacteria Headspace O2 Rodriguez et al.
(2012)
Acidithiobacillus thiooxidans, Proteobacteria Headspace (reactor with O2 Dı́az et al. (2011b)
Arcobacter mytili, sludge recirculation)
Halothiobacillus neapolitanus,
Thiomonas, Thiobacillus,
Sulfuricurvum kujiense
Halothiobacillus kellyi Headspace (reactor with
Arcobacter mytili biogas recirculation)
oxygen will contaminate biogas (Dı́az et al. 2010, 5.1.2 Mixing method
2011b).
When air is dosed into the sludge, the intense The contact between oxygen and liquid phase is also
contact between oxygen and the liquid phase will intensified in digesters mixed by biogas recirculation.
facilitates non-specific oxidation of degradable Analogically to dosing air into the liquid phase, this
organic compounds, i.e. some losses of oxygen. This will increase the consumption of oxygen due to the
will increase the necessary air dosage and, hence, the reaction with organic compounds. Again, sulfide
contamination of biogas by nitrogen. Potentially, concentration in the liquid phase is decreased due to
certain part of organic load can be oxidized along the intensified contact between oxygen and the liquid
with sulfide, but the decrease of methane yield due to phase (Dı́az et al. 2011a, b; Fdz-Polanco et al. 2009).
this oxidation is usually negligible (Krayzelova et al.
2014a). 5.2 The location of sulfide oxidation and sulfur
Dosing air into the liquid phase also causes the accumulation
decrease of sulfide concentration in the liquid phase
(Dı́az et al. 2011b; Krayzelova et al. 2014a; van der For a proper design of microaeration, it is important to
Zee et al. 2007; Zhou et al. 2007). However, this find out where the oxidation of sulfide occurs, i.e.
decrease is usually only about 20–30 % (Krayzelova whether it takes place in the biofilm covering the wall
et al. 2014a) and cannot explain the large decrease in of the gas phase or in the liquid phase. Results from
H2S concentration in biogas. This implies that major- numerous microbial analyses (Table 2) revealed that
ity of H2S oxidation takes place in the head space even SOB populations grow mainly on the walls of the
if air is dosed into the liquid phase. Besides H2S headspace (Dı́az et al. 2011b; Kobayashi et al. 2012;
removal from biogas, the decrease of sulfide concen- Ramos et al. 2014b; Rodriguez et al. 2012) or on the
tration in the liquid has the additional positive effect of gas–liquid interphase Ramos et al. (2014b) suggesting
decreasing sulfide toxicity towards methanogens. that biological oxidation of sulfide takes place there.
123
The intensity of microaerobic processes strongly concentrations detected in the effluent samples was
depended on the available surface area in the head- also observed by van der Zee et al. (2007).
space. Ramos et al. (2014a) operated a pilot reactor Additionally, sulfur deposition in the headspace
with variable size of headspace to investigate where was not reported when oxygen was sparged in fine
the process of biogas desulfurization predominantly bubbles into the bioreactors (Khanal and Huang
took place. In this study, oxygen was injected into the 2003a, 2006; Zitomer and Shrout 1998, 2000), thus
liquid phase. Hydrogen sulfide was entirely removed increasing oxygen transfer to the bulk liquid phase.
from the biogas when the digester had 25 L headspace Under such condition, sulfide oxidation seemed to take
and little or no H2S removal was observed when the place only in the liquid phase. Under this condition a
size of headspace was minimized to almost 0 L. significant consumption of oxygen for aerobic oxida-
Moreover, the deposition of elemental sulfur in the tion of organic matter was observed and SOB were
headspace could represent a clear indication that the found in the sulfur mats formed in headspace walls.
oxidation takes place there (Ramos et al. 2012). This may indicate that oxidation of organic matter out-
Kobayashi et al. (2012) observed the accumulation of competed the development of SOB in the liquid phase
microbial mats, containing elemental sulfur as the (Khanal and Huang 2006; Zitomer and Shrout 2000).
dominant component, on the inner walls of a reactor The problems associated with elemental sulfur depo-
headspace including ceiling, wall, net, and catwalk. sition on reactor walls and pipes will be discussed
Also Ramos et al. (2014b) and Rodriguez et al. (2012) further.
observed the elemental sulfur accumulation all over
the walls of the headspace. This indicates that the 5.3 Oxygen flow rate and biogas residence time
headspace of a bioreactor may act as a ‘‘biofilter’’, in headspace
where SOB can grow on all available surfaces. The
sulfur mats also serve as additional support material In general, bioreactors treating materials with low
where new microbial mats develop. Furthermore, COD/S ratios, such as wastewater from brewery, sugar
scanning electron microscopy revealed that these or paper industries (Table 3), produce large amounts
sulfur mats were formed mostly by upward filaments of hydrogen sulfide. As a result of low COD/S ratios,
(perpendicular to the gas–liquid interphase) creating a these wastewater streams have been shown to require
support with large specific surface. This may help higher amounts of oxygen per volume of biogas (Zhou
SOB in the competition for oxygen (Kobayashi et al. et al. 2007), in comparison to sewage sludge, agricul-
2012). tural wastes or manure. Normally, oxygen dosage (or
In contrast, Dı́az et al. (2011b) observed only partial equivalent air) between 0.3 and 3 % of produced
accumulation of elemental sulfur in the top of biogas in the bioreactor is enough to achieve efficient
headspace and on the walls while Dı́az et al. (2011b) biogas desulfurization (Table 3). However, oxygen
and Ramos et al. (2014c) did not observe any rate of up to 12 % may be necessary if both gaseous
accumulation of elemental sulfur in the headspace. and dissolved sulfide must be removed.
These authors suggested that the elemental sulfur The residence time of biogas in the headspace is a
formed in their reactors has most probably fallen into key factor affecting sulfide removal efficiency, when
the liquid effluent. However, this suggestion could not providing oxygen/air injection into the headspace.
be proved and it remains unclear why sulfur deposition Typically, removal efficiencies over 97 % were
on headspace walls was not observed in these cases. obtained with residence times over 5 h (Table 3).
According to Krayzelova et al. (2014a), only 10 % Schneider et al. (2002) found 88 % removal efficiency
of the produced elemental sulfur remained in the with a residence time of 2.5 h while it was lower than
headspace of a UASB reactor, while 33 % left the 40 % under 1.25 h. When the headspace was sup-
reactor with the liquid effluent. In this case, the small pressed totally, the concentration of hydrogen sulfide
headspace of UASB-type reactors was probably in biogas produced with microaerobic treatment was
responsible for the modest depositions of sulfur in similar to that found in unaerated digesters (Ramos
the headspace. Large range of elemental sulfur et al. 2014a).
123
5.4 Removal of gaseous and dissolved sulfide productivity was observed (Khanal and Huang 2006;
and influence of pH Zitomer and Shrout 1998) in this case.
At pH around 7, at which anaerobic digestion typically 5.5 Reactor configurations

