Journal of Environmental Management 302 (2022) 114088

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Journal of Environmental Management

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Influence of microbial inoculants on co-composting of lignocellulosic crop

residues with farm animal manure: A review
Babett Greff *, Jenő Szigeti, Ágnes Nagy, Erika Lakatos, László Varga
Department of Food Science, Faculty of Agricultural and Food Sciences, Széchenyi István University, 15-17 Lucsony Street, 9200, Mosonmagyaróvár, Hungary

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

Keywords: The rapidly developing agro-industry generates huge amounts of lignocellulosic crop residues and animal
Composting manure worldwide. Although co-composting represents a promising and cost-effective method to treat various
Crop residue agricultural wastes simultaneously, poor composting efficiency prolongs total completion time and deteriorates
Manure
the quality of the final product. However, supplementation of the feedstock with beneficial microorganisms can
Microbial inoculation
Inoculant
mitigate these negative effects by facilitating the decomposition of recalcitrant materials, enhancing microbial
enzyme activity, and promoting maturation and humus formation during the composting process. Nevertheless,
the influence of microbial inoculation may vary greatly depending on certain factors, such as start-up parame­
ters, structure of the feedstock, time of inoculation, and composition of the microbial cultures used. The purpose
of this contribution is to review recent developments in co-composting procedures involving different ligno­
cellulosic crop residues and farm animal manure combined with microbial inoculation strategies. To evaluate the
effectiveness of microbial additives, the results reported in a large number of peer-reviewed articles were
compared in terms of composting process parameters (i.e., temperature, microbial activity, total organic carbon
and nitrogen contents, decomposition rate of lignocellulose fractions, etc.) and compost characteristics (humi­
fication, C/N ratio, macronutrient content, and germination index). Most studies confirmed that the use of mi­
crobial amendments in the co-composting process is an efficient way to facilitate biodegradation and improve the
sustainable management of agricultural wastes. Overall, this review paper provides insights into various inoc­
ulation techniques, identifies the limitations and current challenges of co-composting, especially with microbial
inoculation, and recommends areas for further research in this field.

1. Introduction 2020b; Prasad et al., 2020).

In addition to global population growth, improving living conditions
and increasing food production have also been placing pressure on
agriculture for years (Davis et al., 2017; Turmel et al., 2015; Wu et al.,
2020). In contrast to traditional agriculture, modern agro-industrial
activities including large-scale livestock farming and intensified crop
production result in huge amounts of unutilized solid and liquid wastes
(Jia et al., 2018; Jimenez-Lopez et al., 2020; Ravindran et al., 2021;
Sánchez, 2009). Globally, 125 million tonnes of nitrogen from livestock
manure and 140 billion tonnes of lignocellulosic wastes are generated
every year (FAO, 2020; Patil et al., 2020), which is 30–40% of the total
solid waste production (Wu et al., 2020). Therefore, the disposal and
valorization of these agricultural by-products are a worldwide challenge
(Assandri et al., 2021), and only 30–75% of the total manure and agri­
cultural crop residues are recycled in certain countries (Guo et al.,
Despite its renewable nature (Anwar et al., 2014), lignocellulosic
biomass is usually buried (Zhou et al., 2020), destroyed by incineration,
or treated in landfills, causing serious environmental pollution and
health problems (Qdais and Al-Widyan, 2016). For instance, burning of
crop residues is still a major contributor to air pollution in developing
countries, leading to the emission of various pollutants such as partic­
ulate matter, greenhouse gases, polycyclic aromatic hydrocarbons, and
volatile organic compounds (Ravindra et al., 2019). On the other hand,
unprocessed livestock manure is a widely used direct organic fertilizer
(Hu et al., 2019; Petric et al., 2009), but its over-application leads to the
accumulation of heavy metals (Liu et al., 2020b), emission of particulate
matter and greenhouse gases, and distribution of potential pathogenic
microorganisms, antibiotic residues, antibiotic-resistant bacteria, and
antibiotic resistance genes (ARGs) in the environment (Gou et al., 2018;
Kabelitz et al., 2021; Li et al., 2020; Lima et al., 2020; Yan et al., 2018).

* Corresponding author.
E-mail address: greff.babett@sze.hu (B. Greff).

