Grimalt-Alemany Et Al-2018-Biofuels, Bioproducts and Biorefining

Review
Syngas biomethanation: state-of-the-

art review and perspectives
Antonio Grimalt-Alemany, Center for Bioprocess Engineering, Department of Chemical and
Biochemical Engineering, Technical University of Denmark, Lyngby, Denmark
Ioannis V. Skiadas, PILOT PLANT, Department of Chemical and Biochemical Engineering, Technical
University of Denmark, Lyngby, Denmark
Hariklia N. Gavala, Center for Bioprocess Engineering, Department of Chemical and Biochemical
Engineering, Technical University of Denmark, Lyngby, Denmark
Received June 23, 2017; revised August 24, 2017; and accepted August 25, 2017
View online at October 10, 2017 Wiley Online Library (wileyonlinelibrary.com);
DOI: 10.1002/bbb.1826; Biofuels, Bioprod. Bioref. 12:139–158 (2018)
Abstract: Significant research efforts are currently being made worldwide to develop more efficient
biomethane production processes from a variety of waste streams. The biomethanation of biomass-
derived syngas can contribute to increasing the potential of methane production as it opens the way
for the conversion of recalcitrant biomasses, generally not fully exploitable by anaerobic digestion
systems. Additionally, this biological process presents several advantages over its analogous process
of catalytic methanation such as the use of inexpensive biocatalysts, milder operational conditions,
higher tolerance to the impurities of syngas, and higher product selectivity. However, there are still
several challenges to be addressed for this technology to reach commercial stage. This work reviews
the progress made over the last few years in syngas biomethanation processes in order to provide an
overview of the current state of the art of this technology. The most relevant aspects determining the
performance of syngas biomethanation processes are extensively discussed here, including microbial
diversity and metabolic interactions in mixed microbial consortia, the influence of operating parame-
ters and bioreactor designs, and the potential of modelling as a tool for the design and control of this
bioprocess. © 2017 Society of Chemical Industry and John Wiley & Sons, Ltd
Keywords: biomethanation; synthesis gas; carbon monoxide; methane; microbial consortia;

mixed cultures
Introduction Brazil, China, and India, among others.1 An example of

such policies is the European Directive 2009/28/EC, which
he increase in energy demand over the last few established binding targets for achieving a 20% share of
T decades along with the foreseen future scarcity

of fossil fuels and the climate crisis have driven
policymakers to foster the production of biofuels as an
energy from renewable sources on the overall European
energy consumption by 2020, and a minimum share of
10% in the transport sector emphasizing the need of pro-
alternative energy source. Currently, the EU and several moting second-generation biofuels. Therefore, the current
countries with an important role in the global market have legal and regulatory framework poses an important win-
implemented policies in this direction, including the USA, dow of opportunity for the development of an alternative
Correspondence to: Hariklia N. Gavala, Center for Bioprocess Engineering, Department of Chemical and Biochemical Engineering,
Technical University of Denmark, Søltofts Plads 229, 2800 Kgs. Lyngby, Denmark. E-mail: [email protected], [email protected]
© 2017 Society of Chemical Industry and John Wiley & Sons, Ltd 139
A Grimalt-Alemany, IV Skiadas, HN Gavala Review: Syngas biomethanation: state-of-the-art review and perspectives
technological infrastructure based on the use of non-food Table 1. Energy content of various fuels.20
biomasses and waste streams as feedstock.
Fuel Higher Heating Value (MJ/kg)
One of the most promising approaches within second-
Gasoline 46.5
and third-generation biofuel technologies is the process
of gas fermentation, which has gained increasing interest Diesel 45.4a
in recent years for the conversion of both industrial off- Ethanol 29.7
gases and recalcitrant feedstocks when coupled to their Biodiesel 42.2a
gasification into synthesis gas. This process consists in the Methane 55.5
fermentation of a gaseous substrate, mainly composed by Hydrogen 141.8
H2, CO, and CO2, carried out by anaerobic micro-organ- Butanol 36.6a
isms able to utilize these gases as a carbon and energy Dimethyl Ether 31.7
source. Acetogenic bacteria are currently the predominant
Methanol 22.7a
microbial group subject to study in syngas fermentation a
Extracted from Demirel 21
processes, with ethanol being the most commonly targeted
product. Syngas fermentation processes for the production
of ethanol2–8 and other products, such as acetone, butanol, However, the positive trend in the use of biomethane as
2,3-butanediol, and even biopolymers, have been exten- a vehicle fuel in several European countries, for example
sively reviewed recently including several process-devel- Sweden, France, or Denmark,19 anticipates the expansion
opment related aspects such as bioreactor design, relevant of this emerging market, which could foster the develop-
operational parameters, and genetic tools for broadening ment of more efficient production processes.
the product portfolio of the syngas bioconversion.9–15 An additional aspect of biomethane is its flexibility in
However, the biological process of syngas conversion into terms of production paths and biomass sources, as it can
methane is often overlooked in these reviews despite the be produced by both biochemical and thermochemi-
research carried out in this field in recent years. Therefore, cal methods which separately and in combination may
the scope of this paper is to perform a comprehensive cover a wide range of feedstocks of a different nature.
review of the knowledge available up to date in syngas Anaerobic digestion is a well-established technology
biomethanation processes in order to provide an overview currently processing several feedstock types from the
of the current state of the art of this technology, as well as agricultural sector and other organic industrial waste
to discuss about its future application perspectives. streams.22 On the other hand, catalytic methanation
As a potential product, biogas (or biomethane when technologies for synthetic natural gas (SNG) production
upgraded) presents a significant potential for its integra- have been revisited over the last 10 years due to the ris-
tion into the current biofuel landscape due to its versatility ing prices of natural gas and the need to address energy
as an energy carrier. To date, the most common practice security issues, which has promoted the development
is to exploit biogas in situ for production of combined heat of several new catalytic methanation processes based
and power as the quality standards for this application are on biomass gasification.23 These facts suggest that the
generally lower. However, biogas upgrading to biomethane process of syngas biomethanation would also have a
provides a more flexible application of this fuel, as biom- potential market for its future application once it reached
ethane and natural gas are fully miscible in the natural gas commercial scale. As will be discussed in the next sec-
grid. As a transportation fuel, the use of biomethane in tion, this technology presents several advantages over the
bi-fuel cars is a rather attractive alternative to liquid fuels analogous catalytic methanation process and is also well
in terms of energy content (Table 1). Additionally, the suited for coupling to current anaerobic digestion sys-
fact that it is fully miscible with its fossil analog, natural tems, opening thus good perspectives for further develop-
gas, is a clear advantage over other liquid biofuels such ment of this technology.
as bioethanol or biodiesel, which are usually blended to
some extent in conventional cars.16 On the other hand,
its further development as an automotive fuel is currently Overview of the syngas
hindered by several factors such as the early stage of its biomethanation process
commercial market, the limited number of fi lling stations,
and the high cost of the technological transfer to bi-fuel The biomethanation of biomass-derived syngas is a
vehicles compared to vehicles fueled solely by ethanol.17,18 robust bioconversion route combining the benefits of
140 © 2017 Society of Chemical Industry and John Wiley & Sons, Ltd | Biofuels, Bioprod. Bioref. 12:139–158 (2018); DOI: 10.1002/bbb
Review: Syngas biomethanation: state-of-the-art review and perspectives A Grimalt-Alemany, IV Skiadas, HN Gavala
thermochemical and biochemical conversion processes, as Syngas biomethanation versus