occurs, HS- (d) and H2S(d) are the predominant sulfide
species in the liquid phase [pKa1 = 6.9, Migdisov Over the years, microaeration has been tested in
et al. (2002)]. The concentration of H2S(d) increases several different reactor configurations (Table 3).
when pH declines. Simultaneously, H2S distributes Reported configurations can be divided within two
between gas and liquid phases (dimensionless Henry’s categories; a first one where oxygen/air is directly
constant H = cG/cL = 0.5). Then, the value of pH supplied into the reactor where the whole anaerobic
influences sulfide distribution between liquid and gas digestion takes place, and, secondly, those configura-
phases and it is of particular importance when only tions which comprise a chamber or separate unit where
H2S(g) is removed by microaeration (i.e. by aerating microaeration is performed.
the headspace). Assuming a constant amount of sulfur
reduced by sulfidogenesis within the bioreactor, a 5.5.1 Microaeration directly inside anaerobic
lower pH results in a higher proportion of H2S(d), a digesters
higher amount of H2S(g) in the biogas to maintain the
Henry’s equilibrium and, consequently, requires a Within the first category, microaerobic H2S removal
larger oxygen/air rate for efficient H2S removal. has been traditionally used in digesters treating
In those processes where sulfide removal occurs in agricultural wastes in Germany because of the
the headspace, dissolved sulfide can be removed by simplicity of its application and the convenience for
increasing the contact between gas and liquid phases biogas exploitation (Schneider et al. 2002). However,
or by decreasing pH (to promote H2S stripping). the most reported and successful application, includ-
However, the required oxygen rate to remove both ing full-scale operation, is the digestion of sludge from
gaseous and dissolved sulfide species depends on the WWTP under microaerobic conditions. In fully-mixed
pH and the Qbiogas/Qeffluent ratio (m3 of biogas per m3 sludge digesters (10 L–2100 m3), microaeration can
of liquid effluent) in the bioreactor as shown in Fig. 3. remove H2S from biogas (2500–34,000 ppmv) with
Hence, at pH 7, the rate of oxygen needed to remove efficiency higher than 97 % (Dı́az et al. 2010; Fdz-
both gaseous and dissolved sulfide in digestion Polanco et al. 2009; Jenicek et al. 2008, 2010, 2014;
processes is lower than 1.3 times the rate necessary Ramos and Fdz-Polanco 2014). The lower efficiency
to remove exclusively gaseous sulfide with Qbiogas/ found on full-scale microaerobic CSTR treating
Qeffluent ratios larger than 15. This was confirmed by agricultural wastes, between 68 and 88 % (Kobayashi
switching from sludge to biogas recirculation (Dı́az et al. 2012; Schneider et al. 2002), is probably the
et al. 2011a, b; Fdz-Polanco et al. 2009) at pH close to consequence of the low biogas residence time in the
7 and Qbiogas/Qeffluent = 18. By contrast, processes headspace in comparison to sludge digesters (see
with Qbiogas/Qeffluent ratios below 5, such as industrial Sect. 5.3).
wastewater treatment (Krayzelova et al. 2014a; Recent research has broadened the usage of direct
Rodriguez et al. 2012), would require a much higher supply of oxygen to up-flow anaerobic sludge blanket
rate of oxygen to remove dissolved sulfide than it is (UASB) reactors, expanded granular sludge bed
needed for biogas desulfurization only, and this effect (EGSB) reactors, fluidized bed reactors (FBR) for
is larger when pH increases. Consequently, at high pH the treatment of industrial wastewaters; particularly
or low Qbiogas/Qeffluent, removing dissolved sulfide those from the brewery, sugar and paper industries that
may affect the profitability whether by raising the commonly present elevated sulfur load. The unaerated
costs of pure oxygen supply or by excessive biogas treatment of the wastewater of such industries resulted
dilution by nitrogen if air is used. This negative effect in a biogas with concentrations of H2S higher than
on the costs can be partially neutralized if severe 20,000 ppmv and up to 67,000 ppmv, which was
inhibition on digestion is prevented under microaer- removed with efficiencies between 70 and 82 % under
obic conditions, because a large increase in methane microaerobic conditions (Krayzelova et al. 2014a;
123
Table 3 The overview of anaerobic reactors where the use of microaeration has been reported
712
Reactor OLR Feed (COD:S ratio) Reactive (dosing point) Reactive flow rate O2:biogas O2:H2S(g)
ratio ratio
123
(volume in L) (gCOD L-1 day-1) (%) (mol mol-1)
Fully-mixed digester (10) 2 Sludge (40) Air (liquid) 1.6 L day-1 1.7–9.2 1.3–7.4
UASB (3) 8 Synthetic brewery ww (95) Air (liquid) 1 L day-1 2.5 3.9
Fully-mixed digester (70) 2.3 Sludge (72) O2 (liquid) ORP controlled (-320 to n.a. n.a.
-270 mV)
Fully-mixed digester (7000) 1.5–2.2 gVS L-1 day-1 Sludge (–) 92–98 % O2 (headspace or 5–34 Lm-3 day-1 1 0.9–2
liquid)
Fully-mixed digester (250) 1–1.9 gVS L-1 day-1 Sludge (–) O2 (headspace or sludge rec.) 1.8–19 Lbiogas m-3 0.33–0.5 1
-1 -1
Fully-mixed digester (250) 1.4–2.9 gVS L day Sludge (–) O2 (sludge rec.) 4.4–6.2 Lm-3 day-1 0.44–0.62 1.9–2.8
Fully-mixed digester (338,000) 40–66 Cow manure (–) Air (headspace) 1 % of biogas rate *1 1.8–4.4
gmanure L-1 day-1
Fully-mixed digester (265) n.a. Sludge (–) O2 (liquid) 0.16–0.46 LL-1
feed 0.9–2.5 2.5–7
EGSB (4) 0.5–3.1 Synthetic vinasse (12) O2 (liquid) 0.37 L day-1 4.7 1.7
Fully-mixed digester (250) 1.8–3.4 Sludge (48–93) O2 (headspace) 0.97 L day-1 0.6–12 2–3.4
Fully-mixed digester (250) 2.4–4.7 Sludge (96–188) O2 (headspace or sludge rec.) 0.25 LL-1
feed 1.4 1
-1
Fully-mixed digester (250) 1.9–4 Sludge (143–310) O2 (sludge rec.) 0.25 LL feed 1.2–1.5 1–1.4
-1
Fully-mixed digester (250) 1.9–4 Sludge (137–296) Air (sludge rec.) 1.27 LL feed 1.2–1.5 1–1.4
Fully-mixed digester 3.5 Sludge (–) Air (sludge rec.) n.a. 1.1 3.7
(2 9 1,500,000)
Fully-mixed digester (2,100,000) 3.5 Sludge (–) Air (sludge rec.) n.a. 2.9 5.5
Fully-mixed digester (250) 1.9–4.5 Sludge (152–369) O2 (headspace or sludge rec.) 2.6–4.8 L day-1 1.3–2.4 0.7–1.3
Fully-mixed digester (11) 3.5 Sludge (–) Air (sludge rec.) 1.1 L day-1 2.1 n.a.
CSTR ? SOU (92 ? 1) 1.2 Sludge (690) O2 (liquid) 7.2 L day-1 3 10–14
UASB (11) 2.8–12 Sulfite pulp mill ww. Air (liquid) 45–90 L day-1 n.a. n.a.
(45–60)
FBR (1.7) 3.5 Synthetic vinasse (144) Air (liquid) 1.2–1.5 L day-1 n.a. 440–560
UAF ? SOU (4.5 ? 2) 0.53–2.3 Synthetic ww. (9) O2 (liquid) ORP controlled (-275 to n.a. n.a.
gTOC L-1 day-1 -265 mV)
Fully-mixed digester (5) 1–8 gTS L-1 day-1 Synthetic waste (69) Air 7.5 % of evolved gas 1–2.1 n.a.
Fully-mixed digester n.a. Agricultural waste (–) Air (headspace) n.a. 0.3–0.4 1.3–1.7
Gas residence time in H2S(g) conc. without H2S(g) removal H2S(d) ? HS-
(d) removal Residual O2 in References
headspace microaeration efficiency efficiency biogas
(h) (ppmv) (%) (%) (%)
n.a. 13,000 C99 68 n.a. Jenicek et al. (2014)