https://doi.org/10.1016/j.jenvman.2021.114088
Received 25 June 2021; Received in revised form 27 September 2021; Accepted 8 November 2021
Available online 16 November 2021
0301-4797/© 2021 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
B. Greff et al.
Therefore, manure disposal, storage, and handling also represent a sig­
nificant problem for the industry (Petric et al., 2009).
Since valorization of these by-products is an important step in agri­
cultural development and environmental protection (Wang et al., 2016),
some eco-friendly alternatives have been proposed to meet the objec­
tives of sustainability and circularity (Bruni et al., 2020; Sorathiya et al.,
2014). Both crop residues and raw manure are an excellent source of
plant nutrients and organic matter (OM); however, direct application
can lead to increased levels of greenhouse gas and foul odor emissions,
accumulation of heavy metals and antibiotics, contamination of soil and
groundwater, or spread of pathogens, weed seeds, ARGs, and toxic
substances (Ahmad et al., 2007; Chen et al., 2019b; Guo et al., 2015;
Macias-Corral et al., 2019; Vargas-García et al., 2007b; Zubair et al.,
2020). Co-composting is an applicable method to overcome these dis­
advantages and utilize both wastes simultaneously (Qdais and
Al-Widyan, 2016; Qian et al., 2014), because crop residues and livestock
manure complement each other by providing the missing components
(e.g., organic matter, moisture, nitrogen, etc.) (Cofie et al., 2009;
Guerra-Rodríguez et al., 2001), resulting in a stable organic fertilizer
rich in humic substances (Majbar et al., 2018). However, co-composting
is not that simple because process optimization highly depends on a
variety of physical, chemical (Silva et al., 2009), and microbiological
(Franke-Whittle et al., 2014) factors.
Although several microorganisms occurring in the feedstock are
responsible for the degradation of compost materials (Dastpak et al.,
2020; Holman et al., 2016), inadequate quantity or poor biodegradation
capacity of autochthonous microbes may result in reduced composting
efficiency and undesirable compost quality (Xi et al., 2015; Xu et al.,
2019b). Therefore, the strategy of using specialized microbial cultures is
a promising approach to facilitate compost maturity and enhance final
compost quality (Gou et al., 2017; Liu et al., 2011). However, a lack of
understanding of the role of bioaugmentation in the composting process
is still a major obstacle (Heidarzadeh et al., 2019) and, thus, it cannot be
taken for granted that exogenous microorganisms always promote the
composting process (Awasthi et al., 2018).
There is a multitude of scientific articles available on agricultural
waste valorization through aerobic composting. However, to our
knowledge, no previous paper has reviewed the effect of various mi­
crobial inoculation strategies on co-composting procedures involving
different lignocellulosic crop residues and farm animal manure com­
bined. Thus, the primary purpose of our study is to summarize and
evaluate current scientific literature on this topic to help improve the
bioconversion rate of these major agricultural waste materials. The in­
fluence of single strain inocula, mixed cultures, and various inoculation
techniques on the co-composting process and final compost quality are
also discussed to provide a better understanding of the impacts of mi­
crobial amendments on physical, chemical, and microbiological pa­
rameters of composts. In addition, the present work aims to identify the
challenges facing bioaugmented co-composting methods (i.e., lack of
industrial-scale trials, gaseous emissions, and emerging contaminants)
and offer further solutions for safe and efficient waste valorization.
2. Efficient valorization of lignocellulosic crop residues with
farm animal manure
The valorization of agricultural wastes as profitable products is a key
factor for sustainability and, therefore, the search for economically
viable, fast, and sustainable alternatives is still a great and ongoing
challenge (Harindintwali et al., 2020; Jia et al., 2018; Jimenez-Lopez
et al., 2020).
Composting is not a new technology (Bernal et al., 2009), but it is one
of the most effective methods for reusing organic wastes as
eco-compatible amendments, improving the fertility of soil, supplying
nutrients, and promoting plant growth (Alfano et al., 2008; Liu et al.,
2020a). Composting itself is a controlled, aerobic process involving a
variety of microorganisms that decompose and transform different
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Journal of Environmental Management 302 (2022) 114088
biodegradable organic compounds into an organic fertilizer (Atif et al.,
2020; Du et al., 2020; Grgić et al., 2019; Kaur et al., 2019; Mohamma­
dipour et al., 2021), thereby closing the nutrient loop (Cofie et al.,
2009). As long as the process is properly managed, the mature and stable
end product is free of phytotoxic substances and the vast majority of
potential pathogenic microorganisms are killed (Kaur et al., 2019). To
comply with recommended requirements, promote maturation, and
produce a high-quality agricultural product (Jalili et al., 2019; Wong
et al., 2001), certain parameters of the feedstock material [e.g., tem­
perature, humidity, carbon-to-nitrogen (C/N) ratio, pH value, aeration,
particle size, nutrients, etc.] need to be optimized and adequately
controlled (Table A1). If these conditions are not met, the treated agri­
cultural waste may not be suitable for land application.
In terms of physical and chemical characteristics, certain wastes may
not be suitable for composting as sole feedstock materials (Kumar et al.,
2010; Tabrika et al., 2021). For instance, the conventional composting
of lignocellulose-rich residues is a time-consuming process due to the
high C/N ratio (Jurado et al., 2014b; Paradelo et al., 2013) because high
levels of lignocellulosic fractions can slow down the biodegradation and
biotransformation of the biomass (Bohacz, 2019a), thereby limiting
humus formation as well (Liu et al., 2017). Even though the decompo­
sition of cellulose and hemicellulose is an easier procedure (Gar­
cía-Gómez et al., 2005), lignin–carbohydrate complexes, acting as a
protective factor, enwrap cellulose in plant cell walls and slow down
microbial decomposition (Feng et al., 2011; Huang et al., 2017; Sarika
et al., 2014). Thus, the breakdown of recalcitrant polymeric compounds,
such as lignin (10–25% of lignocellulosic biomass), is a crucial step for
the stabilization of OM (López-González et al., 2015; Su et al., 2020;
Vargas-García et al., 2007b). Without proper decomposition, compost
stability is not ensured, and the application of immature compost leads
to the immobilization of nutrients, inhibition of plant growth, and in­
duction of anaerobic conditions in the soil (Grgić et al., 2019; Ilani et al.,
2016; Vargas-García et al., 2007a).
Co-composting is a globally recognized, efficient method to simul­
taneously treat at least two organic wastes, minimizing the drawbacks of
traditional composting methods (Hwang et al., 2020). To avoid nitrogen
deficit, lignocellulosic by-products can be supplemented with
co-substrates with different characteristics (Guerra-Rodríguez et al.,
2006), such as livestock manure featuring elevated moisture content,
easily degradable organic matter content, and reduced C/N ratios (Bai
et al., 2020; Wu et al., 2019). The study of Guerra-Rodríguez et al.
(2000) showed that barley waste was not suitable for composting due to
an increased C/N ratio (43.72). However, solid poultry manure sup­
plementation decreased the initial C/N ratio of the composting mixture
to 16.19 and the outcome of the 103-day-long co-composting process
was a mature product with a germination percentage of 186 for ryegrass
seeds. Meng et al. (2018) observed that pig manure addition prolonged
the thermophilic phase by 15 days, improved the germination index
from 80 to 87%, and expedited the maturity of spent mushroom sub­
strate and rice husk compost. Karanja et al. (2019) composted rice straw
both with and without animal manure. At the end of the experiments,
the control rice straw compost had the highest C/N ratio (23.75),
whereas the composts supplemented with chicken and donkey manure
(10.84 and 11.32, respectively) were within the recommended range of
10–18. Likewise, Gaind (2014) showed that the addition of cattle or
farmyard manure to paddy straw can improve the agronomic quality of
the finished composts by increasing the total Kjeldahl nitrogen content
(TKN: 1.09–1.25), GI, and microbial biomass carbon, while the final C/N
ratio was reduced to 22.42–23.23. Although El-Haddad et al. (2014)
failed to produce rice straw composts with the required level of matu­
rity, cattle manure supplementation considerably improved the final
C/N ratio, bulk density, and total nitrogen and phosphorus contents.
Sharma et al. (2014) also confirmed that supplementation with poultry
droppings can reduce both the initial and final C/N ratios, thus
increasing the rate of humus formation. Therefore, co-composting
lignocellulosic crop residues with co-substrates that have decreased
B. Greff et al. Journal of Environmental Management 302 (2022) 114088

Table 1
Summary of studies on co-composting of agricultural crop residues with farm animal manure using microbial inoculation.
Feedstock (ratio) Sizea(kg) Method Microbial inoculant Rate of microbial Time of inoculation Duration Reference
inoculant (days)

Fungal inoculant
Rice straw and cattle – Pile Trichoderma harzianum, 5.0 l/ton of rice Initial stage 112 El-Haddad et al.
manure (1:2) Phanerochaete chrysosporium (1:1) straw (2014)
Wheat straw and 60 Pit (Pile) Aspergillus awamori, Aspergillus 180 g of seed-based Initial stage 60 Gaind et al.
poultry manure nidulans, Trichoderma viride, inoculum/pit (2009)
(6.5:1) Phanerochaete chrysosporium
+ Udaipur rock (1:1:1:1)
phosphate
Rice straw and cattle – Bin Aspergillus niger, – Cooling/maturation stage 120 Gaind (2014)
manure/farmyard Aspergillus flavus, Trichoderma
manure/poultry harzianum
manure
Rice straw and dairy 23.8 Reactor Aspergillus niger, 1.0% Initial stage 54 Gou et al. (2017)
manure (1:5.26) Penicillium commune (1:1)
Rice straw and 4 Composter Ligninolytic inoculum: Aspergillus 3.0–3.0% Two-stage inoculation with 42 Kausar et al.
poultry manure niger different inocula (ligninolytic (2013)
(1:1) Cellulolytic inoculum: inoculum: initial stage;
Trichoderma viride cellulolytic inoculum: after
the thermophilic stage)
Rice straw and – Pit (Pile) Aspergillus awamori, 10 g/kg Initial stage 60 Pandey et al.
poultry manure Aspergillus nidulans, (2009)
(89% and 11%) Trichoderma viride,
+ Udaipur rock Phanerochaete chrysosporium
phosphate
Untreated rice 20 Bin MI “compound Trichoderma 40 g Initial stage 38 Wu et al. (2019)
straw/corn straw agent”: Trichoderma viride
and swine manure (~50%), Trichoderma harzianum
(1:4) (~45%)
Bacterial inoculant
Rice straw and cattle 368 Pile Bacillus licheniformis, 1.0% Multi-stage inoculation (days 117 Abdel-Rahman
manure (1:3.6) Bacillus sonorensis (separately or in 1, 11, and 23) et al. (2016)
mixture of 1:1)
Wheat straw and – Reactor Synthetic bacteria consortium – Initial stage 42 Awasthi et al.
cattle manure (1:5 (2020)
on dry weight
basis)
Wheat straw and 9 Reactor Bacillus subtilis 0.5, 1.0, 2.0% (on Initial stage 26 Duan et al.
cattle manure (1:2) dry weight basis) (2020)
Rice straw and dairy 23.8 Reactor Brevundimonas diminuta, 1.0% Initial stage 54 Gou et al. (2017)
manure (1:5.26) Flavobacterium glaciei (1:1)
Poultry manure and 16 Reactor Bacillus megaterium 5.0% (on dry Initial stage 44 Guo et al.
wheat straw weight basis) (2020a)
Swine manure and 23 Reactor Ammonifiers, nitrobacteria, 3.0% Initial stage 45 Jiang et al.
wheat straw Azotobacter (1:1:1) (2015)
(10.5:1)
Swine manure and 23 Reactor Ammonifiers, nitrobacteria, 1.0% Initial stage or after the 45 Jiang et al.
wheat straw Azotobacter (1:1:1) thermophilic stage (2015)
(10.5:1)
Swine manure and – Pile Acinetobacter pittii, 1.0% Initial stage 35 Li et al. (2019)
corn straw (6:1) Bacillus subtilis subsp. stercoris,
Bacillus altitudinis
Cattle manure and – Pile Cellulose-degrading bacteria 0.1% Initial stage 31 Liu et al. (2011)
straw (dominant species: Bacillus sp. and
Pseudomonas sp.)
Poultry manure and 100 Bin Bacillus flexus, 0.05 l/kg Initial stage 31 Selvamani et al.
rice husk (3:1) Bacillus subtilis, (2019)
Bacillus cereus
Untreated rice 20 Bin MI “straw decomposing agent”: 10 g Initial stage 38 Wu et al. (2019)
straw/corn straw Bacillus subtilis (~45%), Bacillus
and swine manure casei (~40%), Actinomyces bovis
(1:4) (~10%)
Cattle manure and 25 Pile Ureibacillus suwonensis, 1.0–1.0 l Two-stage inoculation (days 45 Xu et al. (2019b)
sugarcane leaves Geobacillus thermodenitrificans, 0 and 10)
(4:1) Bacillus licheniformis (1:1:1)
Dairy manure and ~8 Reactor Cellulose-degrading Streptomyces 2.0% (on dry Different inoculation times 60 Zhao et al.
corn straw (2:1) sp. and Actinobacteria bacterium weight basis) (days 0, 6, 15, or all three (2017)
(1:1:1:1) times)
Poultry manure and ~8 Reactor Cellulose-degrading Streptomyces 2.5% (on dry Different inoculation times 36 Zhao et al.
corn straw (1:2) sp., weight basis) (days 0, 7, 16) (2016)
Micromonospora sp.
Mixed complex consortium
Wheat straw and – Reactor Bacterial consortium – Initial stage 50 Duan et al.
cattle manure (2019a)
(continued on next page)

