Bioresource Technology 248 (2018) 20–28

Contents lists available at ScienceDirect

Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Review

Anaerobic digestion of food waste: A review focusing on process stability

Lei Li, Xuya Peng ⇑, Xiaoming Wang, Di Wu
Key Laboratory of Three Gorges Reservoir Region’s Eco-Environment, Ministry of Education, Chongqing University, Chongqing 400045, China

h i g h l i g h t s

 AD is a well-established technology for FW management.

 Performance instability is a common operational issue for AD of FW.
 Methods for improving the stability of anaerobic digesters are reviewed.
 Process monitoring and control are suitable for evaluating digester operation.
 Microbial management facilitates early diagnosis and optimization of digesters.

a r t i c l e i n f o a b s t r a c t

Article history: Food waste (FW) is rich in biomass energy, and increasing numbers of national programs are being estab-
Received 28 April 2017 lished to recover energy from FW using anaerobic digestion (AD). However process instability is a com-
Received in revised form 30 June 2017 mon operational issue for AD of FW. Process monitoring and control as well as microbial management
Accepted 4 July 2017
can be used to control instability and increase the energy conversion efficiency of anaerobic digesters.
Available online 6 July 2017
Here, we review research progress related to these methods and identify existing limitations to efficient
AD; recommendations for future research are also discussed. Process monitoring and control are suitable
Keywords:
for evaluating the current operational status of digesters, whereas microbial management can facilitate
Food waste
Anaerobic digestion
early diagnosis and process optimization. Optimizing and combining these two methods are necessary
Process stability to improve AD efficiency.
Process monitoring and control Ó 2017 Elsevier Ltd. All rights reserved.
Microbial management

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
2. Anaerobic digestion of food waste . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
3. Process monitoring and control. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
3.1. Process parameters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
3.2. Process monitoring . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
3.3. Process control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
4. Microbial management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
4.1. Anaerobic microbiomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
4.1.1. ‘‘Who is there?” and ‘‘who is doing what with whom?” . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
4.1.2. How they behave against disturbances? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
4.2. Microbial indicators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
4.2.1. Ecological parameters. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
4.2.2. Indicative microorganisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
4.3. Biotechnological intensification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

⇑ Corresponding author at: No. 174, Shapingba Zhengjie Street, Chongqing

400045, China.
E-mail address: xuyapengcqu@126.com (X. Peng).

http://dx.doi.org/10.1016/j.biortech.2017.07.012
0960-8524/Ó 2017 Elsevier Ltd. All rights reserved.
 L. Li et al. / Bioresource Technology 248 (2018) 20–28 21

5. Research outlook . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
6. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