it circumvents the limitations of the biological degrada- catalytic methanation
tion of complex substrates by gasifying the biomass into
a directly fermentable gas. The thermochemical conver- The catalytic methanation is an exothermic process using
sion of the feedstock through gasification constitutes hydrogen and carbon oxides present in syngas for the
one of the main advantages since any type of biomass catalytic production of methane and water. This process
can be gasified including agricultural residues, forestry operates at temperatures above 250°C and high pressures,
residues, non-fermentable byproducts from biorefi ner- using previously activated metallic catalysts to drive the
ies, byproducts of any bioprocessing facility, and even catalytic reduction of carbon oxides into methane. The
organic municipal wastes.24 However, the substrate of the catalysts used in methanation are very sensitive to the
syngas biomethanation process is not limited to biomass- impurities present in synthesis gas such as chlorine and
derived syngas, as there are other potential sources of sulfur compounds, ammonia, tars, and particles, which
CO-rich industrial off-gases in the iron and steel sector.25 ultimately cause poisoning and deactivation of the cata-
Alternatively, other industrial CO2-rich off-gases could lysts.29 Therefore, the catalytic methanation requires an
also be used as substrate along with H2 derived from the intensive gas cleaning process of the raw syngas before
surplus of renewable electricity, opening another potential entering the reactor. Furthermore, an additional water-gas
application as a means of storing renewable electricity.26 shift reaction process is often needed in order to correct
Therefore, there is a rather wide range of industrial off-gas the ratio of C/H in syngas, which reduces the overall effi-
sources and biomasses that could be used as feedstock for ciency of the process while increasing the complexity and
this process. the cost of operation.30 The use of biocatalysts in syngas
The biomethanation of syngas involves the synergistic biomethanation is anticipated to result in a more cost-
action of micro-organisms, integrated in a mixed micro- effective process as these present a higher tolerance to the
bial consortium, for the utilization of syngas as a carbon impurities of syngas and operate at mild temperatures. As
and energy source to synthesize a mixture of methane opposed to the catalytic process, the biological process is
and carbon dioxide. The biomethanation of syngas is a not sensitive to the ratio of C/H since the water-gas shift
strictly anaerobic process that can be carried out at both reaction is inherent to the autotrophic metabolism of
mesophilic and thermophilic conditions. Synthesis gas most microbial groups 31 conducting the biomethanation
is converted into methane both directly and stepwise of syngas. Additionally, the biomethanation presents a
through intermediary products by several microbial higher selectivity as methane and carbon dioxide are the
groups such as methanogenic archaea, acetogenic bacteria, only end-products of the fermentation, whereas the cata-
and hydrogenogenic bacteria among others, with all of lytic process produces higher hydrocarbons as byprod-
them thriving in syntrophic association. As a result, the ucts. Lastly, the irreversible character of the biochemical
biomethanation of syngas comprises a complex network of reactions during biomethanation allows the complete con-
biochemical reactions mainly based on the water-gas shift version of the substrates, this way avoiding the thermody-
reaction, acetogenesis, hydrogenotrophic methanation, namic equilibrium limitations of the catalytic process.32
carboxydotrophic methanation, and acetoclastic methana-
tion. Despite the higher complexity of microbial consortia
Coupling syngas biomethanation and
compared to pure cultures, the adoption of this mixed-
culture approach presents a series of inherent merits
anaerobic digestion
such as non-sterile operation, higher adaptation capacity, Anaerobic digestion is so far the default technology for
higher tolerance to the impurities of the raw syngas, and biological production of methane, holding the dual role of
resiliency after a disturbance in the operating conditions, waste treatment and production of biofuels process. 33 The
which represent a crucial advantage when it comes to degradation of organic residues in anaerobic digestion is
maintain the productivity of a continuous process.12,27,28 carried out by undefi ned mixed microbial consortia in
Additionally, using undefined mixed microbial consortia four consecutive stages, namely hydrolysis, acidogenesis,
renders continuous processes more robust, as their adapta- acetogenesis and methanogenesis. Continuous anaerobic
tion to the substrate selects the most efficient and effective digestion processes are generally characterized by long
biocatalysts leading to a long-term improved performance hydraulic retention times due to the presence of refractory
of the microbial consortium.28 compounds in the biomass, which make hydrolysis the
© 2017 Society of Chemical Industry and John Wiley & Sons, Ltd | Biofuels, Bioprod. Bioref. 12:139–158 (2018); DOI: 10.1002/bbb 141
main rate-limiting step of the digestion. 34 Nevertheless, few decades. Yet, studies on the behavior of microbial
the main limiting factor is often the low biomass conver- consortia under different operating conditions still need
sion efficiency due to the low degradability of some spe- to be conducted to improve our understanding of the
cific biomasses. Thus, pre-treatments are usually needed microbial interactions within microbial consortia and
to enhance the digestibility of the biomass and improve achieve an optimal performance in microbial consortia-
the hydrolysis yield. In turn, the syngas biomethanation driven processes. The effect of operational parameters
process circumvents the limitations of the biological deg- such as pH, temperature, gas partial pressure and syngas
radation of complex substrates by gasifying the biomass impurities were recently reviewed in the frame of syngas
into a directly fermentable gas, overcoming the afore- fermentation to ethanol and other products.2,4,5,38,39 Thus,
mentioned shortcomings. Nonetheless, these technologies this review focuses on the progress made in the above-
are not necessarily alternative as their integration in a mentioned aspects of syngas biomethanation processes
combined process seems a promising configuration for over the last years, laying special emphasis on the role of
achieving a more efficient production of methane. Li et microbial interactions within syngas-converting mixed
al.30 studied the feasibility of combining the anaerobic microbial consortia.
digestion of source-separated organic waste with the gasi-
fication and biomethanation of wood pellets to increase Microbial growth on synthesis gas and
both quality and productivity of biomethane, obtaining syntrophic relationships in undefined
a potential increase of 161% in the production of biom- mixed microbial consortia
ethane compared to the stand-alone anaerobic digestion
process. Similarly, Guiot et al.35 estimated the potential of The main components of synthesis gas (H2, CO2, and CO)
the conversion of municipal solid waste through anaero- can sustain growth of a wide array of micro-organisms
bic digestion of the easily digestible organic fraction and belonging to different ecological niches such as certain
syngas biomethanation of the non-digestible organic frac- fungi,40 algae,41 photosynthetic bacteria,42 hydrogeno-
tion, resulting in a production of biomethane of about five genic bacteria43 and archaea,44 sulfate-reducing bacteria
45
times higher than the stand-alone anaerobic digestion of and archaea,46 acetogenic bacteria 47 and methanogenic
municipal solid waste. Other potential benefits are the use archaea 48 among others. However, during anaerobic
of biochar produced during the thermochemical treat- growth only acetogens, methanogens, sulfate-reducers,
ment of the biomass as a support for biofi lm formation or and hydrogenogens can use either CO or H2/CO2 as the
as an in situ biogas upgrading agent during the anaerobic sole carbon and energy source.49,50 These groups are physi-
digestion process.36,37 Therefore, there are several syner- ologically and phylogenetically diverse, although they all
gies that could be exploited upon the combination of share common metabolic features such as the fact that
these technologies. acetyl-CoA plays a central role during the assimilation
of both H2/CO2 and CO in all of them, and CO itself is a
necessary intermediate for the fi xation of CO2 by aceto-
Progress in syngas biomethanation gens and methanogens.51-53 Therefore, the presence of CO
and ongoing research dehydrogenases (CODH) is also a common thread in the
metabolism of these micro-organisms. However, the func-
Despite the potential benefits of the syngas biomethanation of their CODH differs in that they can either oxidize
tion process, there are still important bottlenecks that CO, synthesize acetyl-CoA or cleave acetyl-CoA in a vari-
need to be addressed in order for this technology to be ety of independent energy-yielding pathways in each of
commercially applicable. One of the main shortcomings these microbial groups.54
of continuous syngas fermentation processes is the limited The anaerobic assimilation of CO and H2/CO2 can be
mass transfer rate of H2 and CO due to the low solubility categorized in the following four distinct activities accord-
of these gases in the liquid medium. The low cell growth ing to their final metabolic product: hydrogenogenesis
rate of anaerobic micro-organisms is another limiting (including hydrogenogenic bacteria and archaea, and
factor since the low cell productivities of continuous carboxydotrophic hydrogenogenic sulfate-reducers55),
processes result in low volumetric productivities of CH4. sulfidogenesis (including carboxydotrophic sulfidogenic
The fundamental aspects of the microbial metabolism sulfate-reducers52,55), carboxydotrophic and hydrog-
of the micro-organisms carrying out the biomethana- enotrophic acetogenesis, 56,57 and carboxydotrophic and
tion of syngas have been thoroughly studied over the last hydrogenotrophic methanogenesis.52,58 The biochemistry
Figure 1. Pathways leading to the production of methane. The standard Gibbs free energy change (ΔG°) was calculated
according to Thauer et al.89
of these respiratory processes has been extensively Cross-feeding relationships