n.a. 67,000 73 15 \0.1 Krayzelova et al. (2014a, b)
n.a. 6000 C99 n.a. 1–1.8 Nghiem et al. (2014)
Table 3 continued
Gas residence time in H2S(g) conc. without H2S(g) removal H2S(d) ? HS-
(d) removal Residual O2 in References
headspace microaeration efficiency efficiency biogas
(h) (ppmv) (%) (%) (%)
10 2500–4900 99 &0 \0.1 (Ramos et al. 2014b)

8 3300–5000 99 n.a. \0.1 Ramos and Fdz-Polanco (2014)
6 3400 90 &0 \0.03 Ramos and Fdz-Polanco (2013)
1.4 2000–4000 68 n.a. n.a. Kobayashi et al. (2012)
7.6–0.2 3500 0–99 n.a. 1–2 Ramos et al. (2012)
2.4 25,000 72 40 4.1 Rodriguez et al. (2012), Lopes
(2010)
7.1–8.6 3300–34,000 C97 67–96 0.2–1 Dı́az et al. (2011a)
6.3 13,000 C98 88 (biogas recirculation) 0.6 Dı́az et al. (2011b)
6.6 12,000 97.5 &0 1–1.4 Dı́az et al. (2010)

5.3 10,000 [99 &0 1–1.4 Dı́az et al. (2010)
n.a. 3300 99 n.a. n.a. Jenicek et al. (2010)
5–8 9000–10,000 [99 &0 (sludge recirculation) 0.3–4.8 Fdz-Polanco et al. (2009)
n.a. 1800–2600 [99 94 0.4–0.7 Duangmanee et al. (2007)
n.a. 5000–23,000 – 20–30 n.a. Zhou et al. (2007)
n.a. 0.71 mg-S day-1 [82 [52 n.a. van der Zee et al. (2007)
n.a. 78,000 [99 99 n.a. Khanal and Huang (2006)
n.a. 680 99 n.a. n.a. Ikbal et al. (2003)
2.5 2500 88 n.a. n.a. Schneider et al. (2002)
UASB up-flow anaerobic sludge blanket, EGSB expanded granular sludge blanket, CSTR continuous stirred tank reactor, FBR fluidized bed reactor, SOU sulfide oxidizing unit,
UAF up-flow anaerobic filter, n.a. not available
713
123
gases involved were determined (CH4, CO2, H2S, O2,

N2). The formation of a biofilm over the membrane
surface was observed on the biogas side, similar to that
formed on the surfaces of the headspace of anaerobic
reactors subjected to microaeration. On the other hand,
Camiloti et al. (2013, 2014) reported the application of
silicone tubes for the microaeration of the liquid phase
of anaerobic reactors for wastewater treatment. In this
case, a biofilm containing SOB was also formed,
which was identified as responsible for a large part of
the sulfur oxidation. The application of membranes
with selective permeability for oxygen represents a
great opportunity, since they may partially reduce the
dilution of the biogas with nitrogen, when air is used as
oxygen source. Moreover, membranes preventing
methane permeation would be required to avoid
Fig. 3 Theoretical oxygen rate requirements for the microaer- emissions of this gas to the atmosphere.
obic removal according to Eq. 1 assuming sulfide distribution
obeys Henry’s equilibrium. Oxygen rate to remove gaseous
sulfide only is 1 5.5.2 Microaeration in separate compartments
In the second category, a microaerobic unit (or