1. Introduction 2. Anaerobic digestion of food waste

Food waste (FW) consists of materials intended for human con- Food waste constitutes one of the largest components of
sumption that are ultimately discarded, lost, degraded, or contam- waste around the world (Capson-Tojo et al., 2016; Zhang et al.,
inated (Girotto et al., 2015). Owing to global economic 2014, 2013). Its theoretical methane production rate typically
development and population growth, FW from residential, com- ranges from 0.4 to 0.5 L CH4 g VS 1 (Li et al., 2015, 2014;
mercial (e.g., restaurants), institutional (e.g., school cafeterias), Nagao et al., 2012), suggesting great potential for energy recov-
and industrial (e.g., food-processing factories) sources is being gen- ery. In view of this, interest in AD of FW has escalated over the
erated at an increasingly high rate (Dai et al., 2013; Girotto et al., past few decades. Capson-Tojo et al. (2016) and Uçkun Kiran
2015). Food safety issues frequently occur due to incomplete FW et al. (2014) previously reported and reviewed laboratory-scale
management systems, and the disposal of FW is attracting wide- studies of FW treatment using AD. In many European and devel-
spread attention in many countries (Li et al., 2015; Thi et al., oped Asian countries, AD has been widely applied to treat FW on
2015). Because of its high moisture content, low calorific value, an industrial scale. Germany, Spain, England, and Korea are all
and high lability, traditional approaches for FW disposal, such as equipped with full-scale AD plants with a capacity of 2500 tons
incineration, landfills, composting, thermal treatment, and animal per year or larger (Chiu and Lo, 2016; Thi et al., 2015). In devel-
feed, are sub-satisfactory with respect to sustainability, environ- oping countries, such as India and China, various institutes and
mental impact, and investment (Girotto et al., 2015; Han et al., non-governmental organizations have established different types
2016). In contrast, anaerobic digestion (AD) is an effective of anaerobic digesters on household and commercial scales to
approach for FW management and offers many environmental develop AD technology for FW treatment (Thi et al., 2015). For
benefits, such as generation of renewable energy and production example, a pilot scale study in India implemented AD to treat
of soil amendments, alcohol, volatile fatty acids (VFAs), and other FW, and several institutes have developed biogas plants. In China,
valuable materials (Capson-Tojo et al., 2016; Han et al., 2017, demonstration projects for FW disposal were initiated in 2010
2015; Li et al., 2015; Zhang et al., 2013). Nevertheless, AD often and since then a total of 100 cities have been chosen as the pilot
suffers from process instability, which is further exacerbated when cities. Among those projects, more than 90% adopted AD technol-
treating FW characterized by high oil, salt, and protein contents. ogy for FW disposal.
Process monitoring and control are widely accepted methods for Despite continuously increasing interest and popularity, large-
improving AD stability and efficiency (Boe et al., 2010; Li et al., scale FW anaerobic digesters are usually operated with a low
2014; Molina et al., 2009). Since the 1940s, a large number of stud- organic loading rate (OLR), from 1 to 4 g VS L 1 d 1, or long
ies have been carried out to identify process indicators (particu- hydraulic retention time (HRT), up to 80 d (Banks et al., 2011;
larly physicochemical parameters such as gas production, pH, Tampio et al., 2014; Zhang et al., 2012). The resulting low biogas
VFA, and alkalinity) that can effectively reflect the operational sta- production reduces the efficiency and economic feasibility of the
tus of AD (Boe et al., 2010; Kleyböcker et al., 2012b; Kroeker and process. Raising the OLR (hydraulic or organic loads) can help
Lapp, 1979; Li et al., 2014; Lv et al., 2014; Polag et al., 2015). Accu- increase gas production and improve process efficiency, but insta-
rate methods and robust equipment for monitoring those above bility during continuous AD operation is a major concern
mentioned process indicators have also developed explosively (Capson-Tojo et al., 2016; Chiu and Lo, 2016). The characteristics
(Boe et al., 2007; Jantsch and Mattiasson, 2004; Jin et al., 2017; of FW (high labile organic matter, salt, oil, and protein contents;
Lomborg et al., 2009; Pind et al., 2003). On the other hand, AD is low C/N ratio; and insufficient trace elements) makes anaerobic
a biochemical process with multiple phases, and its overall process digesters prone to acidification, ammonia, salt, and long chain
stability and efficiency rely on multiple syntrophic interactions fatty acid (LCFA) inhibition, and nutrient deficiency (Banks
among different taxa (Goux et al., 2015; Lin et al., 2016b; Poirier et al., 2012; Dai et al., 2013; Gao et al., 2015; Li et al., 2015;
et al., 2016a). Thus, understanding the dynamics of microbial com- Zhang et al., 2013). The reestablishment of stable biogas produc-
munities in digesters is crucial for optimizing AD. Consequently, tion after digester deterioration is a long-term process. Consider-
the management of microbial communities in anaerobic digesters ing that biogas plants often are operated under limited profit,
has become a widely employed technique in recent years, and technical problems and upsets involving a long downtime or high
numerous studies have been conducted to identify anaerobic repair cost can have serious economic consequences (Ganidi et al.,
microbiomes, establish microbial indicators, and develop biotech- 2009; Lienen et al., 2013; Zhang et al., 2013). Therefore, process
nological methods to improve AD (Carballa et al., 2015; Goux instability is a serious limitation to AD of FW. Process monitoring
et al., 2015; Li et al., 2016; Poirier et al., 2016a,b). In this context, and control as well as microbial management are widely used for
we review a large number of studies to summarize the current mitigating process instability and improving AD. In view of the
development status of AD for FW treatment. We then discuss fact that process instability is a ubiquitous phenomenon, and
and compare physiochemical-based versus microbial-based tech- the methods for controlling instability in various digesters are
niques for managing anaerobic digesters. The main goals of this interlinked, a comprehensive summary of achievements in AD
study were to summarize previous research achievements on con- systems fed with various substrates may provide guidance for
trolling and mitigating digester instability, refine the existing lim- mitigating instability of anaerobic digesters used for FW treat-
itations to AD efficiency, and provide recommendations for future ment. Therefore, the following review focuses on, but is not lim-
research. ited to, FW-AD systems.
22 L. Li et al. / Bioresource Technology 248 (2018) 20–28