reviewed by several researchers in recent years.52,53,55–59
Despite the multiple pathways through which syngas can
Thus, this section focuses on the microbial interactions
be converted into CH4, several studies have reported the
prevailing in syngas-converting microbial consortia dur-
preferential use of certain pathways within the consortium
ing the production of methane.
during the biomethanation of syngas. Guiot and Cimpoia
A microbial consortia-driven process of syngas biom- 64
evaluated the mesophilic and thermophilic methano-
ethanation sustains a variety of microbial groups, such
genic potential of anaerobic granules from a UASB plant
as those mentioned, which develop a chain of syntrophic
during the conversion of CO and syngas, observing that
interactions resulting in the production of CH4 as the only
CO was predominantly converted through hydrogeno-
end product of the fermentation. Thus, the conversion of
trophic methanogenesis combined with CO-dependent H2
syngas into CH4 can take place either directly through the
formation. In this study, formation of volatile fatty acids
conversion of both CO and H2/CO2 by carboxydotrophic
(VFA) was also observed, although only in trace amounts
and hydrogenotrophic methanogenesis, or indirectly
consisting of mainly acetate; however, when H2 and CO2
through the conversion of syngas into methanogenic
were also added as substrates, the amount of VFA’s pro-
precursors such as acetate, H2 and formate, followed
duced increased. In turn, Navarro et al.65 found that CO
by aceticlastic and hydrogenotrophic methanogenesis.
was converted into CH4 through acetate as a main inter-
Additionally, acetogenic bacteria have been reported to
mediary product during inhibition experiments (based on
produce other by-products besides acetate, like ethanol,60
the use of BES and vancomycin for inhibiting the metha-
butyrate,61 and butanol,62 which could be further con-
nogenesis and acetogenesis, respectively) at mesophilic
verted into acetate and ultimately into CH4. Therefore,
conditions using a similar anaerobic granular sludge.
a microbial consortium may convert syngas into CH4
These results are in line with the findings of other studies
through a complex network of interconnected biochemical
using the same inhibitors, in which acetate was found to
reactions as shown in Fig. 1. However, the microbial inter-
be the main intermediate product during the conversion
actions within a stable and structured microbial consor-
of CO into CH4 at mesophilic conditions, and H2 at ther-
tium do not simply consist of cross-feeding relationships,
mophilic conditions.66 All these studies concluded that the
as there are other possible microbial interactions besides
carboxydotrophic methanogenic activity was negligible for
cross-feeding, like synergistic interactions between dif-
the anaerobic sludges tested. Similar results were obtained
ferent species and mutual exclusion relationships between
while studying the structure and diversity of microbial
metabolically competitive populations.
consortia on a simultaneous process of thermophilic methanogenic precursors in mixed microbial consortia.