Rodriguez et al. 2012; van der Zee et al. 2007; Zhou compartment) is added to the process, thus maintain-
et al. 2007). Furthermore, microaeration can increase ing the core anaerobic digestion unaerated. This
the performance of the organic matter removal as a allows the utilization of higher O2 rates and avoids
result of the reduction of sulfide inhibition to the accumulation of elemental sulfur in the headspace
methanogens (Rodriguez et al. 2012; Zhou et al. of the anaerobic digester. Hence, anaerobic baffled
2007). An innovative approach of microaeration is the reactors (ABR) can be designed with a final compart-
application of water electrolysis within UASB reactors ment where microaeration is performed to remove the
so that O2 is produced directly in the reactor; H2S can H2S produced in the initial chambers under anaerobic
be removed and the production of H2 and the electrical conditions (Bekmezci et al. 2011; Fox and Venkata-
current significantly enhanced anaerobic digestion subbiah 1996). In a similar way, the sulfide-rich liquor
(Tartakovsky et al. 2011). and biogas, or the biogas alone, produced during
A novel, recently reported, configuration is the anaerobic digestion can be treated in a sulfide
application of membranes as a tool to provide required oxidation unit (SOU) where microaeration is per-
microaeration for sulfur oxidation. Membranes were formed. When liquid and biogas were introduced into
already conceived many years ago as a way to provide the SOU, increasing the ORP to around -265 from the
bubble-less aeration in fermentation processes (Cote natural anaerobic level of -290, H2S was removed
et al. 1988). However, only scarce reports are avail- with efficiency higher than 99 % (Khanal and Huang
able where membranes are used as a way to provide 2006). Alternatively, the raw biogas produced in the
aeration with the objective of sulfide oxidation. In digester can be treated in a SOU, inoculated with
principle, membranes could be used to transfer oxygen anaerobic sludge, which simulates the microaerobic
to the headspace or to the liquid phase of an anaerobic conditions within the headspace of digesters. In this
reactor. This would be accomplished by providing the way S0 can be easily removed without affecting the
flow of oxygen or air on one side of the membrane, and digester (Ramos et al. 2013).
exposing the other side to the biogas in the headspace
or the liquid phase of the reactor. Alvarez (2014) 5.6 Microaeration process control
studied the use of silicon tubing as a way to provide
microaeration to the headspace of an anaerobic A variable oxygen rate is necessary in most reactors,
reactor. Mass transfer coefficients for the different as the consequence of feed composition/rate variations
123
resulting in the varying production of sulfide. Besides, was 10 mV below the target value. Pure oxygen was
residual oxygen in the biogas must meet the require- injected to the reactor until ORP was raised to 10 mV
ments of the biogas utilization technology that will be above the target level. During the operation of the
employed afterwards. Oxygen content below 1 % is chemostat, a target ORP value of -230 mV (50 mV
required for fuel cells and below 3–0.5 % (after carbon above the anaerobic ORP level of -280 mV) almost
dioxide removal) for vehicle fuels or injection of completely removed the dissolved and gaseous sulfide
upgraded biogas into the natural gas grid (Petersson (Khanal and Huang 2003a). In the UAF, the target
and Wellinger 2009). Optimal process control is the ORP value of -265 mV (25 mV above the ORP level
key to the successful microaeration in such cases. of -290 mV) was set, which provided a dissolved
Oxygen supply can be controlled to cope with the sulfide removal over 98.5 %,by converting it mainly
changes of H2S concentration and biogas flow (Ramos to elemental sulfur with a production of small amount
and Fdz-Polanco 2014). Proportional-integral-deriva- of thiosulfate (Khanal and Huang 2003b, 2006;
tive (PID) controller was used to control the oxygen Khanal et al. 2003). ORP as a tool for controlling
flow rate according to the H2S concentration in biogas microoxygenation was also used by Nghiem et al.
(Ramos and Fdz-Polanco 2014). Oxygen flow rate was (2014). In their case, an ORP probe was connected to a
set according to the difference (e) between the supervisory control and data acquisition (SCADA)
measurement and target H2S concentration. H2S system to control the digester. SCADA system was set
concentration in biogas dropped below the set-point to control valve dosing oxygen to maintain ORP level
(0.01 %) in a time range from 4.0 to 5.5 h, subse- between -310 and -290 mV (the natural ORP level
quently stabilizing at zero, while oxygen content was -485 mV). Under such conditions, H2S concen-
remained around 0.05 %. The microoxygenation level tration decreased from over 6000 mg L-1 to just
was optimal since it kept the removal efficiency above 30 mg L-1.
99 % with a minimum oxygen concentration in No study was published that would use sulfide
biogas. The flow of biogas was another parameter concentration in the liquid phase as the control
used for the control of H2S concentration in biogas and parameter for the dose of air into the microaerobic
for the control of oxygen supply in this paper. reactor. This is most probably because the relation
Approximately 3.5 and 5.0 L of O2 per 1 m3 of biogas between H2S concentration in biogas and in the liquid
was needed to successfully remove 0.33 and 0.5 % of phase is not straightforward and large variations in
H2S from biogas, respectively. The average H2S H2S concentrations in biogas often correspond to
removal efficiency was 99 % with 0.08 % of oxygen small or negligible variations in the liquid phase. This
in biogas. Ramos and Fdz-Polanco (2014) suggested would largely depend on the oxygen dosing point (see
that biogas production could be an efficient regulating chapter 5.1). However, even if air is dosed directly into
parameter under variable organic loading rate and the liquid phase, the changes in H2S concentrations in
steady sulfur load, while under non-steady sulfur load, liquid phase are relatively small compare to the
H2S concentration should be used as a regulating changes in H2S concentrations in biogas.
parameter instead.
When using biogas production as a control param-
eter, there is a danger that overdosing by air would 6 Mathematical modelling of sulfide oxidation
increase apparent biogas production which would
induce the increase of air dosage. Therefore this Mathematical modelling is an important tool which
strategy would only work in the case when the changes can provide valuable information that can help to
in biogas flow are considerably greater than the understand the behavior of complex systems. There
potential overdose by air. This was the case of the are many papers describing the kinetics of chemical
study by Ramos and Fdz-Polanco (2014). oxidation of sulfide. The basic relation for the kinetic
ORP has also been used for the control of oxygen model can be expressed as follows (O’Brien and
dosing, in a chemostat (Khanal and Huang 2003a) and Birkner 1977):
a UAF system (Khanal and Huang 2003b, 2006;
Khanal et al. 2003). In general, oxygen injection was Rchem:ox: ¼ km ðSH2 S Þa ðSO2 Þb ð4Þ
automatically turned on whenever the reactor ORP
123
Table 4 The kinetic parameters of chemical oxidation of sulfide described by the Eq. 4
k (min-1) a b c (S2-) (mmoL L-1) c (O2) (mmoL L-1) References
17.46 1.02 0.80 0–5.00 0.15 Klok et al. (2013)a