3. Process monitoring and control anaerobic reactors and provide guidance for process diagnosis
(Ahring et al., 1995; Molina et al., 2009). Thus, various monitoring
Employing scientific methods for monitoring and controlling methods and equipment have been developed. To provide real-
anaerobic digesters is helpful for achieving efficient and stable per- time data, ideal monitoring methods should be in-situ or in-line,
formance (Boe et al., 2010; Li et al., 2014; Molina et al., 2009). The automated, and continuous. Spanjers and van Lier (2006) surveyed
development of a monitoring system requires accurate selection of approximately 400 full-scale AD plants for wastewater treatment
parameters that provide valuable information on the metabolic and found that in-situ and in-line instrumentation at 95% of plants
status of digesters, development of ideal measuring methods for was limited to measurements of pH, temperature, water flow, bio-
the detection of these parameters, and robust on-line monitoring gas flow, level, and pressure. Madsen et al. (2011) also reported
devices. Once monitoring systems detect symptoms of instability, that many plants are operated based on ex-situ analysis and only
the control system must adopt targeted actions to restore process sensors for parameters such as pH, temperature, redox potential,
performance. gas production rate, and gas composition are employed in-situ or
in-line.
Online or in-situ monitoring is employed more extensively in
3.1. Process parameters
laboratory-scale than in full-scale systems. Feitkenhauer et al.
(2002) reported a simple two-point, online titration for determin-
Since the 1940s, studies have been devoted to investigating
ing VFA concentration in wastewater from textile finishing indus-
ideal process parameters (i.e., early warning indictors with high
tries as a reliable method for process control without the use of
sensitivity, fast response, and low monitoring cost). For almost
expensive analytical devices; good reproducibility of VFA concen-
70 years, studies have explored the effectiveness of substrate con-
trations was demonstrated and standard deviations were below
version (based on chemical oxygen demand (COD), and total solid
±1% of measured concentrations. However, solid–liquid separation
(TS) and volatile solid (VS) removal rates), intermediate metabo-
was not considered in this study, which prevents its application in
lites (based on total and individual VFAs, pH, H2, CO, and alkalin-
high-solid systems. Pind et al. (2003) invented a new VFA sensor
ity), and end metabolic products (based on methane yield, gas
system consisting of an in-situ rotating filter, an ultrafiltration unit,
composition, and gas production rate) as indicators of process fail-
a sample preparation unit, and a GC unit for online monitoring of
ure (Boe et al., 2010; Graef and Andrews, 1974; Kroeker and Lapp,
VFAs in animal slurry or manure. Concentrations measured with
1979; Li et al., 2014; Switzenbaum et al., 1990). The thresholds of
the VFA sensor system were strongly correlated with offline mea-
these early warning indictors have also been investigated exten-
surements, and the system can take measurements every 15 min.
sively, and researchers have proposed various normal operating
However, the filtration system requires a high level of maintenance
conditions based on this information. For example, Bernard et al.
due to membrane fouling. Jantsch and Mattiasson (2004) described
(2001) suggested that digester stability is preserved when the
an automated system for monitoring alkalinity, in which liquid
VFA concentration is kept below 1500 mg L 1 and the ratio of
samples are filtered using a nylon cloth (gap size: 20 mm); how-
intermediate to partial alkalinity (IA/PA) is less or equal to 0.3.
ever, membrane fouling was still a significant problem. Boe et al.
Martín-González et al. (2013) reported that to achieve stable reac-
(2007) developed an innovative online VFA monitoring system
tor performance, VFA and total alkalinity (TA) concentrations
based on headspace gas chromatography (HSGC). The method
should be maintained at 2500–3500 and 13,000–15,000 mg L 1,
applies ex-situ VFA stripping based on variable headspace volume
respectively, and the IA/PA ratio should be kept below 0.3. Li
and gas analysis using gas chromatography with flame ionization
et al. (2014) concluded that the total VFA concentration, VFA/TA,
detection. In each extraction, digester samples are acidified with
and the ratio of bicarbonate to total alkalinity (BA/TA) can be com-
H3PO4 and NaHSO4, and heated to strip VFAs into the gas phase.
bined for rapid and effective early warning of process instability.
The gas is sampled with a low friction glass syringe, and then
They reported thresholds for VFA/TA and BA/TA of 0.35 and 0.8,
injected into the GC for measurement. Gas extraction avoids the
respectively, and suggested that the use of relative changes in
issue of fouling, and thus has great potential for application in hos-
VFA concentrations is more feasible than absolute concentrations
tile high-solid environments. However, complex equipment, high
for reflecting process instability. In addition to these conventional
energy requirements, high consumption of chemical agents, and
process parameters, innovative early warning indicators are being
difficult maintenance prevent its commercial application. Recently,
explored. For example, studies have proposed aromatic acids
many researchers have evaluated the feasibility of near infrared
(Hecht and Griehl, 2009), VFA/Ca, PO4/Ca (Kleyböcker et al.,
spectroscopy (NIR) for on-line determination of VFAs, TS, VS, and
2012b), and the stable isotope composition of biogas (such as
alkalinity in anaerobic digesters (Charnier et al., 2017; Krapf
d13CH4 and d13CO2) (Lv et al., 2014; Polag et al., 2015) as indicators
et al., 2013; Lomborg et al., 2009). Compared with other tech-
of process failure. However, several of these parameters are only
niques, NIR has multiple benefits such as nondestructive measure-
applicable in specific AD systems, and some studies have reported
ment, high efficiency, fast detection, and good reproducibility.
conflicting results.
Thus, it is suitable for rapid on-site testing and continuous online