anaerobic digestion of sewage sludge and CO biomethana- However, the Gibbs free-energy change for, for example,
tion, in which the population of hydrogenotrophic metha- butyrate oxidation to acetate, H2 and CO2 is only favorable
nogens increased upon addition of CO into the bioreactor at very low PH2 (<10 -4 atm). This type of symbiotic rela-
due to the higher production of H2 from CO.67 In turn, tionship is thus only feasible in those cases in which H2 is
in a similar study at mesophilic conditions, Wang et al.68 kept at low concentrations due to the continuous removal
found that the addition of CO in the bioreactor resulted of H2 by, for example, hydrogenotrophic methanogens.
in a clear increase of hydrogenotrophic microbial groups Nonetheless, recent studies have demonstrated that
while the population of aceticlastic methanogens remained Geobacter species and Methanosaeta species are capable
at high levels. They concluded that CO was converted to of direct interspecies electron transfer as an alternative
both H2 and acetate, which were further converted into mechanism to H2 or formate transfer.71
CH4 by both direct hydrogenotrophic methanogenesis, Further symbiotic interactions have also been reported
and indirect acetogenesis and aceticlastic methanogen- in other co-culture experiments. Parshina et al.72 found
esis. Thus, it appears that the biomethanation of syngas by that the pure cultures of D. kuznetsovii and D. thermoben-
mixed microbial consortia generally takes place through zoicum subsp. thermosyntrophicum were capable of chem-
indirect conversion rather than direct, with acetate and H2 olithotrophic growth on CO levels up to 0.70 atm when
being the most common methanogenic precursors. cultivated in presence of sulfate. However, when these
species were co-cultured with C. hydrogenoformans, they
were able to grow at 1 atm of CO through the reduction
Mutualistic interactions
of sulfate using the H2 produced by the hydrogenogen.72
There are still other possible metabolic interactions Similar results were obtained by Rajagopal et al.73 who
exhibiting mutualistic properties that could be developed studied the co-culture of D. vulgaris and M. barkeri in the
among different members of a mixed microbial consor- absence of sulfate. The pure culture of D. vulgaris exhib-
tium. An example of such mutualistic relationships is ited partial inhibition of the production of H2 from pyru-
the interspecies diff usion of electron carriers like H2 or vate upon addition of CO to the culture, as the rate of H2
formate between syntrophic bacteria and methanogenic production from pyruvate alone and from both substrates
archaea, which could remain unnoticed due to the low remained unchanged. Nonetheless, when D. vulgaris was
concentration and fast turnover of these compounds.69 The co-cultured with M. barkeri using lactate as substrate,
syntrophic bacterial genus Smithella, a fatty acid-oxidizer, the injection of CO resulted in a H2 burst along with a
was found to be relatively dominant during the simultane- parallel increase in the rate of CH4 production with no
ous biomethanation of sewage sludge and CO; however, apparent inhibitory effect of CO. 73 Additional symbiotic
whether its function was relevant to the biomethanation of interactions have also been observed in experiments using
CO was not determined.68 Similarly, Navarro et al.70 found undefined mixed microbial consortia. Navarro et al.70
that the population of Geobacter unaniireducens, a syn- compared the performance of crushed granular sludge and
trophic acetate-oxidizing bacterium, increased in a granu- whole sludge granules fed on CO, fi nding that the higher
lar sludge after a long-term exposure to CO. The process organization of the granular sludge enhanced the CH4
of interspecies diff usion of electron carriers was studied production rate due to the protection of the inner layers
by Boone et al.69 in co-culture experiments with the fatty of the granule against the toxicity of CO. Therefore, these
acid-oxidizing bacterium S. wolfei and the methanogen M. cases show that the metabolic interaction between micro-
formicicum using butyrate as substrate. When these spe- bial groups can generate synergistic effects due to the
cies were co-cultured, the production of CH4 proceeded lower concentration of CO in the medium or in the inner
exponentially while the concentration of H2 remained layers of the granules, enhancing both the growth and the
constant at 63 nM until depletion of butyrate, after which resiliency of the microbial community as a whole.
the concentration of H2 dropped to 35 nM.69 Similarly in
the same study, a co-culture of S. wolfei and Desulfovibrio
sp. strain GII was incubated with butyrate and sulfate as
Mutual exclusion interactions
substrates, where the concentration of H2 stabilized at 27 The structure of a microbial consortium is not only deter-
nM for 2 days until sulfate was depleted. This illustrates mined by interactions of mutualistic nature since mutual
the importance that such interspecies diff usion of electron exclusion relationships, based on competition for common
carriers may have during the conversion of fatty acids to substrates, also play an important role on the definition of
the community structure. In presence of sulfate, all active be easily outcompeted in a mixed microbial consortium.
microbial groups during syngas biomethanation including However, it is likely that the outcome of the competition
acetogens, methanogens, sulfate-reducers and hydrog- between hydrogenogenic and acetogenic bacteria is not
enogens compete for common substrates such as CO, H2 ultimately dependent upon their kinetics given the simi-
or acetate. The competition for H2 is generally ruled by larity of the doubling times reported.
sulfate-reducers, since both the kinetic properties of this All these microbial interactions can have an influence,
group and the thermodynamics of sulfate reduction are either positive or negative, on the structure and diversity
more favorable than in homoacetogenesis and methano- of a microbial community, ultimately affecting the per-
genesis.74,75 However, in most cases the activity of sulfate- formance of the consortium. Therefore, knowledge on the
reducers can be easily suppressed by controlling the sulfate type of interactions prevailing among the members of a
content in the medium in order to favor the methano- microbial consortium is fundamental for the control and
genesis given the low content of sulfur oxides in syngas. optimization of the process.83 However, the performance
According to Xu et al., 38 the highest concentration of sul- of a consortium is also strongly influenced by the operat-
fur compounds reported in biomass-derived syngas cor- ing conditions of the process, thus requiring the integra-
responds to 0.055 mol% for SO2, and 0.0001 mol% for H2S tion of all aspects determining the outcome of the process
and COS. Moreover, the outcome of the competition for for optimal process control.
H2 appears to depend on additional factors, since in con-
trast to the previous statement hydrogenotrophic metha-
nogens have also been reported to outcompete sulfate- Influencing factors in syngas
reducers. Sipma et al.76 observed that sulfate-reducers were biomethanation
clearly outcompeted by hydrogenotrophic methanogens
The operating parameters of biological processes have a
during operation of a gas-lift reactor fed on CO and sulfate
strong impact on the performance of the culture in terms
at thermophilic conditions. In this study, the dominance
of productivity as these affect several aspects of microbial
of hydrogenotrophic methanogens was attributed to the
growth. Pure culture-based processes are generally oper-
higher growth rates of this microbial group at the operat-
ated at conditions favoring optimal growth and produc-
ing conditions investigated.76 The competition between
tivity based on the characteristics and requirements of
homoacetogens and hydrogenotrophic methanogens for
a particular strain. However, the members composing a
H2 was studied by Liu et al.,77 finding that the kinetic con-
mixed microbial consortium for syngas biomethanation
stants Ks and μ max of homoacetogens were respectively 10
rarely share the same optimal growth conditions, which
times higher and 4 times lower than those of hydrogeno-
make the selection of operational parameters a critical step
trophic methanogens. Hence, homoacetogens were clearly
when it comes to optimizing the process. In this section,
outcompeted by the latter group under substrate-limiting
the influence of parameters such as temperature, pH and
conditions (low PH2). However, homoacetogens were able
gas composition on the CH4 yield and production rate of
to compete for H2 at high PH2, contributing through aceti-
syngas-converting consortia is reviewed.
clastic methanogenesis to the formation of 40% of the CH4
produced.77
pH
The competition for CO in mixed microbial consor-
tia has not been thoroughly studied, although the out- The pH is an important parameter for microbial growth
come of the competition can be predicted based on the due to its influence on the regulation of the metabolism
kinetic properties reported for these microbial groups. and the bioenergetics of micro-organisms as it causes
Carboxydotrophic methanogens typically have long dou- changes in the intracellular pH and the electrochemi-
bling times ranging from 24 h to 200 h.48,78 In turn, the cal gradient across the membrane. Acetogenic bacteria
doubling times exhibited by acetogenic bacteria generally are perhaps the most versatile microbial group as they
oscillate between 1.5 h and 16 h reported for R. Productus are able to tolerate a wide range of pH including both
and C. thermoaceticum, respectively.79,80 Hydrogenogenic acidic and alkaline conditions,56 although they are
growth supports different doubling times depending on known to shift their generally acidogenic metabolism
the microbial group, being 1–2 h for thermophilic hydrog- towards solventogenesis when decreasing the pH.84,85 The
enogens and 4.8–8.4 h for phototrophic bacteria.81,82,76 hydrogenogenic microbial group including phototrophic
Therefore, the comparison of the growth kinetics on CO and hydrogenogenic bacteria generally exhibit optimal
of these microbial groups indicates that methanogens will growth at neutral pH.55 In turn, most methanogens grow
optimally at either neutral or slightly alkaline pH ranging of the gases, which could lead to mass transfer limitations
from 6.8 to 8.5,58 being partially inhibited when decreas- in thermophilic processes.
ing the pH. Consequently, most syngas biomethanation
processes are operated at pH close to neutrality, between Gas partial pressure
7.0 and 7.6, to favor the methanogenesis and avoid the
The effects of the composition of synthesis gas are mainly
accumulation of liquid products (Table 2). Nevertheless,
associated with mass transfer processes of the constituents
the influence of the pH has not been thoroughly studied
of syngas, which are dependent on both the mass transfer
in syngas biomethanation processes. So far, only Pereira et
coefficient (k La) and consequently on the characteristics
al.86 have investigated the biomethanation of syngas using
of the reactor, and the partial pressure of these gases as
a mixed culture approach under different pH conditions.
the driving force for their transportation to the liquid
This study reported that the combination of low pH and
phase. In this section, the effects of the partial pressures
high pressures of syngas (2.5 atm) resulted in high inhibi-
of the main components of syngas are discussed, while the
tion of the methanogenic activity, obtaining the lowest