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B. Greff et al. Journal of Environmental Management 302 (2022) 114088

Table 1 (continued )
Feedstock (ratio) Sizea(kg) Method Microbial inoculant Rate of microbial Time of inoculation Duration Reference
inoculant (days)

Swine manure and ~2.4–2.8 Reactor Complex biological agent 11.9–13.8 g Initial stage 84 Gao et al. (2015)
rice husk/corn
straw (1:1, 1.5:1,
2:1 on dry weight
basis)
Rice straw and cattle 23.8 Reactor Brevundimonas diminuta, 1.0% Initial stage 54 Gou et al. (2017)
manure (1:5.26) Flavobacterium glaciei,
Aspergillus niger,
Penicillium commune (1:1:1:1)
Poultry manure and – Pile Microbial suspension inoculants 0.3% Initial stage 53 Li et al. (2017)
corn straw sourced from aerobic municipal
sludge or municipal solid waste
Corn straw and – Bin “Bio-soils compost+” commercial – Initial stage 168 Luyima et al.
poultry manure inoculant (2019)
Poultry manure and 220 Reactor 25 microorganisms isolated from 200 ml/ Initial stage 60 Wan et al. (2020)
corn straw (10:1) compost (Bacillus sp., Paracoccus microorganism
sp., Ureibacillus sp., Geobacillus (6400 ml in total)
sp.) and Bacillus thuringiensis,
Bacillus licheniformis,
Bacillus subtilis,
Paenibacillus humicus,
Aspergillus fumigatus Fresenius,
Trichoderma longibrachiatum,
Trichoderma sp.
Swine manure and – Pile Bacillus subtilis, 1:1000 Initial stage 20 Xu and Li (2017)
corn straw (10:3) Bacillus licheniformis,
Phanerochaete chrysosporium,
Trichoderma koningii,
Saccharomyces cerevisiae
Cattle manure and 25 Reactor Bacillus licheniformis, 2.0% (on dry Two-stage inoculation (days 45 Xu et al. (2019a)
sugarcane leaves Aspergillus nidulans, weight basis) 0 and 9)
(4:1) Aspergillus oryzae (1:1:1)
Dairy manure and 36.4 Reactor Inoculum A: – Multi-stage inoculation with 45 Zhou et al.
rice straw (29.3:1) Thermoactinomyces sp. GF1, different inocula (Inoculum A: (2015)
Thermoactinomyces sp. GF2 (1:1) day 0; Inoculum B: after the
Inoculum B: thermophilic phase; Inoculum
Coprinus cinerea, C: after 30 days)
Coprinus comatus (1:1)
Inoculum C:
Trichoderma harzianum,
Rhizopus oryzae (1:1)
a
Size only includes straw and manure.

C/N ratios is a recommended strategy to induce biodegradation and
produce a mature and stabilized compost.
3. Microbial inoculants
Microorganisms are important contributors to the composting pro­
cess (Holman et al., 2016; Tu et al., 2019; Yu et al., 2007). They are
responsible for heat generation, transformation of plant nutrients, and
depolymerization of larger compounds by producing extracellular hy­
drolytic enzymes (Bernardi et al., 2018; Holman et al., 2016; Kutu et al.,
2019). During co-composting, indigenous microbes naturally break
down most organic polymers; however, it can result in an extended
completion time and reduced composting efficiency if the natural
microbiota is not sufficiently diverse or is adversely affected by certain
environmental parameters and/or feedstock characteristics, including
the presence of various secondary metabolites (Alkoaik and Ghaly,
2005; Greff et al., 2021b; Jurado et al., 2015; López et al., 2002; Tran
et al., 2015). In such a situation, inoculation with beneficial microor­
ganisms is a useful strategy that can potentially promote the composting
process by reducing the initial lag phase, generating various enzymes,
accelerating the decomposition of organic wastes, promoting the degree
of humification, enhancing the properties of the mature product, and
eventually reducing production costs (Chi et al., 2020; Fang et al., 2019;
Gou et al., 2017; Li et al., 2008).
The use of preselected microbes to improve the composting process
has been a controversial issue for a long time (Zeng et al., 2009). While
some researchers reported the absence of additional effects (Karncha­
nawong and Nissaikla, 2014; Nair and Okamitsu, 2010), others
demonstrated that inoculation could positively influence the duration of
composting, the process of maturation, and final compost quality
(Gaind, 2014; Kausar et al., 2014; Zhao et al., 2017). Nevertheless, such
controversy should not be surprising because the effectiveness of mi­
crobial cultures highly depends on certain factors, such as the type and
viable counts of the microbes used, the time of inoculation, the
competition between exogenous and autochthonous microorganisms,
the specific operating conditions of composting, and the major charac­
teristics of raw materials (Fan et al., 2018a,b; Fang et al., 2019; Wang
et al., 2019; Zhou et al., 2015).
Since the composting process requires a series of enzymes secreted
by various microbes (Tiquia et al., 2002), complex consortia tend to be
more effective compared to single strain or single function inocula,
because these latter inoculants may not meet multiple requirements or
they might be killed by the indigenous microbiota while competing for
nutrients (Song et al., 2016; Yu et al., 2018). Abdel-Rahman et al. (2016)
used pure and mixed cultures of cellulolytic bacteria to accelerate the
composting of a mixture containing rice straw and cow manure.
Compared to pure cultures, mixed consortia exhibited an extended
thermophilic phase and accelerated maturation (C/N ratio of ≤20), but
Duan et al. (2020) showed that the efficiency of pure cultures highly
depends on concentration. A treatment involving inoculation with 2% of
Bacillus subtilis resulted in an accelerated reduction in C/N ratio,
whereas 0.5% of Bacillus subtilis had no effect on this parameter.