Above all, there are no universally accepted diagnostic parame-
analysis. However, sophisticated equipment and careful mainte-
ters for process stability and multiple thresholds for some widely
nance still prevent the technique from being widely commercial-
used warning indicators have been recommended. In addition, pre-
ized. Simple, rapid, and accurate online techniques for process
vious studies have pointed out that the ability of early warning
monitoring are still being investigated.
parameters to predict future performance and stability is limited
because the majority of parameters are intermediate metabolites
3.3. Process control
or metabolic end products of AD, and their fluctuations are the
result of instability but not the origin (Carballa et al., 2011).
Careful management and early detection of AD instability are
essential for minimizing economic loss. However, as these preven-
3.2. Process monitoring tive measures often fail, it is also important to establish a solid
knowledge of control strategies for process recovery and imple-
Despite limitations to the prediction of future performance and ment these strategies as quickly as possible (Li et al., 2014;
stability, many researchers believe that monitoring parameter Regueiro et al., 2015). At present, most control strategies are
trends are sufficient for evaluating the ongoing performance of problem-oriented. For example, a drastic decrease in OLR is the
 L. Li et al. / Bioresource Technology 248 (2018) 20–28
most frequently used method for mitigating OLR stress, but this
strategy simultaneously decreases the utilization capacity of diges-
ters. Additionally, because overloading always causes acidification
and VFA accumulation, alkaline substances can be added simulta-
neously to counteract this problem. For example Goux et al.
(2015) restored an acidified reactor through OLR reduction and
NaOH–NaHCO3 addition. Kleyböcker et al. (2012a) compared the
effectiveness of NaOH and CaO additions for process recovery.
Though both additives increased the pH to a neutral level
(pH > 7.0), the reactor treated with NaOH suffered acidification
again following an increase in OLR; in contrast, the addition of
CaO enabled aggregate formation. Calcium phosphate compounds
were identified as the basis of these aggregates, and phosphate
release by phosphorus-accumulating organisms was observed
after VFA accumulation. Aggregate formation can efficiently
improve process stability and enhance its resistance. However, this
method may be effective only in anaerobic digesters treating
sludge, as phosphate is not commonly founded in other digesters.
Strategies for treating ammonia inhibition typically are based on
reducing ammonia concentrations, and reductions in digesters or
in feed are feasible. Pre-treatment and co-digestion are common
techniques for decreasing ammonia in substrates. Alternatively,
methods such as dilution, struvite precipitation, stripping, mem-
brane technology, and ion-exchange typically are used to remove
ammonia in digesters (Chen et al., 2014; Serna-Maza et al., 2014;
Tampio et al., 2014; Tao et al., 2017). Among these, pre-
treatment and co-digestion are expensive and complex, whereas
dilution and precipitation reduce the effective space in reactors,
resulting in decreased OLR. To effectively remove ammonia via
stripping, the pH of effluent must be increased to 10–11, and a con-
stant heat and/or gas flow is required. Membrane units often suffer
from fouling, whereas high dosage requirements and high costs are
major concerns associated with ion-exchange techniques (Tao
et al., 2017). Thus, most of these methods have low efficiency
and feasibility at full scale conditions. Consequently, although
ammonia inhibition is a well-known problem, many full-scale bio-
gas plants in Denmark are operated without alleviating this prob-
lem, leaving digesters to operate under ‘‘inhibited steady-state”
conditions. Under such conditions, the coexistence of high ammo-
nia and VFA concentrations allows digesters to run stably within a
neutral pH range, but the overall methane production typically is
reduced by up to 30% (De Vrieze et al., 2016; Tsapekos et al., 2017).
Therefore, process monitoring and control based on physico-
chemical parameters (defined as routine process monitoring and
control) have the following limitations: 1) no universally accepted
early warning indicators exist, and the monitoring of physico-
chemical parameters cannot predict future performance and sta-
bility; 2) only a few parameters can be monitored on-line, which
weakens the timeliness of process diagnosis; and 3) process con-
trol is a remedial measure that is difficult to implement success-
fully. Therefore, process optimization is difficult to achieve. Based
on a microbiological perspective, many studies have reported that
process instability is the result of imbalanced microbial metabo-
lism. Therefore, understanding the composition and behavior of
microbial communities is helpful for improving AD, and the con-
cept of microbial management is attracting widespread attention
(Carballa et al., 2015; Goux et al., 2015; Tang et al., 2015).
4. Microbial management
Microbial management aims to improve methane production
and process stability by initiating a change in microbial communi-
ties. Three requirements for microbial management of anaerobic
reactors have been identified: 1) understanding the anaerobic
microbiome, including ‘‘who is there,” ‘‘who is doing what with
23
whom,” and ‘‘how they behave against disturbances”; 2) establish-
ing early warning microbial indicators; and 3) developing biotech-
nological intensification methods (Carballa et al., 2015; de Los
Reyes et al., 2015).
4.1. Anaerobic microbiomes
4.1.1. ‘‘Who is there?” and ‘‘who is doing what with whom?”
Anaerobic digestion is an important microbial process in which
interacting microbial populations convert a variety of complex
organic materials to methane through the processes of hydrolysis,
acidogenesis, acetogenesis, and methanogenesis. A variety of tech-
niques have been applied to study microbial community composi-
tions in AD systems. Early techniques, such as fluorescence in situ
hybridization (FISH), denaturing gradient gel electrophoresis
(DGGE), terminal restriction fragment length polymorphism