effects of the mass transfer rates are addressed in the sec-
production of CH4 among all conditions tested.86
tion for process configurations.
Carbon monoxide, besides being a substrate for
Temperature carboxydotrophs, is also a well-known inhibitor for most
The temperature is one of the most influential factors carboxydotrophic microbial groups. Carboxydotrophic
in syngas biomethanation processes as it affects several methanogens and sulfate-reducers appear to be the most
aspects of the performance of mixed microbial consortia. sensitive, tolerating partial pressures of CO (PCO) between
As mentioned already, the temperature of the broth has 0.5 and 1.0 atm and 0.2-0.5 atm respectively, with some
been reported to have an effect on the microbial interac- exceptions.45,48,78,88 In turn, both acetogens and hydrog-
tions among members of microbial consortia as it appears enogens exhibit a higher tolerance to CO, generally being
to determine the predominant metabolic pathways used able to grow at PCO higher than 1 atm.4,55 Nevertheless, the
by the consortia. Several studies on biomethanation of CO effects of CO on syngas biomethanation processes are not
indicate that acetate is the main precursor of the metha- limited to direct inhibition of carboxydotrophic growth,
nogenesis at mesophilic conditions, whereas H2 is a more as other non-carboxydotrophic microbial groups with a
relevant precursor at thermophilic conditions. This could significant role might also be affected, including fatty-
be explained by the higher diversity of carboxydotrophic acid oxidizing bacteria, aceticlastic and hydrogenotrophic
hydrogenogenic bacteria in thermophilic environments. methanogenic archaea.
However, another possible explanation could be the fact In syngas biomethanation processes, the increase in PCO
that H2-producing reactions become more exergonic with generally results in partial inhibition, ultimately affect-
increasing temperatures,87 favoring a higher hydrogeno- ing the yield and the productivity of CH4. The effects on
genic conversion of CO at thermophilic conditions. In the CH4 yield were evaluated on a mesophilic granular
either case, it has been shown that these changes in the sludge fed on syngas, in which a decline in the CH4 yield
microbial structure of the consortia due to higher tem- was observed while increasing the total pressure of syngas
peratures lead to higher conversion rates in syngas biom- from 1 to 2.5 atm due to the inhibition of the methano-
ethanation processes. Guiot and Cimpoia 64 compared the genic activity.86 In turn, the specific carboxydotrophic and
rates of CH4 production of a granular sludge at mesophilic methanogenic activities of a mesophilic granular sludge
and thermophilic conditions, finding that the CH4 pro- under different initial PCO were studied by Navarro et al.,70
ductivity at thermophilic conditions (5.6 mmol/g VSS/d observing that the rate of consumption of CO increased
at 60°C) was much higher than that at mesophilic condi- with the amount of CO supplied until a maximum was
tions (1 mmol/g VSS/d at 35°C). Similarly, another study reached at a PCO of 0.5 atm. However, the rate of produc-
investigated the correlation between the rates of conver- tion of CH4 reached its maximum at 0.2 atm of CO, fol-
sion of CO and the temperature, observing that the rates lowed by a gradual decline along with the increase of PCO
of conversion of CO and the productivity of CH4 increased until the methanogenic activity was totally inhibited at
gradually from 40°C onwards until a maximum was 1 atm of CO.70 Additionally, in this study a shift in the
reached at 55°C.66 Nonetheless, despite the higher conver- metabolic pathways with increasing PCO was observed,
sion rate and productivity, the increase in temperature in which aceticlastic methanogenesis was displaced by
also poses certain drawbacks related to the lower solubility hydrogenotrophic methanogenesis between 0.5 and 1 atm.
Table 2. Overview of syngas biomethanation process configurations and operating conditions.
Micro-organism Reactor Operation Gas Co- Gas Gas H2 CO CH4 prod. Yieldi T pH Ref.
mode composition substrate rec. rate flow rate flow rate flow rate (mmol/l/d) (mol /mol) (C°)
(%) (ml/min) (ml/min) (mmol/l/d) (mmol/l/d)
Cow pasture BCa Batch H2/CO2 - 300 - 1380 - 300 0.22-0.26 55 7.4 Bugante
sludge (-) et al.107
Cow pasture BCa Batch CO - 300 - - 480 120 0.25 55 7.4 Bugante
sludge (40) et al.107
Sewage plant TBb Cont. H2/CO2 - - n.d. 268 - 66.5 0.248 37 7.2 Burkhardt
anaerobic sludge (-) et al.103
Fruit processing GLc Cont. CO - 1150 57.5 n.d. - 2.92h 0.228 35 7.1 Guiot et al.64
plant granular (41)
sludge
Triculture TBb Cont. CO/CO2/H2 light n.d. 70 n.d. n.d. 48-72 0.2 37 n.d. Kimmel
(R. rubrum, 55.6/9.7/19.7 et al.105
M. barkeri,
M. formicicum)
Review: Syngas biomethanation: state-of-the-art review and perspectives
Triculture TBb Cont. CO/CO2/H2 light n.d. 174 n.d. n.d. 9.6 0.2 37 n.d. Kimmel
(R. rubrum, 54.4/9.7/21.1 et al.105
M. barkeri, M.
formicicum)
Granular sludge MOBBd Cont. CO/CO2/H2 - 600 100 24.2 54 73 0.6-0.8 35-37 5.8-6.7 Pereira109
(60/10/30)
MSW sludge RMBe Semi-Cont. CO/CO2/H2 3.4 g COD 300 n.d. 7 15 8.3 n.d. 55 n.d. Westman110
(55/10/20) VFA’s/l/d
Anaerobic sewage STRf Cont. H2/CO2 - n.d. 700 1344 - 352.8 n.d. 37 n.d. Wise102
sludge (-)
Triculture (R. TBb Cont. CO/CO2/H2 light n.d. 300 n.d. n.d. 72 0.214 37 6.8-7.2 Klasson108
rubrum, M. barkeri, (55.6/9.9/19.7)
© 2017 Society of Chemical Industry and John Wiley & Sons, Ltd | Biofuels, Bioprod. Bioref. 12:139–158 (2018); DOI: 10.1002/bbb
M. formicicum)
Triculture (R. PBCg Cont. CO/CO2/H2 light n.d. 80 n.d. n.d. 4.8-7.2 0.214 34 6.8-7.2 Klasson108
rubrum, M. barkeri, (55/9.6/20.4)
M. formicicum)
a
bubble column; btrickle-bed; cgas-lift; dmulti-orifice oscillatory baffled bioreactor; ereverse membrane bioreactor; fstirred tank reactor; gpacked bubble column; hmmol/g VSS/d.
i
Yield expressed in mol CH4/mol syngas (H2 + CO)
147
A Grimalt-Alemany, IV Skiadas, HN Gavala
Thus, these studies clearly show that CO exerts a strong been found to inhibit the activity of several enzymes in
inhibitory effect over all microbial groups of the micro- acetogenic bacteria.38,92,93 On the other hand, the sulfur
bial consortium. Nevertheless, the differences observed gases H2S and COS barely affected the growth and the
between the carboxydotrophic and the methanogenic substrate uptake rate of the acetogen R. productus and the
activities illustrate a distinctive inhibition over aceticlastic methanogen M. barkeri, whereas the hydrogenogen R.
methanogens, which appear to be less tolerant than ace- rubrum and the methanogen M. formicicum were strongly
togenic, hydrogenogenic bacteria, and hydrogenotrophic inhibited even at low concentrations of these gases.94 Thus,
methanogenic archaea. The lower tolerance of the metha- each of the microbial groups appears to be affected differ-
nogenic group was also evident during the enrichment ently by the impurities. Guiot et al.95 studied the effects
of a thermophilic methanogenic microbial consortium of HCN, NH3, H2S and aromatic hydrocarbons on the
using increasing amounts of syngas along the successive overall performance of a methanogenic anaerobic sludge.
transfers.89 In these experiments, both H2/CO2 and CO The results of this study showed that the performance of
were initially converted into CH4 as the only end product. the mixed culture was not significantly affected at levels
However, the enriched consortium lost its methanogenic below 500 ppm, 50 ppm, and 1 ppm of NH3, H2S and
activity at the fourth transfer due to the inhibition caused aromatic hydrocarbons, respectively. However, HCN was
by the increasing partial pressure of syngas, resulting in found to inhibit the aceticlastic methanogenic activity at
the production of H2 as an intermediate product and the levels below 15 ppm. It was thus concluded that aceticlastic
accumulation of acetate and propionate as end products.89 methanogens were generally the most sensitive microbial
The concentration of H2 seems to have a milder influ- group, although the activity of all microbial groups was
ence on the performance of the consortium, although inhibited at higher levels of these impurities. Despite it has
changes in the PH2 have been reported to have an effect been shown that the activity of microbial consortia is not
on the microbial activity. The activity of the hydroge- significantly affected by low levels of impurities, further
nase of a clostridial species denoted as P11 was studied research in this area is still necessary in order to establish
under increasing PH2, finding that higher PH2 enhanced the minimum gas clean-up requirements of raw syngas as
the activity of the hydrogenase.90 However, the efficiency these may have an important influence on the overall effi-
of the hydrogenase decreased as the pressure of H2 built ciency of syngas biomethanation processes.
up due to the saturation of the enzyme.90 These findings Some of the influencing factors discussed here, such as
are in line with the results of other experiments using a the effect of the temperature and the growth inhibition
mixed culture approach, in which the production rate due to high PCO, have been studied thoroughly in micro-
of CH4 increased sensibly from 0.035 mmol/h to 0.072 bial consortia-driven syngas biomethanation processes.
mmol/h upon an increase of the initial pressure of H2/ Nevertheless, studies on the influence of pH and the
CO2 from 1 to 5 atm,91 as it can be noted that the increase impurities of syngas are still very limited. Additionally,
in the productivity appears not to correspond proportion- other factors such as the redox potential and the trace
ally to the increase of pressure. Therefore, it is likely that metal content of the media that have been studied in pure
the hydrogenases of other H2-utilizing micro-organisms, culture experiments,96,97 have not been investigated yet in
for example hydrogenotrophic methanogens, are also microbial consortia. Studying the potential interactions
affected by high PH2 resulting in lower rates of conversion. among the influencing factors discussed in this section
Additionally, in this study the structure of the microbial could also provide more insights on possible synergistic
community was found to be affected by the PH2, reducing effects on the behavior of microbial consortia. Therefore,
its diversity as the PH2 increased due to the more stringent further research on both the influencing factors and their
conditions.91 potential interactions is still necessary in order to fully
comprehend their influence over the performance of each
Impurities of synthesis gas microbial group and the consortium as a whole.
An additional aspect of the composition of syngas is the
content of impurities typically found in the raw syngas,
Process configurations
which may affect the process of syngas biomethanation Besides the limitations related to the inhibitory effects of
either causing perturbations in the performance of the CO and other aforementioned factors, syngas biomethana-
consortia or altering the operating parameters such as tion processes are often restricted by poor gas-to-liquid
pH or redox. Impurities such as tars, NOx and NH3 have mass transfer and low cell concentrations in the reactor,
which ultimately reduce the volumetric productivity of also be accounted when scaling up a process as the high
CH4. In an attempt to address these shortcomings, syngas energy requirements of maintaining a high mixing regime
biomethanation processes have been studied in a number in large scale stirred tank reactors often can render this
of process configurations including both batch and con- process not economically feasible.9