4
B. Greff et al.
However, the addition of 0.5% of Bacillus subtilis promoted the trans­
formation of humic substance precursors into humic substances during
the middle and late stages of composting. In particular circumstances,
inoculants containing two or more types of microorganisms might also
not have the desired effect on the composting process. Karnchanawong
and Nissaikla (2014) used commercial microbial inoculants (EM and
LDD1) to facilitate the degradation of food preparation scraps mixed
with dry leaves. Although these products consisted of different mi­
crobes, their use was deemed unnecessary. Milanović et al. (2019) re­
ported that Azotobacter chroococcum strains and Phanerochaete
chrysosporium had a modest influence on the microbiological, physical,
and chemical parameters of mature wet olive pomace–wheat straw
compost. Nair and Okamitsu (2010) treated various waste materials (i.
e., kitchen waste, matured compost, sawdust, paper/cardboard, and
grass clippings) with EM. The results revealed that inoculation with
lignocellulolytic bacteria had a slight effect on the final compost. Similar
results were reported by Fan et al. (2018b). These studies have
confirmed that the applicability of cultures depends on both the
composition of microbial amendments and the initial feedstock
material.
The best candidates are usually the microbes naturally occurring in
the composting system (Xu et al., 2019a). They can balance the native
microbiota and hasten the co-composting process by promoting the
growth of desired microorganisms (Selvamani et al., 2019). Wan et al.
(2020) combined 25 different cellulosic isolates from chicken manure
and maize straw compost with seven purchased strains. The complex
inoculum positively influenced the thermophilic phase, elevated the
temperature, and provided a mature product with increased GI (96% as
opposed to 62%). Likewise, Li et al. (2017) reported that a microbial
suspension sourced from municipal sludge could accelerate the
biodegradation of chicken manure–corn stalk compost by providing
enhanced cellulase, urease, and catalase activities. Duan et al. (2019a)
added an indigenous bacterial consortium to a mixture of cattle manure
and wheat straw to improve the composting process by achieving
elevated temperature and pH.
Another key factor that largely affects composting is the time of
inoculation (Jiang et al., 2015; Zhao et al., 2016). According to Ryck­
eboer et al. (2003), composting can typically be divided into four major
phases by temperature as follows: an initial mesophilic phase, a ther­
mophilic phase, a second mesophilic phase, and the maturation and
stabilization phase. Each phase is characterized by the growth and ac­
tivity of various microbial populations with which the inoculated mi­
croorganisms must compete (Zhou et al., 2015). As a result of
improperly chosen inoculation time, the added microorganisms may not
have the desired performance (Xi et al., 2005).
Microbial cultures are usually applied at the onset of composting to
initiate biodegradation (Jusoh et al., 2013; Li et al., 2018; Qu et al.,
2019). However, some researchers suggested that other inoculation
strategies should also be considered. Zhao et al. (2016) found that
inoculation during the cooling stage of composting could avoid the
damaging effect of high temperatures on inoculants. Bernal-Vicente
et al. (2012) observed that inoculation with the biological control agent
(BCA) Trichoderma harzianum was ideally done at the maturation phase
because this compost suppressed Fusarium wilt more efficiently
compared to composts inoculated with the same BCA at the start of the
composting process. Taccari et al. (2009) applied Phanerochaete chrys­
osporium immediately before the curing phase of olive mill waste­
water–agricultural waste compost. The white-rot fungi promoted the
co-composting process by reducing the phytotoxic effects of the
remaining phenols and improving the final GI. Gaind (2014) reported
that an exogenous fungal consortium consisting of Aspergillus niger,
Aspergillus flavus, and Trichoderma harzianum, used at the cool­
ing/maturation phase, lowered both the C/N and E4/E6 ratios (18.3 and
5.38, respectively) of paddy straw–poultry manure compost. Kausar
et al. (2013) added a ligninolytic inoculant (Aspergillus niger) to the
feedstock material at the initial stage of co-composting and, following
5
Journal of Environmental Management 302 (2022) 114088
the thermophilic stage, the compost mixture was re-inoculated with
cellulolytic fungi (Trichoderma viride). This two-stage inoculation tech­
nique enhanced the biodegradation of certain recalcitrant substrates (i.
e., lignin and cellulose) and shortened the composting period.
All these results highlight the importance of analyzing the relation­
ship between the microbial cultures added to feedstock materials and
the time of inoculation. As shown in Table 1, numerous microbial
amendments combined with various composting strategies and inocu­
lation techniques have been proposed for the production of lignocellu­
losic waste–manure composts.
Several microorganisms have been used either in consortia or as
single strain inoculants to speed up the co-composting process of
lignocellulosic waste and manure, and there are some microbes that
have been applied on multiple occasions. Trichoderma spp. are
nonpathogenic soil-borne fungi (Coelho et al., 2021) that are often used
as beneficial microorganisms (Mbarki et al., 2017) because they
compete for space and nutrients, utilize diverse substrates, inhibit a wide
variety of phytopathogens, are resistant to various soil fungicides and
harsh environmental conditions, and even stimulate plant growth
(Abdel-Kader et al., 2013; Bernal-Vicente et al., 2014; Chakroun et al.,
2010; Joos et al., 2020; Mbarki et al., 2017; Siddiquee et al., 2017).
Previous studies demonstrated that certain Trichoderma strains as
compost activators (Parkash and Saikia, 2015) can promote the miner­
alization of organic matter (Mbarki et al., 2017) by producing cellulo­
lytic (Gautam et al., 2012), ligninolytic, xylanolytic (Bohacz and
Korniłłowicz-Kowalska, 2020), and proteolytic enzymes (Coelho et al.,
2021). During the composting of empty fruit bunches, Siddiquee et al.
(2017) achieved greatly reduced maturation time when Trichoderma
strains were added to the feedstock. This is in agreement with the results
of Haddadin et al. (2009), who used the mixed culture of Trichoderma
harzianum and Phanerochaete chrysosporium to facilitate the composting
of olive pomace. For co-composting of crop residues with manure,
various Trichoderma species (e.g., Trichoderma harzianum, Trichoderma
longibrachiatum, Trichoderma koningii, and Trichoderma viride) have been
applied as microbial inoculants (El-Haddad et al., 2014; Gaind, 2014;
Gaind et al., 2009; Kausar et al., 2013, 2014; Pandey et al., 2009; Wan
et al., 2020; Wu et al., 2019; Xu and Li, 2017; Zhou et al., 2015).
Similarly, aspergilli are important micromycetes that produce
cellulase, hemicellulase, amylase (Grujić et al., 2015), and secondary
metabolites inhibiting the growth of fungal pathogens (Abdallah et al.,
2015). Some of them such as Aspergillus fumigatus (Jurado et al., 2014a;
Langarica-Fuentes et al., 2014; Tian et al., 2017), Aspergillus flavus (van
Heerden et al., 2002), and Aspergillus niger (Zhang et al., 2016; Zhou
et al., 2016) have previously been isolated from composts and used as
microbial inoculants during co-composting (Gaind, 2014; Gou et al.,
2017; Kausar et al., 2013, 2014; Wan et al., 2020).
Phanerochaete chrysosporium is one of the most widely used basid­
iomycetes capable of efficiently degrading lignocellulosic materials and
a broad range of organopollutants (Taccari et al., 2009). In contrast to
other white rot-fungi, this species produces nonspecific extracellular
enzymes including lignin peroxidase, manganese peroxidase, and lac­
case (Haddadin et al., 2009; Varma et al., 2015). During composting, the
application of Phanerochaete chrysosporium can shorten the cycle of
composting, enhance bacterial community abundance, accelerate the
decomposition of lignin and cellulose, increase macronutrient content,
promote humification, and improve final compost quality (Chen et al.,
2019c; Gong et al., 2017; Zhang et al., 2013). El-Haddad et al. (2014),
Gaind et al. (2009), Pandey et al. (2009), and Xu and Li (2017) also
proved its effectiveness in microbial amendments during co-composting
experiments.
Although fungi are the main cellulase producing microorganisms,
bacteria and actinomycetes play a specific role in the biodegradation of
waste materials (Eida et al., 2012). Bacilli are commonly used species
due to their resilience against a wide spectrum of abiotic and biotic
environmental stressors (Angelina et al., 2020). Former studies