(TRFLP), and real-time polymerase chain reaction (qPCR), are
time-consuming, have relatively low-throughput, and can detect
only dominant microbes. More recent high-throughput technology
(e.g., the Illumina MiSeq platform) allows identification of less
abundant microbes due to dramatically increased sequencing
depth (Vanwonterghem et al., 2014b). This technique enables the
relative abundance of most microbes present in digesters to be
determined.
Genome sequencing reflects the spatial existence of bacteria
(live, dormant, and dead) in the form of cellular quantities, and
the resulting spatial ecological niches are used to clarify ‘‘who is
there”. In contrast, proteome and transcriptome sequencing indi-
cate the actual metabolic roles of microbes based on cellular activ-
ity, and the resulting functional ecological niches can be used to
answer ‘‘who is doing what with whom” (Heyer et al., 2016; Lin
et al., 2016b). Although isolation and cultivation is the conven-
tional method for function identification, the majority of microor-
ganisms in AD systems have not yet been cultivated. Moreover, the
metabolic characteristics of culturable microorganisms may differ
from those in natural communities due to the characteristics of
complex microbial networks (Vanwonterghem et al., 2014b). The
development of the ‘omics’ approach has opened new avenues
for analyzing community structure and function. Whereas metage-
nomics is used to indicate genetic potential, metatranscriptomics
and metaproteomics can identify gene expression and better
represent the physiological state of microbial communities. For
example, Lin et al. (2016a,b) revealed a temperature-regulated
mechanism using metatranscriptomics and showed that methano-
genesis and oxidative phosphorylation are positively correlated to
reactor efficiency. Elevated temperature can reduce the diversity of
functional pathways but enhance central functional pathways,
thereby increasing the conversion efficiency of substrate to
methane. Euryarchaeota are the main organisms participating in
core functional pathways. Heyer et al. (2013) applied metapro-
teomics to monitor microbial communities at the functional level.
They identified Methanosarcinales as dominant methanogens and
acetyl-CoA decarbonylase/synthase, which is affiliated with
acetoclastic methanogenesis (AM), as the only related enzyme
associated with methane production; therefore, the versatile
Methanosarcinales only participated in AM. As microbes live within
complicated networks and engage in a multitude of interactions,
such as competition, syntrophy, and predation, identifying poten-
tial interactions among microbial populations at the community
level is necessary to understand AD systems (Wu et al., 2016). Net-
work analysis has been used to deduce potential interactions
among microbial populations. For example, by using network anal-
ysis to evaluate microbial interactions in digesters, Wu et al. (2016)
detected a clear successional pattern (increasing modularity but
decreasing connectivity) among microbial populations. Clostridiales
were identified as keystone organisms in the networks (i.e., they
24 L. Li et al. / Bioresource Technology 248 (2018) 20–28
had strong effects on other species), suggesting their important
role in maintaining process stability. Lin et al. (2016b) suggested
that the existence of a larger number of microbial interactions
may optimize resource utilization, and thereby increase methane
production efficiency.
4.1.2. How they behave against disturbances?
Anaerobic digestion is a highly sensitive process, and small
variations in operational conditions can induce fluctuations in
microbial community composition and activity. However, if phys-
iological compensation within the microbial community is possi-
ble, reactor performance will not be adversely affected despite
changes in microbial community composition and abundance
(Theuerl et al., 2015). Ecological studies have identified three basic
mechanisms for maintaining community function (i.e., reactor per-
formance) independent of process disturbance: resistance (popula-
tions are able to withstand changes without variations in
composition), resilience (populations rebound following a distur-
bance), and redundancy (a disturbed population is replaced by a
new group with the same function) (Allison and Martiny, 2008).
Hydrolytic and acidogenic bacteria are highly dynamic and rely
on redundancy to maintain overall community function, whereas
syntrophic populations tend to be more resilient (Niu et al.,
2015b; Werner et al., 2011). Syntrophic bacteria perform specific
metabolic functions, and a disturbed community is likely to
rebound to its previous composition (Carballa et al., 2015;
Werner et al., 2011). Methanogens have displayed both redundant
and resilient behavior. Some researchers have also extended these
concepts to specific microorganisms (Goux et al., 2015; Niu et al.,
2015a,b). For example, Goux et al. (2015) concluded that Bac-
teroidales are resistant to high VFA concentrations and low pH.
Carballa et al. (2015) identified Methanobacteriales as resistant,
Methanosaeta as redundant, and Methanosarcina and Methanomi-
crobiales as resilient and redundant. The succession of resilient
groups is closely related to process performance; thus, these
groups play an important role in indicating the actual state of AD
(Li et al., 2016). The identification of microbes that are resistant
to stress or emerge after stressful conditions can provide a basis
for biotechnological intensification (Poirier et al., 2016a,b).
Under high disturbance levels, the above three mechanisms
may not be sufficient to maintain stable microbial community
function, and changes in community structure and function may
simultaneously occur. In this case, the microbiological mechanisms
of process instability should be elucidated, including successions in
microbial communities during the course of instability, the origin
of these successions, the interactions among microbial communi-
ties, and the correlations between microbial communities and pro-
cess stability. Related studies have reported microbial community
succession in anaerobic digesters during different process stages
(Razaviarani and Buchanan, 2015; Luo et al., 2015; Goux et al.,