tinuous operating modes and several reactor designs, each
one of them having specific drawbacks and advantages. Trickle-bed reactors
The main characteristics, yields and CH4 productivities
Trickle-bed reactors are a suitable alternative to stirred
obtained in such process configurations are summarized
tank reactors in terms of costs of operation as this type of
in Table 2. Different syngas fermentation process configu-
reactors do not require mechanical mixing. These reac-
rations and bioreactor design issues have been reviewed
tors generally offer a more efficient gas-to-liquid mass
before for the production of H2, ethanol and other poten-
transfer while maintaining low gas and liquid flow rates
tial products. 2,4,9,98 Therefore, this paper covers only the
due to the higher contact surface area between the gaseous
findings related to syngas biomethanation.
substrate and the liquid fi lm on the packing material. The
influence of the liquid recirculation rate and the thickness
Stirred-tank reactors of the liquid fi lm on the mass transfer and the productiv-
The traditional stirred-tank reactors have been widely ity of CH4 was studied during the biomethanation of H2
used in syngas fermentation processes.60,99–101 In this type and CO2 using anaerobic sewage sludge as inoculum.103 A
of reactor, the volumetric mass transfer coefficient (K La) correlation between increasing productivities of CH4 and
is affected by several factors such as the geometry of the decreasing liquid recirculation rates was observed in this
reactor, the impeller configuration, the agitation speed, study, concluding that a high conversion (nearly 100%)
and the gas flow rate. Typically, higher mass-transfer rates and productivity (1.49 LCH4/L/d) could be achieved with-
are attained by increasing both the agitation speed and the out gas recirculation by just increasing the H2 loading rate
gas flow rate, which increase the gas-liquid interfacial area while decreasing the liquid recirculation rate. Thus, trickle
due to the smaller size of the bubbles. Klasson et al.32 stud- bed reactors seem a promising option for their applica-
ied the influence of these parameters on the K La during tion in syngas biomethanation as the plug flow regime of
the biomethanation of CO using a triculture of R. rubrum, these reactors allows high gas loading rates while main-
M. formicicum and M. barkeri. The K La was observed to taining high productivities and conversion efficiencies.
increase from 28.1 h-1 to 101.1 h-1 when increasing the Nevertheless, as found in other processes, compromised
agitation speed from 300 rpm to 450 rpm. However, the stability of continuous processes due to channeling of the
authors also observed that the efficiency in the conver- gaseous substrate through the packing material attributed
sion of CO decreased sharply while the gas loading rate to the excessive accumulation of microbial biofi lm was
increased, being 90% the maximum conversion efficiency observed during the biomethanation of H2 and CO2.104
reported at a gas loading rate of around 0.2 h-1. It can be Kimmel et al.105 compared the performance of two trickle
thus concluded that although relatively high K La values bed reactors with different diameters on the process of
are attainable in this type of reactors, a high productivity syngas biomethanation using a triculture of R. rubrum,
of CH4 can only be achieved at the expense of low conver- M. formicicum and M. barkeri. The productivity of CH4
sion efficiencies owing to the high gas flow rate needed. An in the smaller reactor was observed to increase as the gas
alternative strategy for increasing the productivity of CH4 loading rate increased, reaching a maximum productivity
is to increase of the concentration of microbial biomass in of 2-3 mmol CH4/L/h. However, the productivity of the
the bioreactor. This possibility was studied in a continuous larger reactor barely reached 0.4 mmol CH4/L/h at very
process of biomethanation of H2 and CO2 using a mixed low gas loading rates, showing a decreasing trend as the
culture from sewage sludge by including a cell recycling gas loading rate was raised. Apparently, the lower porosity
stream into the bioreactor.102 The cell recycle resulted in along with the smaller size of the packing material used
an increase of the cell concentration from 2.5 g/L to 8.3 in the smaller reactor favored an enhanced productivity
g/L, boosting the volumetric productivity of CH4 from as the lower pore size of the packing promoted a better
1.3 LCH4/L/h to 4 LCH4/L/h. Therefore, an increase in the distribution of the liquid medium. Therefore, trickle bed
productivity of CH4 can be achieved through both cells reactors have been successfully applied to syngas biom-
recycling and enhancing the gas-to-liquid mass transfer. ethanation processes achieving high productivities and
Other considerations such as the cost of operation should conversion efficiencies. Nevertheless, there are still certain
aspects of the continuous operation of these reactors such 0.2 mmol/L/h.108 Higher productivities (0.4 mmol CH4/
as biofi lm accumulation, porosity and the size of the pack- L/h) could be achieved when raising the gas flow rate to
ing material that need further study for attaining full 13.3–16.6 sccm; this however had a dramatic impact on the
exploitation of their potential. conversion efficiency as it dropped from 79% to 20–25%.
The authors concluded that the low productivity was
Bubble column and gas-lift reactors caused by mass transfer limitations and the high porosity
of the packing material given the low K La value obtained
The use of bubble columns and gas-lift reactors has also
(3.5 h-1). It seems that despite the simplicity of the design
been studied in syngas biomethanation processes as they
of these reactors, each of them has a good potential for
offer a number of benefits such as high gas-liquid inter-
their application in syngas biomethanation processes.
facial area, high volumetric mass transfer coefficient,
However, there are several key operational parameters that
non-mechanical mixing, and relatively low cost of opera-
need to be optimized in order to achieve a high productiv-
tion. As there is no mechanical mixing, the mass transfer
ity of CH4 while maintaining relatively high conversion
coefficient of these reactors generally depends on the gas
efficiencies.
flow rate and the size of the bubbles. The effect of these
operational parameters on the mass transfer of CO was
studied in both a bubble column and a gas-lift reactor,
Other reactor designs
showing that the K La increases along with the increase of Other reactor designs have also been studied for improv-
the gas flow rate and the decrease of the pore size of the ing the productivity of CH4 in syngas biomethanation pro-
column diff user.106 The maximum K La values reported cesses by either overcoming the mass transfer limitations
for the bubble column and the gas-lift reactor were 78.8 or increasing the concentration of cells in the bioreactor.
h-1 and 91.1 h-1, respectively, when a gas flow rate of 5000 A novel multi-orifice oscillatory baffled bioreactor with
sccm was combined with a 20 μm bulb diff user.106 Another a unique baffle design for improving both mixing and
common feature of these reactors is the need of applying mass transfer rates was fully characterized and tested for
a high gas recirculation rate in order to attain a relatively the biomethanation of syngas using a mesophilic granu-
high conversion efficiency for sparingly soluble gases such lar sludge as inoculum.109 The maximum productivity
as H2 and CO. Guiot et al.64 studied the effects of different achieved with this bioreactor was 73 mmol CH4/L/d at
gas recirculation rates during the biomethanation of CO the maximum flow rate tested (100 sccm). Nonetheless, as
in a gas-lift reactor using granular sludge. In these experi- the gas loading rate was raised the conversion efficiency
ments, the insufficient gas holdup when gas recirculation dropped as a result of the intensive mixing at high flow
was not applied resulted in a CO conversion efficiency as rates. Another reactor design intended to achieve total
low as 4%; however, when the gas recirculation-to-feed retention of cells into the bioreactor was also studied for
ratio was set to 18:1 the conversion efficiency increased to its application in syngas biomethanation. This design
70%, obtaining an improvement of the productivity from consisted in a reverse membrane bioreactor, in which the
0.49 mmol CH4/g VSS/d to 2.55 mmol CH4/g VSS/d. The micro-organisms from a thermophilic MSW sludge were
increase in partial pressure of CO in the feed was also membrane encased prior to their inoculation in the biore-
observed to have a positive impact on the productivity, actor.110 The maximum productivity of CH4 reported for
although when both high gas recirculation rates and high the biomethanation of solely syngas was 0.109 LCH4/L/d
CO partial pressure were applied the conversion efficiency when using a gas flow rate of 200 sccm, which was compa-
dropped significantly due to the inhibitory effects of CO.64 rable to the productivity of an analogous reactor operated
Similar results were obtained in batch experiments using with free cells.110 However, the increase of the gas loading
a bubble column, as the productivity of CH4 from H2 and rate and the organic loading rate by addition of VFA’s as
CO2 increased from 480 mmol/L/d to 660 mmol/L/h while co-substrate resulted in a sharp increase in the productiv-
raising the gas recirculation rate from 18 L/h to 40 L/h.107 ity of CH4 (0.186 L/L/d) in the reverse membrane reactor,
The continuous biomethanation of syngas has also been whereas in the free cells reactor the productivity gradu-
tested in a packed bed bubble column using a triculture of ally decreased to 0.046 LCH4/L/d as the cells were washed
R. rubrum, M. formicicum and M. barkeri.108 A maximum out due to the more stringent conditions.110 Thus, the use
conversion efficiency of 79% was reached at the lowest of these membranes seems to effectively maintain a high
gas flow rate tested (1.3 sccm) without gas recirculation, concentration of cells in the bioreactor under harsh con-
obtaining a rather low productivity of CH4 of around ditions, yet the effect of the membranes on the transport
of the gaseous substrates to the micro-organisms still determined the kinetics of the growth of the acetogen R.
remains to be investigated. productus on CO using a modified Monod equation in
As shown in this section, the productivity of CH4 is order to simulate the inhibitory effects of high PCO. This
highly dependent on the particular process configura- model was then used for studying the conversion rate of
tion and type of reactor. A high productivity of CH4 can CO as a function of the gas loading rate and the volumet-
be achieved in each type of reactor under specific process ric mass transfer coefficient in a stirred tank reactor and
configurations. Generally, the most influential parameters a bubble column. The growth kinetics of the acetogen C.
affecting the productivity in continuous processes are the ljungdahlii were determined using several dual-substrate
concentration of cells, the gas-to-liquid mass transfer, the kinetic models in order to study the effects of the initial
gas and liquid flow rates, the recycle of these streams and pressure of syngas on the simultaneous consumption of H2
the mixing regime. Nevertheless, the relevance of these and CO.113 Among all kinetic models tested in this study,
parameters is different for each type of reactor. A common the combination of Luong and Monod kinetics was found
feature of stirred tank reactors, bubble columns and gas- to give the best fitting for simulating growth on mixed