0.1165 1.00 1.00 0.04–0.10 Saturated (25 C) Luther et al. (2011)
0.57 0.41 0.39 0.16–9.38 0.003–0.266 Buisman et al. (1990a)
0.055 0.38 0.21 0.09–0.30 0.16–0.62 Wilmot et al. (1988)
67.6 1.15 0.69 0.05–0.20 0.60 Jolley and Forster (1985)
1.44 1.02 0.80 0.02–1.21 0.21–1.10 O’Brien and Birkner (1977)
a
Measured in the gas phase
where Rchem:ox: is the sulfide oxidation rate (mmoL it is very hard to summarize the results and to make
L-1 min-1), km is the rate constant (min-1), SH2 S is the a unified conclusion.
H2S concentration (mmoL L-1), SO2 is the O2 Sharma et al. (2014) proposed the following kinetic
expression for chemical oxidation of sulfide:
concentration (mmoL L-1), a is the reaction order
SO2
with respect to the sulfide concentration (–), and b is Rchem:ox: ¼ km ðSH2 S Þa ð5Þ
the reaction order with respect to the oxygen concen- KO2 þ SO2
tration (–). with km being 4.46 h-1, a 0.56, and KO2 1.30 mg L-1.
The summary of available kinetic parameters and H2S oxidation rate was independent of the O2 concen-
the tested range of sulfide and oxygen concentra- tration at the O2 concentration above 5 mg L-1, which
tions are shown in Table 4. The parameters vary they explained by Monod type equation.
significantly across the literature. Different research- Nielsen et al. (2004) included the effect of pH and
ers used different analytical methods to determine temperature in their model of chemical oxidation of
sulfide and sulfide oxidation rate, and used different sulfide:
buffer solutions. Reported experiments were also k0 þ k1 K1 =SH þ
conducted at different sulfide and oxygen concen- Rchem:ox: ¼ ðSS2 Þa ðSO2 Þb hT20
1 þ K1 =SH þ
trations ranging from 0 to 9.38 and 0 to 1.10 mmoL
L-1, respectively. The reaction order of oxygen very ð6Þ
likely depends on sulfide concentration (Buisman where SS2 is the concentration of total sulfide
et al. 1990a). Due to the uniqueness of each system, (g m-3), k0 and k1 are the rate constants for the
Table 5 The kinetic parameters of biological oxidation of sulfide to elemental sulfur