2015), and numerous stress-tolerant microorganisms have been
identified. For example, Poirier et al. (2016b) reported microbial
community shifts in reactors with total ammonia nitrogen (TAN)
concentrations ranging from 0.0 up to 50.0 g L 1. They observed
high tolerance of Treponema and Methanosarcina thermophila to
TAN stress. Hao et al. (2015) observed that Methanosarcina can cat-
alyze AM when exposed to high ammonia stress (free ammonia
(FAN) concentrations of up to 916 mg L 1). In contrast, some stud-
ies have shown that increasing ammonium concentrations can ini-
tiate a shift in mesophilic acetate degradation from AM to
hydrogenotrophic methanogenesis (HM) and syntrophic acetate
oxidation (SAO) (Sun et al., 2016, 2014; Gao et al., 2015). Besides,
higher VFA concentrations favor the growth of Methanosarcina over
Methanosaeta and salt accumulation favors Methanoculleus as
hydrogenotrophic methanogens have also been reported (Franke-
Whittle et al., 2014; Guo et al., 2014; Li et al., 2015; Lim et al.,
2013). Some researchers have also attempted to link community
characteristics with process stability (Li et al., 2015; Carballa
et al., 2011; Nakasaki et al., 2015). For example, Li et al. (2015)
introduced OLR disturbance in a mesophilic anaerobic digester
treating FW and found that the relative abundance of acid-
producing bacteria and syntrophic VFA oxidizers increased dra-
matically under high OLR, whereas the abundance and activity of
their syntrophic partners (hydrogenotrophic methanogens)
decreased. The succession of methanogens during disturbance
may be ill-suited for operation under high OLR, and thus may cause
process deterioration. Nakasaki et al. (2015) used qPCR to identify
associations between methane production rate and archaea cell
density—under very high OLR, VFA concentration increased,
archaeal cell density decreased, and methane production subse-
quently decreased. Werner et al. (2014) reported that anaerobic
digesters rely on the diversity and distribution of parallel meta-
bolic pathways mediated by complex syntrophic microbial com-
munities to maintain robust and optimal performance. Therefore,
reduced diversity and evenness may be responsible for process
instability.
Despite various causes of instability have been suggested, there
is still a gap in understanding the instability mechanisms. Previous
studies often simply evaluated reactor performance (stable or
deteriorated) and then explained such performance based on the
community characteristics of a particular profile (e.g., composition,
amount, activity, metabolic pathways, diversity, and evenness).
These results are likely biased because communities may undergo
several changes simultaneously. Future studies should combine
meta-omics with advanced visualization and isotope labeling tech-
niques to comprehensively evaluate anaerobic microbiomes
(including taxonomic and functional composition, metabolic path-
ways, and activity). Combing this information with data on reactor
performance during different operational conditions (especially
transitional states) can help elucidate the mechanisms of process
instability.
4.2. Microbial indicators
Understanding anaerobic microbiomes is necessary to identify
microbial-based early warning indicators. Although microbial indi-
cators cannot be detected as quickly as process parameters due to
limitations of monitoring techniques, it is recognized that fluctua-
tions in process parameters are the result of microbial succession
due to environmental stress. Thus, changes in microbial indicators
will occur earlier than changes in process parameters (Carballa
et al., 2015; Vanwonterghem et al., 2014b; Williams et al., 2013).
Two types of microbial early warning indicators have been pro-
posed: ecological parameters and indicative microorganisms.
4.2.1. Ecological parameters
Various ecological parameters have been applied based on the
concept of microbial resource management. The commonly used
parameters of richness, evenness, and dynamics correspond to
‘‘who is there,” ‘‘who is doing what with whom,” and ‘‘how they
behave against disturbances”. Richness may be an important per-
formance indicator because richer communities correspond to a
higher number of possible pathways for substrate degradation,
and thereby increased possibility of adapting to disturbance
(Carballa et al., 2011; Regueiro et al., 2014). Evenness is a measure
of the equitability of abundance, which strongly influences ecosys-
tem stability from a theoretical point of view. High evenness
reflects an adequate distribution of dominant and sparse species,
indicating that the community employs a variety of metabolic
pathways. In contrast, low evenness indicates that the community
is dominated by one or a few species, and resistance to perturba-
tion will only occur if the dominant species are tolerant of the dis-
 L. Li et al. / Bioresource Technology 248 (2018) 20–28
turbance (Kinet et al., 2015; Wittebolle et al., 2009). Dynamics
evaluations are used to determine the ability of microbial commu-
nities to adapt to changing or stressful conditions (De Vrieze et al.,
2016). Some studies have attempted to link these parameters with
process stability. Carballa et al. (2011) analyzed the statistical cor-
relations between ecological parameters and VFA/TA and biogas
production. They observed that both richness and evenness are
positively correlated with biogas production and negatively corre-
lated with VFA/TA, whereas dynamics is not significantly corre-
lated with either performance parameter. Thus, dynamics
evaluations are not sufficient to reveal correlations between com-
munity composition and reactor function, whereas a more even
and diverse bacterial community represents a well-functioning
reactor. Wittebolle et al. (2009) found that initial community even-
ness is a key factor for preserving ecosystem stability. In contrast,
Kinet et al. (2015) observed the coexistence of weak richness and
high cellulolytic potential, suggesting that simpler microbial com-
munities correspond to greater process stability. Li et al. (2016)
observed that certain ecological parameters either show no obvi-
ous changes among different operational stages or fluctuate ran-
domly and concluded that no correlations exist between