lift reactors is that for a given gas loading rate there is a substrates. Other kinetic models based on different equa-
maximum conversion efficiency threshold as a result of the tions have also been proposed. For instance, the kinetic
mixed-flow regime of these reactors when high gas inflow parameters of the growth of C. ljungdahlii on CO and
and gas recirculation rates are applied. In turn, trickle-bed syngas were also determined using the Andrew equation
reactors seem to outperform the other type of reactors in and a novel equation for simulating microbial growth, cell
several aspects due to their plug-flow regime. However, decay and the inhibition of CO.114 Hydrogenogenic cul-
the application of microbubble dispersion in stirred tank tures have also been studied using kinetic models in order
reactors, bubble columns and gas-lift reactors, not studied to determine the optimum process parameters for the con-
yet in syngas biomethanation processes, could enhance tinuous production of H2. A Monod chemostat model was
significantly the mass transfer and hence the performance used to determine the kinetic parameters of R. rubrum
of these reactors. Other aspects of the operation of these growing on CO during washout experiments in a stirred
reactors such as scaling-up issues or economic considera- tank reactor with dual impellers.99 The productivity of H2
tions for each of the process configurations discussed, was then optimized by using this model to determine the
which have not been accounted for here, may also play a optimum dilution rate for the particular process configu-
crucial role when it comes to determine the feasibility of ration of this reactor. Another hydrogenogen, C. hydrog-
these processes. enoformans, was characterized kinetically using the Han
and Levenspiel model in order to study the effects of the
PCO and the influence of the ratio of substrate/biomass on
Kinetics and modeling of syngas the activity of the culture.115 The growth kinetics of other
biomethanation processes relevant microbial groups in syngas biomethanation pro-
Mathematical modeling of bioprocesses is usually applied cesses such as methanogenic archaea have also been evalu-
in order to simulate and predict the outcome of different ated using a number of kinetic models based on Monod
process configurations, as well as to optimize the pro- kinetics, the Andrew equation and a modified Gompertz
cess in terms of yield and productivity of the desirable model, among others.116–119 However, the influence of the
product(s). Unstructured models are perhaps the most partial pressure of CO on the kinetics of this microbial
simplistic expression of mathematical models, using only a group has not been determined yet, as most of these stud-
few state variables for describing the concentration profi les ies have been carried out in the frame of anaerobic diges-
of microbial biomass, substrates and products.111 However, tion processes.
unstructured kinetic models are frequently used as they Despite all microbial groups typically found in a syngas-
are simple and can successfully simulate the effects of converting microbial consortium have been characterized
the main variables on the microbial growth and the pro- using kinetic models, a kinetic model able to describe the
ductivity in batch and continuous processes, being thus a simultaneous growth of these microbial groups in syngas
valuable tool for design and operation of bioprocesses. biomethanation processes has not been developed yet.
Kinetic models used so far for the determination of The development of such a model, including, for exam-
the kinetic properties of several syngas-converting pure ple, the kinetic competition among microbial groups or
cultures under different fermentation conditions and the effects of the operating parameters on the growth
process configurations are shown in Table 3. Vega et al.112 of each microbial group, could contribute to improving
152
Table 3. Unstructured kinetic models used for several acetogens, hydrogenogens and methanogens.
Micro-organism Kinetic Growth rate/Substrate-uptake rate equation Empirical constants Ref.
model
μmax Ks Ki
L
R. productus Andrew L 0.21 h–1 0.044atm PCO < 0,6 atm: Vega et al.112
μ P
max CO
μ= W=∞
L
L 2 PCO < 0,6
L (P ) CO
K s + PCO + atm:
W W = 3 atm
A Grimalt-Alemany, IV Skiadas, HN Gavala
C. ljungdahlii Luong + μ max 0.195 h–1 CO = 0.855 atm Sm = 0.743 Mohammadi et al.113
Monod μ= H2 = 0.412 atm atm
n
S CO S CO SH 2 n = 0.465
− +
K S ,CO + SCO Sm K S ,H 2 +S H 2
C. ljungdahlii Andrew * 0.022 h–1 0.078 mmol CO/I 2 mmol CO/l Younesi et al.114
μ max, COC CO
μ = 2
* *
K CO + CCO + CCO ( ) / Ki
R. rubrum Monod 0.0225 h–1 0.13 gCO/I – Najafpour et al.99
μ maxC S
μ=
K S + CS
C. hydrogenoformans Han and n 8.2 mol CO/g VSS/d 2.1mM SI = 1.37 mM Zhao et al.115
Levenspiel
⎛ S ⎞ S n = 1.4 m =
k = kmax ⎜1 − ⎟ m
⎝ SI ⎠ ⎛ S ⎞ 4.7
S + K m ⎜1 − ⎟
⎝ SI ⎠
M. barkeri 227 Andrew μ max, acS ac 0.038 h–1 1.75 g ac/1 7.37 g ac/1 Yang et al.117
μ= 2
K S , ac + Sac + ( Sac ) / Ki
M. barkeri MS Andrew μ max, acS ac 0.63 h–1 100 g ac/1 0.46 g ac/1 Yang et al.117
μ= 2
K S ,ac + Sac + ( Sac ) / Ki
M. mazei S6 Andrew μ max, acS ac 0.029 h–1 1.00 g ac/1 48.66 g ac/1 Yang et al.117
μ = 2
© 2017 Society of Chemical Industry and John Wiley & Sons, Ltd | Biofuels, Bioprod. Bioref. 12:139–158 (2018); DOI: 10.1002/bbb
K S ,ac + Sac + ( Sac ) / Ki
M. thermoautotrophicum Monod 0.69 h–1 H2 = 20% – Schönheit et al.116
μ C
μ = max S CO2 = 11%
K S + CS
Review: Syngas biomethanation: state-of-the-art review and perspectives
the criteria for the selection of operational parameters due to its lower operational costs, which would provide an
and easing optimization tasks in syngas biomethanation alternative outlet to the excess energy generated during
processes. Additionally, the inclusion of microbial interac- periods of low heat and electricity demand. Other pro-
tions in the model could provide a certain control over the cess configurations considered include the integration of
metabolic pathways dominating the microbial consortium. anaerobic digestion and syngas biomethanation processes
Nonetheless, a more complex model structure would be as their combination could result in a much higher bio-
required in order to include the microbial interactions, mass conversion efficiency and methane productivity. The
thus complicating the estimation of the kinetic parameters gasification of either source-separated organic waste or
describing the behavior of the microbial consortium. More solid digestate and re-injection of syngas into the bioreac-
structured modeling approaches that intended to describe tor would certainly enhance the productivity of methane,
the metabolic network of mixed culture-based processes achieving a nearly complete conversion of the biomass.
have been proposed on the perspective of modeling However, the overall efficiency of the process could be
anaerobic digestion processes 120 or the product distribu- compromised by the high moisture content of the solid
tion in mixed culture fermentations.121 The only attempt digestate as an intensive drying process would be required
of modeling the metabolic network of syngas biomethana- in order to lower its moisture content to the optimal range.
tion processes has been carried out based on a flux balance Therefore, regardless of the process configuration consid-
analysis approach, although the low number of compo- ered, there are still several challenges to be overcome in
nents of the metabolic network monitored over time lim- both the gasification of biomass and the biomethanation of
ited the accuracy of the model.109 However, this work sets syngas in order for these technologies to be commercially
a precedent in modeling of syngas biomethanation pro- applicable.
cesses. Research in this direction is thus encouraged here Research on syngas biomethanation processes have
given the potential of these models for the control and undergone a considerable progress over the last years,
optimization of syngas biomethanation processes. evolving from the early pure culture-based studies aim-
ing at understanding the metabolism of carboxydotrophic
micro-organisms to the current mixed culture-based
Future perspectives approach for its industrial exploitation in the bioenergy
sector. The continuous biomethanation of syngas has
A significant research effort is being made worldwide in so far been successfully applied in a number of bioreac-
order to develop efficient processes for the production of tor designs and process configurations, achieving high
biomethane from agricultural, domestic and industrial yield and conversion efficiency for both CO and H2/CO2.
waste streams. This is of particular importance to several Nevertheless, the performance of the bioreactors could
European countries currently showing an increasing inter- still be further improved in order to achieve a higher con-
est in the production of biomethane, as it can contribute version efficiency and productivity. Recent advances in the
to offset the decreasing trend of production of natural gas design of hollow fiber membrane reactors and microbub-
and reduce their dependency on imported natural gas sup- ble spargers have been applied in other syngas fermenta-
plies. Several process configurations based on the syngas tion processes, and seem a promising way for overcoming
platform are being explored for increasing the share of the mass transfer limitation. More research is also nec-
biomethane to be used as a vehicle fuel or injected into the essary in order to improve our knowledge on microbial
natural gas grid. A combined process of gasification and consortia-driven processes. In this sense, adopting a
syngas biomethanation presents a significant potential as cross-disciplinary approach is crucial for understand-
it offers the possibility of producing renewable methane ing the nature of the metabolic interactions in microbial
from a wide array of waste streams regardless of their consortia, and how these are affected by changes in the
recalcitrance, broadening the spectrum of biomasses cur- operational conditions of continuous processes. Important
rently available to anaerobic digestion systems. In the near advances have been made so far in characterizing the
future, the biomethanation of syngas could become a suit- effects of the operating conditions on the performance of
able alternative for increasing the flexibility of gasification microbial consortia, finding common patterns of activity
plants exploiting syngas for heat and electricity produc- on microbial consortia originated from different sources.
tion. As opposed to the catalytic methanation process, However, further studies are still necessary in this area
the biological conversion of syngas to methane could be in order to find possible interactions between influencing
economically feasible for small-scale gasification plants factors, and to correlate these effects to the behavior of the
population dynamics of microbial consortia. The poten- fuels through microbial intervention: potential and current sta-
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(1989). candidate at the Technical University of
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Gaddy JL, Methane production from synthesis gas using a production through syngas fermen-
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Appl Biochem Biotechnol 24–25:317–328 (1990). consortia. His research interests focus
109. Pereira FM Intensified Bioprocess for the Anaerobic on fermentation-based processes for
Conversion of Syngas to Biofuels. Universidade do Minho, waste valorization.
Braga (2014).
Dr Ioannis V. Skiadas Hariklia N. Gavala

