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Journal of Hazardous Materials 461 (2024) 132446

Contents lists available at ScienceDirect

Journal of Hazardous Materials


journal homepage: www.elsevier.com/locate/jhazmat

Global landfill leachate characteristics: Occurrences and abundances of


environmental contaminants and the microbiome
Youfen Qian a, b, 1, Pengfei Hu a, b, 1, Naama Lang-Yona b, Meiying Xu c, Changhong Guo d,
Ji-Dong Gu a, b, e, *
a
Environmental Science and Engineering Research Group, Guangdong Technion - Israel Institute of Technology, 241 Daxue Road, Shantou, Guangdong 515063, China
b
Civil and Environmental Engineering, Technion – Israel Institute of Technology, Haifa 320003, Israel
c
Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, State Key Laboratory of Applied Microbiology Southern China, Guangdong
Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou 510070, China
d
Key Laboratory of Molecular Cytogenetics and Genetic Breeding of Heilongjiang Province, College of Life Science and Technology, Harbin Normal University, Harbin,
Heilongjiang 150025, China
e
Guangdong Provincial Key Laboratory of Materials and Technologies for Energy Conversion, Guangdong Technion - Israel Institute of Technology, 241 Daxue Road,
Shantou, Guangdong 515063, China

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Large regional variations are detected


among 318 landfill leachates globally.
• Heavy metals and new emerging con-
taminants are prevalent in leachates.
• Major microbes driving nitrogen turn-
over are identified in leachate
treatment.
• Correlation exists between specific mi-
croorganisms and leachate parameters.
• Leachate parameters are determinants
for the specific microbes.

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

Editor: Maria Sonia Rodriguez-Cruz Landfill leachates are complex mixtures containing very high concentrations of biodegradable and recalcitrant
toxic compounds. Understanding the major contaminant components and microbial community signatures in
global landfill leachates is crucial for timely decision-making regarding contaminant management and treatment.
Therefore, this study analyzed leachate data from 318 landfill sites primarily used for municipal solid waste
Keywords:
disposal, focusing on their chemical and microbiological characteristics. The most prevalent and dominant
Heavy metals
Emerging contaminants
components in landfill leachates are the chemical oxygen demand (COD, 3.7–75.9 × 103 mg/L) and NH+ 4
Global distribution (0.03–0.81 × 104 mg/L), followed by salt species such as SO2- 3 - 3
4 (0.03–5.25 × 10 mg/L), Cl (3.2–7.8 × 10 mg/L),

* Corresponding author at: Environmental Science and Engineering Research Group, Guangdong Technion - Israel Institute of Technology, 241 Daxue Road,
Shantou, Guangdong 515063, China.
E-mail address: jidong.gu@gtiit.edu.cn (J.-D. Gu).
1
These authors contributed equally to this work.

https://doi.org/10.1016/j.jhazmat.2023.132446
Received 8 February 2023; Received in revised form 13 August 2023; Accepted 29 August 2023
Available online 4 September 2023
0304-3894/© 2023 Elsevier B.V. All rights reserved.
Y. Qian et al. Journal of Hazardous Materials 461 (2024) 132446

Microbial composition K+ (0.58–4.20 × 103 mg/L), Na+ (1.3–13.0 × 103 mg/L) and Ca2+ (2.35–230.23 × 103 mg/L), which exhibit
Nitrogen turnover significant fluctuations. Heavy metals and metalloids are widely distributed in most landfill leachates but at
relatively low concentrations (<182.8 mg/L) compared to conventional parameters. Importantly, there is a
distinct global variation in the occurrence of emerging environmental contaminants (ECs). Among these com-
pounds, perfluorooctanoic acid (PFOA, 0.02–7.50 × 103 μg/L) of per- and poly-fluoroalkyl substances (PFAS),
bisphenol A (BPA, 0.01–33.46 × 103 μg/L) belonged to endocrine-disrupting compounds (EDCs), together with
di-ethyltoluamide (DEET, 1.0–1.0 × 103 μg/L) affiliated to pharmaceuticals and personal care products (PPCPs)
are the most frequently detected in landfill leachates. Additionally, the microbial community compositions in
most leachates are primarily dominated by Proteobacteria, Bacteroidota, Firmicutes, and Chloroflexi, and some
- -
of their abundances are correlated with the concentrations of NH+ 4 , NO3, Cl , Na and Cr. Notably, the leading
+

microbes driving advanced removal of inorganic nitrogen in the treatment systems are Candidatus Brocadia
(anammox), denitrifying Thauera, nitrite-oxidizing bacteria Nitrospira, along with ammonia-oxidizing bacteria
Nitrosomonas and Nitrosospira. The findings of this work provide a deeper insight into the leachate characteristics
and the sustainable management of landfill leachates, especially presenting a snapshot of the global distribution
of pollutants and also the microbiome.