ecological parameters and process stability. Goux et al. (2015) also
claimed that richness, evenness, and diversity indices are inade-
quate for predicting process failure and process perturbation. Thus,
it is still controversial what level of community complexity a
healthy, well-balanced, efficient microbial consortium should have
for optimal biogas production. This may be because general ecolog-
ical indices describe community diversity independently of com-
munity composition. High richness or diversity cannot guarantee
a stable and resilient community because these indicators do not
provide information on the presence of stress-resistant species or
the direct adaptive potential of the community (De Vrieze et al.,
2016; Li et al., 2015). The correlation between dynamics and pro-
cess stability is more elusive, as reflected in Section 4.1.2. There-
fore, an increasing number of researchers are realizing that
indicative microorganisms are fundamental to the AD process,
regardless of their abundance.
4.2.2. Indicative microorganisms
Previous studies have induced various environmental distur-
bances in digesters to investigate community succession during
different operating stages and subsequently selected microbes
related to process performance as indicative microorganisms/
biomarkers. Li et al. (2016) introduced OLR disturbance into a
mesophilic anaerobic digester treating FW to induce various oper-
ating stages (stable, disturbance, recovery, and stable). They iden-
tified Syntrophomonas and Treponema as resilient groups, whose
abundances increased during the deteriorative stage and
rebounded after disturbance, suggesting that these microbes can
be used as potential early warning indicators. Williams et al.
(2013) monitored microbial populations in a full-scale anaerobic
digester fed with FW for 18 months. They observed decreasing
methanogenic populations in response to increasing VFA content
and instability. These results suggest that monitoring of microbial
populations can provide valuable insight into the complex pro-
cesses occurring within digesters and can be used to predict and
optimize AD performance. Poirier et al. (2016a) explored microbial
early warning indicators of phenol inhibition and identified the
genus Methanosarcina and the family Syntrophomonadaceae as
key organisms for efficient AD performance under uninhibited con-
ditions. However, Methanoculleus tended to replace the dominant
Methanosarcina with increasing initial phenol concentrations;
among syntrophic populations, Synergistaceae proliferated at the
expense of Syntrophomonadaceae. Because AD performance was
not impaired by these shifts, these microbes may be possible indi-
cators of phenol inhibition. Similarly, Regueiro et al. (2015)
25
showed that Tepidimicrobium and Actinomyces are indicative of
process acidification, whereas Porphyromonadaceae are important
to reactor recovery. Goux et al. (2015) reported that most bacteria
and archaea show redundant functional adaptation to changing
environmental conditions and the replacement of the dominant
Methanosaeta by Methanoculleus may be a potential indicator of
acidosis.
Unfortunately, there seems to be no difference between the use
of indicative microorganisms and process parameters as early
warning indicators, as both indices are variable and depend on
the individual AD system. In fact, whether deterministic correla-
tions between environmental conditions and community structure
exist is a controversial subject. There are two ecological mecha-
nisms of community assembly: niche-based theory and neutral
theory. Historically, community composition is thought to be gov-
erned by niche-based theory, which supports the idea that com-
munities are shaped by deterministic factors such as competition
and niche differentiation (Luo et al., 2015). According to this the-
ory, community composition should converge towards a single
pattern under similar environmental conditions; therefore, it
may be possible to reliably predict changes in community struc-
ture and function over time under controlled conditions, and uni-
versally applicable biomarkers may exist. In contrast, neutral
theory only considers stochastic processes, disregards competition,
and predicts random drift of populations under identical condi-
tions because it assumes that all individuals are ecologically equiv-
alent (Vanwonterghem et al., 2014a). According to this theory,
biomarkers inevitably vary among different systems. Luo et al.
(2015) and Vanwonterghem et al. (2014a) ran multiple parallel
digesters under controlled conditions to examine the role of
stochastic and deterministic factors in shaping microbial commu-
nities. They found that deterministic processes may play a larger
role in microbial community dynamics than previously realized,
whereas stochastic factors do not strongly influence the commu-
nity composition and activity in biogas reactors. However, Goux
et al. (2015) observed that stable operational conditions led to sim-
ilar microbial populations in four reactors; once the environment
became deterministic due to increased feeding rate, the microbial
populations in different reactors began to diverge. Other studies
have also suggested that both deterministic and stochastic pro-
cesses play a role in structuring microbial communities (Caruso
et al., 2011; Ofitßeru et al., 2010). In view of the fact that the confor-
mation of community succession to niche theory is a prerequisite
for the universality of biomarkers, designing controlled conditions
and replicate experiments to clarify the mechanisms and factors
that affect community assembly is paramount.
Besides, most previous studies have focused on community suc-
cession during different operational stages, simply used altered
microbes as indicative microorganisms, and did not explore the
correlations in a statistical sound manner. It could be another rea-
son for different indicative microorganisms identified. Statistical
analysis is necessary to investigate the correlations between
microbial communities and process stability in order to produce
reliable and reproducible results. A few studies have made prelim-
inary attempts. For example, De Vrieze et al. (2016) recently fol-
lowed four full-scale AD plants for one year to link operational