bSOB lSOB Ks;S2 Ks;O2 YSOB Dominant microorganisms References
(day-1) (day-1) (mg S2- L-1) (mg O2 L-1) (mg 9 mg-1 S2-)
n.a. 0.67 11.00 0.0002 0.0900 (x = VSS) SOB from activated sludge Xu et al. (2013)
0.130 n.a. n.a. n.a. 0.0380 (x = COD) SOB of c-Proteobacteria and Munz et al.
Halothiobacillaceae class (2009)
0.034 8.64 63.68 n.a. 0.0006 (x = ATP) Thiomicrospira sp. Gadekar et al.
(2006)
n.a. n.a. 8.96 n.a. 0.0891 (x = protein) Thiobacilli sp. Alcántara et al.
(2004)
n.a. 7.20 0.32 n.a. 0.0969 (x = protein) Pure culture of De Zwart et al.
Thiobacillus thioparus (1997)
n.a. not available
123
oxidation of H2S and HS-, respectively (0.09 mg L-1) and then gradually decreased with
[(g S m-3)1-a (g O2 m-3)-b h-1], h is the Arrhenius continuously elevated DO levels. Therefore, the
constant, T is the temperature (C), and K1 is the first oxidation of sulfide under microaerobic (oxygen
dissociation constant for H2S (&1.0 9 10-7). The limited) conditions must be further studied.
reaction order a and b were 0.9 and 0.2 respectively, h Botheju et al. (2009) developed a model of oxygen
was 1.06, and k0 and k1 fluctuated from 0.02 to 0.08 effect in anaerobic digestion, however, the model
and from 0.25 to 1.00, respectively. The rate constants focused on aerobic oxidation of soluble carbon and
varied significantly and should be employed with inhibition of strict anaerobic organisms, not on sulfide
caution. Moreover, the rate equation is valid within the oxidation. Biomass dependent first order hydrolysis
pH and temperature intervals of 6–9 and 5–25 C, kinetics was used to relate increased hydrolysis rate to
respectively (Nielsen et al. 2004). oxygen induced increase in biomass growth rate
For biochemical oxidation of sulfide, Monod-type (Botheju et al. 2009, 2010). An integrated model
equation for substrate utilization should be used as describing the effects of microaeration on biological
follows (Xu et al. 2013): and chemical oxidation of sulfide in anaerobic diges-
dSS2 : l SS2 SO2 tion has not been addressed yet. Therefore, mathe-
¼ SOB XSOB matical modelling remains a research gap in
dt YSOB Ks;S2 þ SS2 Ks;O2 þ SO2
microaeration.
ð7Þ
where lSOB is the maximum specific growth rate (h-1),
YSOB is the yield coefficient for SOB (g VSS g-1 S2-), 7 Adverse effects of oxygen in anaerobic treatment
Ks;S2 and Ks;O2 are sulfide and oxygen affinity
constants (kg m-3), SS2 and SO2 are sulfide and 7.1 Oxygen toxicity to methanogens
oxygen concentrations (kg m-3), and XSOB is the
concentration of SOB (kg m-3). Strict absence of oxygen has previously been consid-
Xu et al. (2013) presented an integrated model ered as vital for anaerobic digestion, because of the
describing sulfur cycle processes of sulfate reduction, toxicity of oxygen to methanogens (Zehnder 1988).
sulfide oxidation and sulfur bioreduction. They found Later, methanogens were shown to be tolerant to
out that the ratio of oxygen to sulfide is a key factor for certain oxygen concentrations or protected by facul-
controlling elemental sulfur formation. tative anaerobic bacteria in both granular (Guiot et al.
Kinetic data for biological oxidation of sulfide 1992; Kato et al. 1993a, b; Shen and Guiot 1996) and
found in the literature are summarized in Table 5. suspended sludge (Estrada-Vazquez et al. 2003).
However, these kinetic studies were made in aerobic Methanogens in granular sludge appear to be more
environments. It has been reported that the maximum tolerant to the presence of oxygen than methanogens
specific activity for sulfide oxidation by SOB is in flocculent sludge. Based on the multilayer structure
different under aerobic and anaerobic conditions of anaerobic granular sludge, facultative anaerobes are
(McComas et al. 2001), i.e. 23.7 and 8.6 mg HS- predominant in the periphery of the granules, while
g-1 -1
protein min , respectively. Yu et al. (2014) studied oxygen-sensitive methanogens are located in the
the microbial community structures in a biological deeper layers, protected from the exposure to air
desulfurization reactor under microaerobic conditions (Guiot et al. 1992; Shen and Guiot 1996). In most
(0.02–0.33 mg L-1). The results indicated that the studies, no significant oxygen inhibition (Dı́az et al.
microbial community functional compositions and 2010, 2011b; Fdz-Polanco et al. 2009; Jenicek et al.
structures were dramatically altered with elevated 2011a, 2014; Krayzelova et al. 2014a; Nghiem et al.
dissolved oxygen levels. Genes involved in sulfate 2014; Ramos and Fdz-Polanco 2014; Tang et al. 2004;
reduction processes significantly decreased at rela- Zhou et al. 2007) of methanogens was observed during
tively high dissolved oxygen concentration (0.33 microaeration. Only two studies (Jenicek et al. 2010;
mg L-1), while genes involved in sulfur/sulfide oxi- Zitomer and Shrout 2000) reported slightly lower
dation processes significantly increased in low dis- specific methanogenic activity in microaerobic reactor
solved oxygen concentration conditions compared to anaerobic reactor.
123
7.2 Explosion risks of methane/oxygen mixtures volatile suspended solids removal (VSS). The evalu-
ation of side-effects of microaerobic sulfide removal
In general, mixing oxygen or air with biogas is during anaerobic digestion showed the decrease in
undesirable because of the increased explosion risks of VSS/TSS ratio of the digested sludge in all experi-
methane/oxygen mixture. However, the amount of ments with microaerobic conditions, due to its better
oxygen dosed in microaerobic digestion is very small VSS degradation (Jenicek et al. 2008).
and it is quickly consumed. Therefore, it is far from the
flammable range, which is typically 85–95 % of air 7.4 Clogging the walls and pipes of microaerobic
and 5–15 % of methane by volume (Appels et al. reactor with elemental sulfur
2008; Wase and Forster 1984). The leakage of biogas
in air should be considered as the higher threat According to some authors, microaeration takes place
compare to the mixing of a small amount of air/oxygen solely or almost solely in reactor headspace (Dı́az et al.
with biogas. During microaeration, the amount of 2011b; Kobayashi et al. 2012; Ramos et al. 2014b;
oxygen or air in biogas should never reach these Rodriguez et al. 2012). The whitish deposition of
values. Most authors mentioned almost no or very elemental sulfur on the walls and pipes can clog the
limited amount of oxygen detected in biogas during system resulting in headspace overpressure and biogas
microaeration (Krayzelova et al. 2014a; Ramos and leakage. de Arespacochaga et al. (2014) operated a
Fdz-Polanco 2013, 2014). Nonetheless, the explosion biotrickling filter with a solid oxide fuel cell for on-site
risk is always present when working with biogas and electricity and thermal energy production. Around
should not be underestimated. 70 % of H2S removal was done by partial oxidation to
elemental sulfur which increased the pressure drop
7.3 Partial oxidation of organic substrate over the column, reduced the availability of the
treatment line, and eventually led to a fuel cell
When oxygen is present in anaerobic treatment shutdown. A cleaning interval of less than 14 months
methanogenic substrates or methane can be partially is necessary to minimize microaeration costs (Ramos
oxidized. However, the oxygen dosing rate typically et al. 2014b). Ramos et al. (2014b) opened their
applied during microaerobic removal of sulfide microaerobic reactors, cleaned the surface of its
(0.001–0.01 kg m-3 day-1) and organic loading rate headspace, removed the liquid interface, and restarted
(ORL) of digesters expressed in COD in the same microaeration. Hydrogen sulfide removal was not
oxygen units (1–10 kg m-3 day-1) are three orders of affected, however, it was not clear which mechanism
magnitude different. Therefore, the amount of oxi- (biological or chemical oxidation) played the main
dized substrate cannot be significant. Some authors role in this set-up. The collection of elemental sulfur is
observed lower methane production in microaerobic a remaining challenge in microaeration technology
reactors compare to anaerobic reactors caused prob- and requires further research, especially in full-scale
ably by an aerobic degradation of organic matter applications.
(Khanal and Huang 2003a; Kobayashi et al. 2012;
Ramos and Fdz-Polanco 2013; Rodriguez et al. 2012). 7.5 Dilution of biogas by nitrogen from air
However, most authors report no or negligible
decrease of methane production due to microaeration By using air for microaeration, nitrogen will remain
(Dı́az et al. 2010, 2011a, b; Fdz-Polanco et al. 2009; and dilute biogas. This is especially challenging when
Jenicek et al. 2010; Krayzelova et al. 2014a; Nghiem biogas with low amount of methane (around 50 %) is
et al. 2014). In these cases the dose of oxygen was not produced, e.g. from lignocellulose (Chandraa et al.
controlled according to the sulfide content (or it was 2012), because then, even small dilution of biogas may
controlled very roughly by ORP). Therefore, oxygen complicate its further use in cogeneration unit. Celis
was apparently overdosed or digesters were in unbal- (2012) reported that when extremely high H2S
anced conditions which contributed to the decrease of concentrations (around 12,000 ppm) must be
methane production. removed, the concentration of N2 to increased up to
The partial oxidation of organic compounds in 20 % in biogas. It caused a decrease of methane
anaerobic digester can improve the efficiency of concentration below 50 % and such concentration is
123
too low for most cogeneration units. However, the 8.2 Better recovery from shock loading or serious
replacement of air by oxygen solved the nitrogen decrease of pH
dilution of biogas without affecting digestion and
desulfurization efficiency. Wang et al. (2014) described that microaeration was a
promising strategy to handle shock loading in anaer-
obic treatment of coal gasification wastewater. The
8 Additional advantages of microaeration recovery time was shortened from 23 to 11 days under
natural condition. Ramos and Fdz-Polanco (2013)
8.1 Enhancement of hydrolysis subjected microaerobic digester to a hydraulic over-
load. Microaeration improved the biogas quality and