confirmed that Bacillus is the most dominant genus recovered from
B. Greff et al.
feedstock materials, and bacilli are also predominant bacteria
throughout the entire composting process, likely due to their ability to
form endospores under thermophilic conditions (Chandna et al., 2013;
Li et al., 2018; Tuomela et al., 2000). Certain species (e.g., Bacillus
licheniformis, Bacillus subtilis, Bacillus megaterium, Bacillus flexus, Bacillus
cereus, etc.) have been used as bacterial inoculants during
co-composting (Duan et al., 2020; Guo et al., 2020a; Selvamani et al.,
2019; Xu et al., 2019b) due to their role in the biodegradation of organic
matters, including cellulose, starch, lipids, and proteins by producing
specific enzymes (Zhou et al., 2021). Moreover, these bacteria take part
in both nitrogen fixation and solubilization of phosphorus (Li et al.,
2018) and certain strains are also potent microbial biopesticides (Bal­
lardo et al., 2020).
Although many bacteria can solubilize and modify the structure of
lignin, their lignin mineralization potential is mostly limited. In addition
to their cellulose degradation activity, filamentous actinomycetes are
also capable of solubilizing lignin (Tuomela et al., 2000). These
spore-forming microorganisms, including Micromonospora, Strepto­
myces, Frankia, and Thermoactinomyces spp., are typically found in ma­
terials rich in lignocellulose, and have an essential role in degradation,
mineralization, nitrogen fixation, and solubilization of phosphorus
(Javed et al., 2021; Zhao et al., 2016). Such beneficial effects have been
demonstrated by several studies that used microbial consortia contain­
ing actinomycetes strains (Jurado et al., 2015; Wu et al., 2019; Zhao
et al., 2016, 2017; Zhou et al., 2015).
Microbial inoculants containing nitrogen-fixing bacteria, in addition
to bacilli and actinomycetes strains, can promote the composting pro­
cess by decreasing nitrogen losses, removing phytotoxic compounds,
and producing exopolysaccharides (Jiang et al., 2015; Milanović et al.,
2019). Nitrogen-fixing organisms are all prokaryotes, which include
actinomycetes and microaerobic, aerobic, anaerobic, and photosyn­
thetic bacteria (Rodrigues et al., 2018). The genus Azotobacter is
comprised of important species (Biabani et al., 2020) that can fix at­
mospheric nitrogen, produce siderophores for chelating iron, synthesize
plant growth regulating substances and phytohormones, promote solu­
bilization of minerals, and provide protection to plants against phyto­
pathogens (Ewusi-Mensah et al., 2020; Rodrigues et al., 2018). These
diazotrophs may naturally occur in composting materials, but their
utilization as a microbial inoculant is also common due to their positive
influence on final compost quality (Biabani et al., 2020; Cayuela et al.,
2009; Meunchang et al., 2005; Singh and Sharma, 2003).
4. Effects of microbial inoculants on the co-composting process
and final compost quality
Both the co-composting process and the quality of the mature
compost can be directly influenced by microbial inoculants, which
induce changes in physicochemical, microbiological, and biological
parameters. Inoculation with beneficial microorganisms positively af­
fects the degradation process, resulting in variations in temperature,
microbial activity and enzyme production, total organic carbon and
total nitrogen contents, carbon and nitrogen losses, C/N ratio, decom­
position of lignocellulose fractions, and humification.
4.1. Effects of microbial inoculants on the co-composting process
4.1.1. Temperature
The temperature pattern of compost is an important maturity indi­
cator (Gao et al., 2015), because changes in the temperature profile of
the composting material reflect both the progress of the composting
process and the rate of microbial activity (Greff et al., 2021b; Li et al.,
2018). Thermophilic conditions largely contribute to the degradation of
phytotoxic compounds and polymers, in addition to controlling
heat-sensitive pathogenic microorganisms (Selvamani et al., 2019;
Zhong et al., 2018). Previous co-composting studies have demonstrated
that microbial inoculation can stimulate microbial activity in the early
6
Journal of Environmental Management 302 (2022) 114088
phase of composting, leading to a sharp increase in temperature
(Abdel-Rahman et al., 2016; Duan et al., 2020; Kausar et al., 2014; Xu
and Li, 2017). Moreover, Wu et al. (2019) observed that commercial
microbial inoculants mitigated the temperature fluctuations and pro­
longed the thermophilic period by 1–6 days. Similar findings were re­
ported by other authors (Duan et al., 2020; Guo et al., 2020a; Jiang
et al., 2015; Li et al., 2019). Likewise, a complex mixture of microor­
ganisms was shown to elongate the thermophilic phase of chicken
manure–maize straw compost (Wan et al., 2020). Xu et al. (2019b)
composted dairy manure and sugarcane leaves together with Ureibacillus
suwonensis, Geobacillus thermodenitrificans, and Bacillus licheniformis
isolated previously from the thermophilic phase of another compost.
Overall, the high temperature phase was extended by 2 days in the
inoculated compost. For co-composting rice straw with dairy manure,
Gou et al. (2017) used a microbial culture containing Aspergillus niger
and Penicillium commune. These thermophilic fungi improved the
self-heating properties of the compost and increased the composting
temperature (63 ◦ C) compared to the control treatment (55 ◦ C).
All things considered, several microbial cultures are capable of
promoting the maintenance of thermophilic conditions due to an
increased microbial metabolism, thereby enhancing OM decomposition,
especially at the early stages of composting (Gou et al., 2017; Abdel-­
Rahman et al., 2016). The higher temperature profiles achieved with
microbial amendments may contribute to the inactivation of pathogens
and the removal of heavy metals, ARGs, and phytotoxic compounds (Cui
et al., 2020; Jiang et al., 2021).
4.1.2. Microbial activity and enzyme production
Co-composting is a microbe-mediated process, which involves the
succession of bacteria, actinomycetes, and fungi (Greff et al., 2021a;
Kutu et al., 2019). Previous studies demonstrated that inoculation with
preselected microorganisms may induce positive changes in the micro­
bial community composition of the composting material and in enzyme
activity (Chi et al., 2020; Fang et al., 2019; Kausar et al., 2013). Xu et al.
(2019a) applied Bacillus licheniformis, Aspergillus nidulans, and Aspergillus
oryzae as a mixed microbial inoculant during the early phases to accel­
erate the co-composting process of dairy manure and sugarcane leaves.
The inoculated pile was characterized by rapid succession of the mi­
crobial populations involved in organic matter and lignocellulose
decomposition and transformation. Kausar et al. (2013) added lig­
ninolytic and cellulolytic microbes to a mixture of rice straw and poultry
manure in a two-stage inoculation program (day 0: ligninolytic fungi,
day 12: cellulolytic fungi). Whereas bioaugmentation reduced the
abundance of bacterial including actinobacterial populations, the total
density of fungi significantly increased in the treated compost. More­
over, the lignocellulolytic fungi stimulated the growth of ligninolytic
and cellulolytic microorganisms, resulting in higher lignin peroxidase,
endoglucanase, and exoglucanase activities in the first half of the
co-composting process. Likewise, Wu et al. (2019) demonstrated that
various microbial inoculants could positively affect lignocellulose
degradation in straw–manure composts by increasing the relative
abundance of Firmicutes during the thermophilic stage of composting.
Awasthi et al. (2020) proposed that synthetic bacterial consortia may
permanently increase the numbers of aerobic cellulolytic bacteria. The
results of a co-composting study by Pandey et al. (2009) showed that
inoculation with fungi (i.e., Aspergillus awamori, Aspergillus nidulans,
Trichoderma viride, and Phanerochaete chrysosporium) could influence the
activity of β-1,4-exoglucanase, β-1,4-endoglucanase, β-glucosidase, and
xylanase in the early stage of composting. Zhao et al. (2017) inoculated a
dairy manure–corn straw compost with four different actinobacteria in
three steps (days 0, 6, and 15). This strategy promoted cellulose
degradation by increasing FPase and CMCase activities. Li et al. (2017)
studied enzyme activities during windrow composting of chicken
manure and corn stalks both with and without addition of a complex
microbial suspension. The use of inoculants significantly increased the
activities of catalase, urease, and cellulase, which indicated enhanced
B. Greff et al.
microbial concentrations and accelerated the degradation of cellulose
and N compounds. Li et al. (2019) performed pig manure–corn stalk
co-composting experiments with a compost-related bacterial culture