characteristics with microbial community composition and struc-
ture. Statistical analysis demonstrated that each of the four diges-
ters hosted a unique microbial community including two
phylotypes belonging to the genus Syntrophomonas and one
unclassified bacterium; these microorganisms were considered to
be biomarkers of the community. Heyer et al. (2016) evaluated
the microbial communities of 40 samples from 35 different indus-
trial biogas plants using metaproteomics. Three potential biomark-
ers were identified: 1) 5,10-methylenetetrahydromethanopterin
reductase (Q8TXY4 Euryarchaeota) for high TAN, 2) the order Ther-
26 L. Li et al. / Bioresource Technology 248 (2018) 20–28
motogales for high process temperature, and 3) decreased methyl-
coenzyme M reductase (MCR) [P07962 MCR subunit alpha (Metha-
nosarcina barkeri str. Fusaro)] for high OLR. As these biomarkers
were identified in full-scale AD reactors with diverse operating
conditions, the very high number of metaproteins, taxonomic
orders, and biological processes considered in the statistical analy-
sis as well as the large biological variation between individual
plants caused the low explanation of statistical results. For exam-
ple, the two main components of the principal component analysis
(PCA) for taxonomic orders, biological processes and the metapro-
teins explained only 25, 33 and 28% of the variances, suggesting
the results are likely biased. Nevertheless, this research can serve
as a template to encourage more systematic studies to screen more
specific core taxonomies and core functions in digesters with com-
parable substrate supply and similar process conditions.
4.3. Biotechnological intensification
In addition to early diagnosis, understanding anaerobic micro-
biomes can provide a basis for the development of targeted
biotechnological intensification methods. Bioaugmentation is a
well-known biotechnological intensification method that refers
to the practice of adding specific microorganisms to a system to
enhance a desired activity and improve efficiency (Li et al.,
2017). Bioaugmentation has been employed to decrease the recov-
ery time of anaerobic digesters stressed by propionate
(Venkiteshwaran et al., 2016), organic overloading (Tale et al.,
2011), and oxygen (Schauer-Gimenez et al., 2010) or ammonia
(Li et al., 2017), and to improve biogas production in stable diges-
ters (Bagi et al., 2007). However, previous studies have reported
transient improvements in performance or complete failure of
bioaugmentation; no instances of long-term improvement have
been reported. This may be because indigenous microorganisms
tend to outcompete extraneous microorganisms. Therefore, future
studies focused on determining interactions between microbes,
clarifying metabolic networks, and creating a competitive advan-
tage for target microorganisms are necessary. Alternatively, in-
situ selection or targeting of microorganisms under controlled con-
ditions may be a more direct and convenient method for improving
AD efficiency. By changing the feeding rate or shear frequency, pre-
vious studies have selected the more tolerant Methanosarcina (over
Methanosaeta), to improve process stability (Conklin et al., 2006;
Hoffmann et al., 2008). However, systematic studies in this area
are rare. Comparisons and selection of microorganisms currently
are restricted to Methanosarcina and Methanosaeta, but the effi-
ciency of different hydrogenotrophic methanogens is also varied.
For example, the hydrogen consumption efficiency of Methanobac-
terium is higher than that of Methanospirillum and Methanoculleus
(Shigematsu et al., 2006a,b). Theoretically, high VFA concentra-
tions in digesters will lead to high hydrogen pressure. Breeding
Methanobacterium under these conditions may help reduce hydro-
gen pressure and avoid VFA accumulation. However, no relevant
studies have been reported. Further studies on the growth kinetics,
ecology, and competition are necessary to provide guidance for
controlling operating conditions, selecting target microorganisms,
and achieving stable operation.
5. Research outlook
Anaerobic digestion is a biochemical process driven by microor-
ganisms, and process instability results from disruptions to micro-
bial metabolism. Microbial management can improve early
diagnosis and process optimization, but it is limited by the follow-
ing technical issues: 1) elusive instability mechanisms; 2) variable
microbial indicators; and 3) transient intensification effects. Study-
ing the organization and behavior of microorganisms on multiple
scales in addition to monitoring physicochemical parameters can
help elucidate the microbiological mechanisms of process instabil-
ity. The origins of instability are closely related to microbial early
warning indicators. Reproducible experiments and statistical cor-
relations between biomarkers and process performance are neces-
sary to ensure the reliability of established microbial indicators.
Clarifying the roles of niche-based theory and neutral theory in
driving community succession is crucial for identifying universal
biomarkers. Selection and proliferation of target microorganisms
is the basis for long-term biotechnological intensification. Future
research should focus on microbial growth kinetics, ecology, and
competition to help control operating conditions and create a com-
petitive advantage for target microorganisms. In addition, on-line
detection of microbial indicators (e.g., via biosensors) can be used
to complement routine process monitoring and control.
6. Conclusions
Performance instability is a key operational issue for AD of FW.
Process monitoring and control as well as microbial management
are major research directives for improving AD stability and effi-
ciency. The lack of overall and dynamic research has limited the
success of routine process monitoring and microbial analysis for
process optimization. Combining multi-scale microbial manage-
ment with real-time monitoring of various physicochemical and
biochemical parameters is necessary to achieve efficient and stable
process operation.
Acknowledgements
This work was financially supported by the Fundamental
Research Funds for the Central Universities (No.
106112017CDJXY210006).
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