Dr Ioannis V. Skiadas is a chemi- Hariklia N. Gavala is an associate
cal engineer and works as associate professor at the Department of Chemi-
professor at the Chemical Engineering cal and Biochemical Engineering at
department at the Technical University Technical University of Denmark. Her
of Denmark where he teaches biotech- expertise lies in the field of Bioprocess
nology, process design, fermentation Engineering and her current research
technology and unit operations. His focuses on harnessing the potential
research lies in the area of biological conversion of bio- of mixed microbial consortia by optimizing the selec-
mass to chemicals and fuels. He holds a PhD in Chemi- tion and enrichment process as well as the fermentation
cal Engineering from the University of Patras, Greece. operating strategy toward the development of innovative
and cost-efficient processes for production of chemicals,
materials, and biofuels. She holds a PhD in Chemical
and Biochemical Engineering from University of Patras,
Greece.

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Review

Syngas biomethanation: state-of-the-

Keywords: biomethanation; synthesis gas; carbon monoxide; methane; microbial consortia;

Introduction Brazil, China, and India, among others.1 An example of

T decades along with the foreseen future scarcity

thermochemical and biochemical conversion processes, as Syngas biomethanation versus

of these respiratory processes has been extensively Cross-feeding relationships

consortia on a simultaneous process of thermophilic methanogenic precursors in mixed microbial consortia.

Dr Ioannis V. Skiadas Hariklia N. Gavala

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