consisting of Acinetobacter pittii, Bacillus subtilis subsp. stercoris, and
Bacillus altitudinis. This microbial consortium was shown to reduce the
abundance of human disease-related functional genes.
4.1.3. Carbon-to-nitrogen ratio
The levels of bioavailable carbon and nitrogen in the composting
mixture can significantly influence the efficiency of microbial cultures
and the rate of biodegradation (El-Haddad et al., 2014). Carbon serves as
a source of energy for composting, whereas nitrogen is required for
protein synthesis and microbial growth (Zhou, 2017). Initially, the
optimal C/N ratio is in the range of 20–30:1 because microorganisms are
known to utilize approximately 30 parts of carbon for each part of ni­
trogen (Azim et al., 2018; Harindintwali et al., 2020). In contrast, the
final C/N ratio should be below 20–25, which indicates maturity and
safety (Awasthi et al., 2020; Jusoh et al., 2013). Taking this into account,
the environmentally friendly utilization of lignocellulosic residues is a
particularly difficult task. To achieve proper composting performance, a
high level of microbial activity is required during the composting pro­
cess (Henry et al., 2020).
Microbial additives can enhance the degradation of C and the
retention of N, resulting in a product with a reduced C/N ratio. Several
studies have reported that specific microorganisms are capable of pro­
moting the biodegradation of composting substrates (Gaind, 2014; Gao
et al., 2015; Kausar et al., 2014). At the same time, an increase in the
total and organic nitrogen (TN and ON, respectively) contents can also
be observed due to the concentrating effect of organic matter mineral­
ization (Sánchez-Mondero et al., 2001). Upon addition of a complex
fungal inoculant consisting of Aspergillus awamori, Aspergillus nidulans,
Trichoderma viride, and Phanerochaete chrysosporium to a mixture of
poultry droppings and wheat straw, a fast decrease in C/N ratio was
observed by Gaind et al. (2009) due to the higher TKN content. Similar
findings were reported by Pandey et al. (2009), although the composting
substrate was different. In a study by Abdel-Rahman et al. (2016),
bacterial cultures containing Bacillus licheniformis 1-1v or Bacillus
sonorensis 7-1v, or both strains caused a sharper decline in TOC content
during the first weeks of co-composting compared to the control treat­
ment. As for TN content, it gradually increased from day 23, and the
treated composts reached maturity (C/N ratio ≤20) 3–5 weeks earlier
than did the control compost. Jiang et al. (2015) reported that initial
inoculation with 1% of a nitrogen turnover bacterial culture facilitated
the composting process by reducing the N loss (from 45% to 35%) and
improving the TOC degradation rate. Liu et al. (2011) demonstrated that
cellulose degrading bacteria isolated from soil, straw, and fresh manure
supported TOC degradation and shortened the stabilization time of
manure–straw compost by 6 days. Selvamani et al. (2019) also used
indigenous bacteria to improve the co-composting process of poultry
manure and rice husk. Following 31 days, the inoculated mixture was
shown to have improved total and organic carbon contents, total ni­
trogen content, and C/N ratio compared to the uninoculated compost. In
addition to native isolates, commercially available inoculants may also
have a significant influence on the biodegradation process. Luyima et al.
(2019) successfully accelerated the maturation process in a maize sto­
ver–poultry litter compost by supplementation with a commercial
inoculant named Bio–soils compost+. The ratio of water-soluble carbon
to organic nitrogen in the inoculated bin was below 0.55 on week 12,
indicating a mature and stabilized product, whereas the control compost
remained immature until week 22. Likewise, another commercial
inoculant composed of Bacillus subtilis, Bacillus licheniformis, Phaner­
ochaete chrysosporium, Trichoderma koningii, and Saccharomyces cer­
evisiae promoted TOC mineralization and TN fixation, thereby reducing
the maturation time of pig manure compost (Xu and Li, 2017).
7
Journal of Environmental Management 302 (2022) 114088
4.1.4. Degradation of recalcitrant substrates
Although composts produced from raw lignocellulosic materials are
the main source of humus precursors (Bohacz, 2019b), lignin and cel­
lulose are the most stable fractions of total OM (Zhu et al., 2021).
Therefore, the breakdown of such polymers is a critical step determining
the composting process and the humification and stabilization of the
final product (Gou et al., 2017). To facilitate the biodegradation of
lignocellulosic wastes, several studies used microbial inoculants with
ligninolytic or cellulolytic properties (Wang et al., 2011; Zeng et al.,
2009). These microorganisms are capable of secreting extracellular en­
zymes to degrade lignin and cellulose (Wei et al., 2019; Zhao et al.,
2016).
Zhao et al. (2017) demonstrated that a three-stage inoculation with
cellulolytic actinomycetes could regulate the indigenous microbiota,
thus accelerating the degradation of cellulose fractions. Another study
involving cellulose-degrading actinobacteria showed increased cellulose
degradation (Zhao et al., 2016). Gou et al. (2017) reported that a psy­
chrotrophic–thermophilic complex microbial agent (PTCMA) including
a thermophilic cellulolytic fungal consortium (TCFC) could enhance the
decomposition of lignocellulose. On day 54, the lignin and cellulose
degradation rates were significantly higher in the inoculated composts
(TCFC: 35.0 and 50.0%, PTCMA: 35.4 and 51.1%) than in the control
product (26.7 and 30.2%). A similar trend was observed by Xu et al.
(2019a) in another study wherein a mixed microbial inoculant con­
taining Bacillus licheniformis, Aspergillus nidulans, and Aspergillus oryzae
resulted in increased degradation rates of cellulose, hemicellulose, and
lignin. Zhou et al. (2015) used a complex inoculation strategy for
co-composting dairy manure with rice straw. The degradation ratio of
lignin was higher in the inoculated compost than in the control pile from
day 15, with a final lignin degradation percentage of 35. Similar ob­
servations were made with respect to cellulose decomposition. Saha
et al. (2012) co-composted paddy straw and poultry droppings with or
without white rot fungi including Polyporus versicolor, Phanerochaete
chrysosporium, and Pleurotus sajor caju. Over the 5-week composting
period, increased lignin and cellulose decomposition rates were found in
the inoculated products, with combined total losses ranging from 10.4%
to 14.0%. The highest lignin and cellulose losses were observed upon
inoculation with Phanerochaete chrysosporium (11.2% and 15.3%,
respectively).
4.2. Effects of microbial inoculants on final compost quality
(humification, carbon-to-nitrogen ratio, macronutrient content, and
germination index)
The two key attributes of the final product of composting are
maturity and stability (Salgado et al., 2019). A high-quality compost can
safely be transported, stored, and used as soil amendment (van Heerden
et al., 2002). In contrast, the application of immature and unstable
compost may cause adverse environmental effects (Huang et al., 2006;
Wichuck and McCartney, 2010). However, compost quality assessment
is sometimes a difficult task (Moral et al., 2009). Therefore, as shown in
Table A2, a variety of parameters and criteria have been proposed to
evaluate the maturity and stability of composting products. Humus
formation, C/N ratio, nutritional value (e.g., total N, P, and K contents),
and GI are common indicators to evaluate the maturity, quality, and
phytotoxicity of composts (Gao et al., 2015; Wang et al., 2021b).
Inoculation with microbial cultures, including Penicillium expansum,
can improve the efficiency of the composting process and the overall
quality of composts (Wang et al., 2011). As regards co-composting of
crop residues with livestock manure, there have been numerous studies
on the impact of microbial inoculants on compost stability and maturity
(Table A3). The results indicated that the microorganisms used could
beneficially influence certain physical, chemical, and biological prop­
erties of composts, such as the rate of humification, macronutrient
content, OM content, C/N ratio, bulk density, GI, and the concentrations
of toxic elements. In a study by Gaind (2014), microbial inoculation was
B. Greff et al.
shown to result in mature composts with improved C/N (18.3–19.4) and
E4/E6 (5.3–6.3) ratios. Similarly, Wan et al. (2020) measured a signif­
icantly decreased E4/E6 ratio (2.3) in the inoculated compost, which
reflected a high degree of maturation. The addition of effective micro­
organisms can also influence macronutrient content indirectly by
decreasing the dry mass weight of the finished compost (Gao et al.,