Since hydrolysis is often considered as the bottle- oxygen seemed to contribute to a stable digestion
neck of the anaerobic digestion of solid materials system, which increased the ability to deal with
(Myint et al. 2007), improving this limiting step can overloads. Also Jenicek et al. (2010) observed faster
improve the whole process (Botheju and Bakke methanogenic bacteria recovery after the inhibition
2011). An adequate microaeration intensity can caused by overloading. Aero-tolerant methanogenic
significantly enhance the hydrolysis of carbohydrate culture was added to anaerobic digester to improve the
and protein in food waste by 21–27 and 38–64 %, recovery time after organic overload or toxicity upset
respectively (Xu et al. 2014). A sufficient microaer- (Tale et al. 2015). In contrast to the anaerobic
ation strategy should be employed during the early enrichment, the aerated enrichments were more
period of digestion to enhance the hydrolysis of effective, resulting in faster recovery of methane and
easily biodegradable organics, promote acidogene- COD removal rates.
sis, and avoid the accumulation of lactic acid (Zhu After a shock-load of sucrose, the pH in the
et al. 2009). Johansen and Bakke (2006) studied the complete-mix methanogenic reactors recovered more
effects of microaeration on hydrolysis of primary quickly under microaeration conditions (Zitomer and
sludge and observed 50–60 % increase in the rate of Shrout 1998). Aeration may prevent pH decreases in
the hydrolysis of carbohydrates and proteins. The other highly loaded systems since volatile acids were
extra hydrolyzed products were oxidized to carbon potentially oxidized and carbon dioxide and hydrogen
dioxide or incorporated into new biomass. The were stripped out. O’Keefe et al. (2000) observed no
increase of soluble proteins due to microaeration adverse effect of aeration on the microbial activities in
was also observed by Diak et al. (2013) together anaerobic digester.
with the increase of ammonia. Microaeration effec-
tively solubilized COD, and improved the subse- 8.3 Better sludge quality
quent degradation of COD. However, the increase of
carbohydrates was not observed. On the other hand, Microaeration also appeared to improve the quality of
Nguyen et al. (2007) reported no enhancement of the digested sludge in the way of lower foaming
hydrolysis by microaeration, but the applied amount potential and better dewaterability (Jenicek et al.
of air per kilogram of total solids per day was 109 2011a, b, 2014). The extent of foaming problems was
lower than in the study of Johansen and Bakke lower in microaerobic digester compare to anaerobic
(2006). digester.
Moreover, microaerobic assays presented shorter
lag-phase than the anaerobic assays in the study 8.4 Production of elemental sulfur
conducted by Dı́az et al. (2011c). This resulted in
faster production of methane during the first steps of As mentioned previously, there is a lack of technology
the cellulose degradation. The maximum methane available to recover elemental sulfur from bioreactors
production in the anaerobic assay was observed on day where microaeration is applied. However, if this
19 while in the microaerobic assay it was observed technology were to be developed, the elemental sulfur
before day 15. could be used in bioleaching processes (Tichý et al.
123
1994) or for the autotrophic sulfur-oxidizing denitri- wastewater treatment) and for optimization of
fication (Krayzelova et al. 2014b; Zhou et al. 2011). microaeration in current application (agricultural
The biologically produced elemental sulfur has some digesters).
distinctly different properties as compared to ‘‘nor-
mal’’ inorganic (orthorhombic) sulfur (Kleinjan et al. 10.1 Mechanism of sulfide oxidation
2003). The density of biologically produced sulfur is
lower and the particles have hydrophilic properties There is still discussion to what extend bacteria are
whereas orthorhombic sulfur is known to be responsible for the oxidation of sulfide under
hydrophobic with higher density. Due to this, the microaerobic condition. It is clear that both biotic
biologically produced sulfur could be more available and abiotic processes run in parallel (Buisman et al.
and suitable for microorganisms compared to the 1990a), but the rates of these processes in microaer-
chemically produced one. More information about obic digesters are not well quantified yet.
biologically produced elemental sulfur can be found in Moreover, the exact metabolic pathway of sulfide
the papers by Janssen et al. (2009) and Kleinjan et al. oxidation under microaerobic condition is not well
(2003). defined. It is not clear yet, what is the role of
intermediate sulfur species such as sulfite, thiosulfate,
polysulfide, and polythionates. It is also not clear, to
9 Economic considerations what extend can be elemental sulfur repeatedly
reduced to sulfide and how this process contributes
When considering microaeration to remove sulfide, air to the overall oxygen consumption and reduction of
is, at least initially, the most economical alternative; methane yield.
however, biogas dilution with nitrogen (1–8 %) when
air is employed may result in a lower performance of 10.2 Control of microaeration
biogas combustion or higher costs during biogas
upgrading to remove nitrogen. In fact, a recent To maximize the efficiency of microaeration, precise
economic evaluation revealed that the utilization of control of air dosing is needed. In the current
concentrated oxygen (92–98 %) presented higher net applications, microaeration often cannot cope with
present value (NPV5 and NPV20) than the utilization sudden changes of sulfide concentration in biogas
of pure oxygen or air to substitute the current addition induced e.g. by the start of intermittent mixing
of FeCl3 to the anaerobic digesters of a full-scale (personal communication with plant operators). It
WWTP producing 550 m3 h-1 of biogas. This alter- can be expected that similar problems will take place
native presented the lowest operational costs per cubic in high-rate digesters should microaeration be intro-
meter of biogas treated (0.0019 EUR) compared to air, duced for them too.
pure oxygen supply and the addition of FeCl3 (0.0027 The spatial control of microaeration, i.e. the spatial
EUR, 0.0039 EUR and 0.0100 EUR, respectively) distribution of the formation of elemental sulfur is
(Dı́az et al. 2015). even more pressing problem. In current applications,
most of sulfur forms on the walls of reactor’s
headspace (Kobayashi et al. 2012; Ramos et al.
10 Needs for further research 2012, 2014b; Rodriguez et al. 2012) and is expected
to continually fall of into the liquid effluent (Ramos
Microaeration as a method for biogas desulfurization et al. 2014c). However, partial or complete clogging of
has been gaining attention over the past years and it biogas piping has also been reported (de Arespa-
has been often used in full-scale digesters in agricul- cochaga et al. 2014). When introduced into high-rate
tural applications [personal communications with digesters such as UASB, IC or EGSB, formation of
plant operators and Schneider et al. (2002)]. However, sulfur will partially take place in the three-phase
some theoretical and practical aspects of microaera- separators of these reactors (Krayzelova et al. 2014a)
tion still remain unclear and need further research. which may seriously impair the function of the
This is important both for introduction of microaer- digester. Therefore, new methods for controlled safe
ation into new fields (high rate digesters for sulfur formation in dedicated compartments of the
123
digesters should be developed. The application of of microaeration taking place in the gas phase.
biomembranes (biofilm grown on the surface of However, there are reports showing that microaer-
membrane modules) for air delivery is one of the ation can take place also in the liquid phase.
promising options (Alvarez 2014). This technique • The residence time of biogas in the headspace and
would facilitate sulfur formation directly on the available surface area are the key factors affecting
surface of these membranes and thus preventing the the efficiency of hydrogen sulfide removal through
clogging of three-phase separators. sulfur oxidation in the headspace.
• Intensified contact between oxygen and anaerobic
10.3 Microbiology biomass may improve the removal of dissolved
sulfide, decrease the amount of oxygen in biogas
There are several reports describing the microbiolog- and increase the rate of hydrolysis. This effect can
ical composition of microaerobic biofilms, but there be facilitated when the reactor is mixed by biogas
has been very little systematic work on this topic. Most or when air/oxygen is dosed into the liquid phase.
of the knowledge on SOB microbiology is derived • An integrated mathematical model describing
from studies with pure SOB cultures (De Zwart et al. microaeration has not been developed so far. Such
1997) or environments different from microaerobic model would greatly improve the understanding of
digesters such as activated sludge biotrickling filters the process and research on this topic is of high
etc. (Alcántara et al. 2004; Munz et al. 2009; Xu et al. priority.
2013).
Acknowledgments This research was financially supported by
the specific university research (MSMT No. 20/2015), the
10.4 Mathematical modelling
International Research Staff Exchange Scheme project
‘‘Renewable energy production through microalgae cultivation:
Microaeration as a method for biogas desulfurization Closing material cycles—ALGAENET’’ (PIRSES-GA-2011-
in anaerobic digestion has not been modelled yet and 295165) and by the Technology Agency of Czech Republic—
Project TA03021413. Lucie Krayzelova received funding for a
remains an important research gap. Although, there
joint doctorate from Ghent University’s Special Research Fund
are a few papers describing sulfate reduction and (BOF—01SF2012). David Jeison would like to thank for support
sulfide oxidation (Xu et al. 2013), the conditions of provided by CRHIAM Centre (CONICYT/FONDAP/15130015).
limited amount of oxygen are specific and require its
own modelling approach.
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Microaeration For Hydrogen Sulfide Removal During Anaerobic Treatment: A Review