2015). Wu et al. (2019) reported that the mixed culture of Trichoderma
viride and Trichoderma harzianum improved both the total N + P + K
content (inoculated compost: 12.29 and 11.78%; control compost: 10.87
and 11.17%) and the GI (86.54 and 74.21%) of untreated corn straw–pig
manure and rice straw–pig manure composts, respectively. Kausar et al.
(2014) also found fungal inoculation to increase the macronutrient
content of mature compost. Following 21 days of composting, the
inoculated product (pH 6.75) contained 2.48% of calcium, 1.14% of
phosphorus, 2.63% of potassium, and 1.42% of magnesium. By com­
parison, the control compost had considerably lower levels of macro­
nutrients (i.e., Ca: 1.71%, P: 0.95%, K: 2.19%, and Mg: 0.87%).
Abdel-Rahman et al. (2016) and Awasthi et al. (2020) observed that
bacterial inoculants could enhance final compost quality, in terms of
C/N ratio, available N, P, K content, and total N/P/K ratio, by supporting
degradation and maturation processes. This is in agreement with the
findings of Gao et al. (2015), who used a complex biological agent
containing various fungi and bacteria capable of increasing the total
potassium (TK) content (2.94–3.28%) and GI (73.7–76.1%) of the final
corn stalk–swine waste compost compared to the control treatments
(TK: 2.87–3.14%, GI: 65.6–73.2%). In addition, decreased C/N ratios of
below <20 were measured due to an accelerated reduction in OM.
However, inoculation had no additional effect on the levels of patho­
genic microbes and parasites (i.e., Escherichia coli and ascarid eggs).
In conclusion, the use of microbial additives can potentially improve
the co-composting process and final compost properties, including hu­
mification processes, C/N ratio, macronutrient content, and germination
index, but the quantity and quality of microbial inoculants should
carefully be considered prior to application based on the results of
previous studies.
5. Challenges and potential solutions during co-composting and
microbial inoculant application
5.1. Lack of information on industrial-scale co-composting
Although several studies reported that microbial inoculants could
expedite the co-composting process of lignocellulosic crop residues and
animal excreta, most researches were performed in small-scale com­
posting systems. To ensure sustainability in large-scale facilities, tech­
nical, environmental, economic, and social aspects of composting need
to be co-optimized. Currently, various sustainable composting methods
are available (e.g., rotary drum composting and other reactor technol­
ogies) that can reduce gaseous and odor emissions, leachate-related
problems, labor and operating costs, land requirement, composting
time, and noise pollution (Makan and Fadili, 2020).
Microbial inoculation techniques tend to be inexpensive biological
methods in waste management, but low efficiency and controlling issues
may be observed during full-scale composting (Fan et al., 2018a).
Furthermore, microbial additives, especially those containing
non-sporulating bacteria, are highly sensitive to storage conditions and
storage time. An inadequately chosen formulation technology can
reduce microbial viability and adaptability to composting substrates
(Berninger et al., 2018; Faure and Deschamps, 1991; Lobo et al., 2019).
Nevertheless, the integrated application of microorganisms and other
additives is an effective way to promote and optimize microbial activity
during composting (Awasthi et al., 2020).
To overcome the challenges facing industrial-scale composting,
future studies should consider the size of composting treatments, the
form of the microbial inoculants used, and the simultaneous application
of various additives.
8
Journal of Environmental Management 302 (2022) 114088
5.2. Gaseous and odor emissions
Stabilized compost, as an important source of organic matter, car­
bon, nitrogen, phosphorus, and potassium, supplies crops with available
macronutrients (Oldfield et al., 2018; Siddiquee et al., 2017; Steel et al.,
2012). Although properly managed composting has a slight environ­
mental impact, the loss of agronomic value (i.e., nutrient loss) through
nitrification, denitrification, NH3 volatilization, and methanogenesis is
inevitably part of the process via leaching and gaseous emissions of
ammonia, other volatile organic compounds, and greenhouse gases (e.
g., CH4 and N2O), contributing to odorous pollution and climate change
(Bryndum et al., 2017; Cao et al., 2019; Hwang et al., 2020; Sánchez
et al., 2015). Macronutrient losses may also limit the application po­
tential of compost as a plant nutrient source (Eghball et al., 1997).
However, nutrient loss can be minimized through the adjustment of
initial composting parameters, including C/N ratio, aeration rate, tem­
perature, moisture content, and structure of the feedstock (Bryndum
et al., 2017; Hwang et al., 2020). While the effects of various combi­
nations of organic and inorganic additives on emission have been
extensively studied in recent years (Awasthi et al., 2020; Cao et al.,
2019), there is scarce information in the literature on the influence of
bioaugmentation on gaseous emissions during co-composting of crop
residues with farm animal manure. Nevertheless, Yaman (2020) high­
lighted the importance of monitoring the composting process due to the
generation of greenhouse gases.
Jiang et al. (2015) reported the average ammonia emissions from
inoculated composts to range between 109 and 202 mg/m3 on days 2–20
of the composting process. The observed NH3–N losses in all treatments
were 14.5–22.7% of the total N loss. The results revealed that inocula­
tion with 1% of a nitrogen turnover bacterial culture during the early
phase of composting reduced NH3 emission and N losses compared to
the other microbiological treatments. Selvamani et al. (2019) also tested
the effect of a bacterial consortium on ammonia levels. Following 31
days of composting, the microbial additive significantly increased the
concentration of ammonia in the poultry manure–rice husk compost
(1770 ppm) compared to the control product (1360 ppm). Wan et al.
(2020) observed a decrease in the volatile solids content of an inoculated
compost due to volatilization of ammonia and methane. Awasthi et al.
(2020) experienced reduced levels of CH4 emission during the
co-composting process of cow manure and wheat straw involving a
bacterial inoculant. Compared to the control compost, inoculation
reduced the mass balance of CH4–C (i.e., from 0.42% to 0.28%). As for
nitrogen balance, the inoculated compost was characterized by
decreased total N loss (42.4%) and increased cumulative NH3–N emis­
sion (55.8 g).
Many of the reviewed studies have highlighted the importance of
using proper microbial inoculants for various feedstock materials.
However, bioaugmentation techniques can be combined with the
application of other additives to reduce the loss of agronomic value.
Gaseous emissions may be regulated by the use of bulking agents,
physical and chemical additives, aeration techniques, or mature
compost as a covering material (Cao et al., 2019; Ma et al., 2018; Ren
et al., 2010). Besides inoculants, addition of biochar, basalt, active
carbon, coir, clay, peat, zeolite, and certain chemicals (e.g., nitrification
inhibitors and acidic chemicals) and struvite crystallization method can
also control nitrogen loss and air pollution. Chemical reagents, including
magnesium oxide, magnesium hydroxide, phosphoric acid, calcium su­
perphosphate, phosphogypsum, or the integrated addition of lime and
struvite salts are some of the feasible options to precipitate the available
ammonia into struvite crystals without increasing the salinity and
reducing the microbial activity of feedstock (Chen et al., 2017; Ren
et al., 2010; Shan et al., 2021; Song et al., 2018; Zhang and Lau, 2007).
Moreover, the simultaneous application of magnesium sulphate with
calcium dihydrogen phosphate may also reduce the loss of CH4 and N2O,
respectively (Jiang et al., 2016).
B. Greff et al.
5.3. Emerging contaminants
Composting has become a widely adopted method to help the
bioremediation of organic residues (Kupper et al., 2008). Although it
follows strict recycling principles and the mature product has several
positive effects on the physical, chemical, and biological parameters of
soil, compost may introduce an abundance of pollutants into soil eco­
systems (Brändli et al., 2007). Inoculation with microbial additives can
affect the bioremediation process of specific substances, but only a few
studies have focused on the direct influence of bioaugmentation on the
passivation and reduction of pollutants during co-composting of ligno­
cellulosic agroresidues with animal manure. However, this is an
important issue because emerging contaminants may pose a significant
risk to human health (Cui et al., 2020) and, therefore, their reduction in
composts should receive increasing attention.
Farm animal manure is a major source of antibiotic residues (e.g.,
penicillin, tetracycline, streptomycin, sulfonamides, etc.) and ARGs
(Ezugworie et al., 2021; Gou et al., 2018; Li et al., 2020). During com­
posting, bacterial proliferation allows the spread of ARGs via vertical
gene transfer, while ARGs located on mobile genetic elements (MGEs)
contribute to the invasion of other bacteria via plasmid binding, trans­
posons, integrons, bacteriophages, and other mechanisms (Duan et al.,
2019b; Wang et al., 2021a). In a controlled composting environment,
the generation and degradation of ARGs are affected directly and/or
indirectly by microorganisms, microenvironmental parameters, and
horizontal gene transfer (Huang et al., 2021), while the concentrations
of residual antimicrobials decrease due to significant temperature in­
creases at the thermophilic stage (Yoshizawa et al., 2020). Similarly,
high temperature exposure during the thermophilic phase of composting
largely contributes to a reduction in ARGs and MGEs, but it should be
noted that thermal treatment often has a short-term effect only, and
ARGs may reemerge when the temperature drops (Cui et al., 2020).
Some researchers have attempted to improve the removal efficiency
of ARGs using microbial additives during lignocellulosic waste–animal
manure co-composting. Guo et al. (2020a) reported that Bacillus mega­
terium could largely enhance (i.e., by 65%) the removal of ARGs from
chicken manure–wheat straw compost, and especially the abundances of
tetW, tetM, and tetG encoding resistance to tetracyclines were decreased.
Wang et al. (2021a) co-composted swine manure with wheat straw.
Inoculation of the feedstock material with mature compost resulted in
promoting the growth of thermophilic bacteria and reducing the total
abundances of MGEs and ARGs. An increased peak temperature and an
extended thermophilic phase in the inoculated compost helped elimi­
nate the potential hosts of ARGs, including Romboutsia and Lactobacillus
spp. However, the abundances of total ARGs rebounded during the
second mesophilic phase because this stage must have provided condi­
tions suitable for regenerating the host bacteria of some ARGs. Overall,
inoculation with mature compost decreased the abundances of 10 out of
12 ARGs by up to 0.6 log cycles, and the total ARG removal rate was 1.11
times higher than in the control compost. Similar results were reported
by Zhong et al. (2021) with respect to bioaugmented biogas residue–pig
manure–rice straw compost.
In addition to the emerging pollutants mentioned, agricultural
wastes from heavy metal contaminated sites may also affect public
health via the food chain (Huang et al., 2017). Although some heavy
metals are essential for optimum plant growth, their excessive accu­
mulation in soils may be detrimental to plants and all other organisms in
the food chain (Mishra et al., 2017). The stabilization of these contam­
inants through co-precipitation, complexation, and adsorption with
various additives has been studied in detail (Mounissamy et al., 2021).
Nevertheless, their removal from solid wastes is a difficult process (Chen
et al., 2019a). A wide variety of fungi and bacteria can enhance the
passivation of heavy metals by producing chelating agents (Mishra et al.,
2017). In particular, humic substances (e.g., fulvic and humic acids) are
capable of influencing the bioavailability and toxicity of heavy metals
(Li et al., 2021; Pinto et al., 2020) and other soil–environment pollutants
9
Journal of Environmental Management 302 (2022) 114088
(Winarso et al., 2016). In a 60-day-long composting trial by Gaind et al.
(2009), supplementation with a complex fungal consortium resulted in
substantially reduced heavy metal contents in the products, with final
copper, iron, manganese, and zinc concentrations of 0.15, 2.10, 3.38,
and 2.06 mg/kg, respectively.
Overall, microbial inoculants may improve the removal of emerging
contaminants from manure- and lignocellulosic waste-based composts
by prolonging the thermophilic phase of composting, increasing the
activity and enzyme production of beneficial microorganisms, acceler­
ating the maturation process, and producing chelating agents.
6. Conclusions and future perspectives
Due to their physical and chemical properties, lignocellulosic crop
residues, and specifically their valorization, pose a great challenge to
sustainable agro-industry. However, co-composting with other types of
wastes is an effective way to eliminate the negative effects of these
byproducts (i.e., high C/N ratio, high level of lignocellulosic fractions,
low concentration of easily degradable organic matter, etc.) and con­
ventional composting approaches, thereby resulting in high-quality
organic fertilizers. Farm animal manure is a suitable co-composting
material to treat lignocellulosic biomasses by providing both nutrients
and microorganisms that can play a key role in the decomposition of
organic matter. Nevertheless, the efficiency of the co-composting pro­
cess may not be satisfactory if the natural microbiota lacks diversity or is
adversely affected by certain environmental factors. Over the past de­
cades, microbial amendments have been widely used to initiate and
speed up co-composting processes, promote the biodegradation of
feedstock materials, and ultimately produce mature and stable com­
posting products. Carefully chosen inoculants can positively influence
both the co-composting process and the quality of the final product if
optimum environmental conditions are provided.
This review article has summarized the major effects of bio­
augmentation on co-composting processes. The use of inoculants
composed of cellulolytic and/or ligninolytic microorganisms (i.e., Pha­
nerochaete chrysosporium, Trichoderma spp., Aspergillus spp., Actinomyces
spp., Streptomyces spp., and Bacillus spp.) is an effective approach to
facilitate the biodegradation of crop residues and farm animal manure,
resulting in an improved final product. Under optimum environmental
conditions, microbial inoculants prolong the thermophilic phase of
composting, regulate the abundance of microbial communities, accel­
erate the mineralization of composting substrates, and promote humus
formation. If applied to agricultural land, the final composting products
induce positive changes in the soil, stimulate the germination of seeds,
and ultimately increase crop productivity.
Although data on the specific ability of fungal and bacterial cultures
to remove emerging contaminants from feedstock materials are limited,
the use of microbial inoculants undoubtedly has beneficial effects on the
biological augmentation process as a whole. However, further research
needs to be conducted to comprehensively evaluate the specific effects
of microbial cultures on degradation processes, thereby making large-
scale co-composting environmentally and economically more feasible.
Such investigations should also focus on the effectiveness of microbial
inoculants combined with other organic and inorganic bulking agents
that can facilitate compost maturation and the removal of various
contaminants.
Credit author statement
Babett Greff: Conceptualization, Methodology, Investigation,
Writing – original draft. Jenő Szigeti: Conceptualization, Methodology,
Resources, Funding acquisition, Project administration, Investigation.
Ágnes Nagy: Conceptualization, Resources, Funding acquisition, Project
administration. Erika Lakatos: Resources, Funding acquisition, Super­
vision. László Varga: Conceptualization, Methodology, Supervision,
Formal analysis, Writing – review & editing. All authors have read and
B. Greff et al.
agreed to the published version of the manuscript.
Declaration of competing interest
The authors declare the following financial interests/personal re­
lationships which may be considered as potential competing interests:
This research was funded by the Government of Hungary, the European
Union, and the European Social Fund (grant number EFOP-3.6.3-
VEKOP-16-2017-00008). This research was supported by the ÚNKP-20-
3-II-SZE-16 New National Excellence Program of the Ministry for Inno­
vation and Technology from the source of the National Research,
Development and Innovation Fund.
Acknowledgments
This research was funded by the Government of Hungary, the Eu­
ropean Union, and the European Social Fund (grant number EFOP-3.6.3-
VEKOP-16-2017-00008). This research was supported by the ÚNKP-20-
3-II-SZE-16 New National Excellence Program of the Ministry for Inno­
vation and Technology from the source of the National Research,
Development, and Innovation Fund.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.jenvman.2021.114088.
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