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Rev Environ Sci Biotechnol (2015) 14:703–725

Microaeration for hydrogen sulfide removal

Published online: 14 November 2015

L. Krayzelova (&) J. Bartacek P. Jenicek Abbreviations

SRB Sulfate-reducing bacteria demanding and expensive (Appels et al. 2008). In

For very large gas volumes or

Biological Electron acceptor Dominant microorganisms Situation Additional comments References

In this paper, the process of biological oxidation of

2HS þ O2 ! 2S0 þ 2OH increased up to 2, sulfide was completely oxidized to

Table 2 Sulfide oxidizing bacteria found in anaerobic reactors subjected to microaeration

Acidithiobacillus thiooxidans Proteobacteria Bottom of biotrickling filter Air de Arespacochaga

At pH around 7, at which anaerobic digestion typically 5.5 Reactor configurations

n.a. 13,000 C99 68 n.a. Jenicek et al. (2014)

10 2500–4900 99 &0 \0.1 (Ramos et al. 2014b)

6.6 12,000 97.5 &0 1–1.4 Dı́az et al. (2010)

gases involved were determined (CH4, CO2, H2S, O2,

In the second category, a microaerobic unit (or

17.46 1.02 0.80 0–5.00 0.15 Klok et al. (2013)a

Table 5 The kinetic parameters of biological oxidation of sulfide to elemental sulfur

Alcántara S, Velasco A, Muñoz A, Cid J, Revah S, Razo-Flores

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