1. Introduction communities [84,102]. However, majority of the reported studies only


include one or two types of landfill sites, and there is a lack of systematic
Landfills serve as the primary disposal sites for large quantities of analysis of microbial community characteristics in landfill leachates
consumer products at the end of their useful life [43]. The quantity of from different countries worldwide, especially with regard to metabol-
municipal solid wastes (MSWs) is projected to reach 3600 million tons ically functional microbes involved in the removal of nutrients such as
by 2050, exerting tremendous pressure on available land space and nitrogen. Furthermore, landfill physicochemical parameters such as
leachate treatment [16,67]. Landfill leachate is a highly contaminated NH+ 4 , total nitrogen (TN), salinity, pH, and others have been identified as
wastewater containing a wide range of pollutants, including heavy important driving forces shaping and influencing the microbial com-
metals, inorganic salts, nitrogen compounds, together with other toxic munity structure through canonical correlation analysis (CCA) [102],
and newly emerging pollutants [14]. The diverse physicochemical and redundancy analysis (RDA) [68], and principal component analysis
biological characteristics of landfill leachates are associated with the (PCA) [72]. Profiling the relationship between specific microbial groups
types of waste materials, landfill age, and construction methods [89]. and leachate parameters can provide valuable information about mi-
Landfill leachate contains multiple detrimental emerging contami- crobial ecophysiology and survival strategies in landfill leachates, thus
nants (ECs), including per- and poly-fluoroalkyl substances (PFAS), enhancing our understanding of treatment and management schemes in
pharmaceuticals and personal care products (PPCPs), and endocrine- the future.
disrupting compounds (EDCs) [94]. Owing to their unique properties This study sought to provide an overview of the contaminant dis-
such as hydrophobicity, lipophilicity, and high chemical stability, PFAS tribution in landfill leachates, as well as its microbial community
is persistent in leachate treatment systems [44]. PPCPs have raised composition and the potential taxa involved in nitrogen removal glob-
concerns regarding their toxic impacts on living organisms, their ally. Here, available data were compiled from published research arti-
contribution to the worldwide spread of antibiotic resistance genes cles to comprehensively analyze the occurrence and distribution of
(ARGs) [97], and the mobility and leakage of leachate that may exac- various chemical contaminants in landfill leachates across different
erbate the dispersal of these contaminants into surface sediment and continents and countries, covering conventional pollutants, heavy
groundwater [61]. Similarly, EDCs have also received increasingly metals, metalloids, and EDCs of public concerns. Additionally, we
public attention due to their widely occurrence in landfill leachates and retrieved raw amplicon sequences of the 16S ribosomal RNA (rRNA)
natural ecosystems, particularly their endocrine-disrupting effects on gene from published databases to uncover the microbial community
animals and public health [94]. As a result, there are extensive in- compositions in landfill leachates on a global scale, with a focus on the
vestigations on various individual types of pollutants, including works functional microbes involved in advanced nitrogen treatment. Finally,
on heavy metals [22,35], PFAS [43,98], EDCs [62,71], and PPCPs [95, correlation analysis was conducted to delineate the association between
101], along with other conventional nutrients such as BOD/COD, ni- microorganisms and leachate parameters. An examination of the avail-
trogen, and phosphorus. Also, most efforts have focused only on the able public literature reveals that this work is the first to integrate
leachates discharged from several local landfill sites, leaving a gap in conventional contaminants, heavy metals, emerging contaminants, and
scientific knowledge on the comprehensive understanding of the microbial community signatures, thus providing comprehensive infor-
occurrence and distribution of pollutants in landfill leachates around the mation about global landfill leachates for future management and
world. treatment of pollutants.
Microorganisms are the main processors for material transformation
of both toxic and non-toxic materials in various ecosystems, including 2. Materials and methods
landfills and leachate treatment plants. Their metabolic capacity to
mineralize and detoxify specific leachate chemicals is essential for 2.1. Public data acquisition for pollutants in landfill leachates
pollutant removal and water purification by degrading carbonaceous
and nitrogenous compounds in the leachates [8,53]. For instance, two To assess the current status of pollutant types and distributions in
strains of Novosphingobium with the potential to degrade aromatic hy- global landfill leachates, the published research articles (available on-
drocarbons were isolated from landfill leachate [26]. Currently, an line before September 2022) were searched from databases such as Web
increasing number of studies has taken advantage of the of Science, Google Scholar, Elsevier, and PubMed. The following search
culture-independent techniques (e.g., high-throughput sequencing) over terms were used to browse in the database: “leachate & endocrine-
the conventional culture-dependent (traditional isolation and cultiva- disrupting compounds”, “leachate & pharmaceuticals and personal
tion) one to detect and reveal the whole microbial community and care products”, “leachate & per- and poly-fluoroalkyl substances”,
composition in landfill leachates [19,28]. The recent advances in “leachate & heavy metal”, and “leachate & emerging pollutants”. After
application of sequencing technologies to analyze landfill leachates have receiving the full text, we first read the description of landfill sites in the
unveiled a variable and complex, but very unique, microbial Materials and Methods section of each article to determine if the

2
Y. Qian et al. Journal of Hazardous Materials 461 (2024) 132446

leachate was discharged from the landfills, excluding studies on soil figures were plotted based on the maximum concentration of a specific
leachate. Subsequently, data were collected from tables and supple- pollutant in each country, as this value is less influenced by the number
mentary tables instead of relying solely on the information provided in of sampling campaigns. The distribution of pollutants on a world map
figures, as detailed contaminant concentrations are often not captured in was implemented on the R platform (version 4.0.4) by the packages,
figures. When collecting pollutant information of landfill leachates, we including ggheatmap (version 2.1) and ggpubr (version 0.4.0), sp (version
recorded general parameters such as pH, conductivity (EC), chemical 1.4–5), ggplot2 (version 3.3.3), ggmap (version 3.0.0) and maptools
oxygen demand (COD), biological oxygen demand (BOD), ammonium (version1.1–1). The relationships between microorganisms and physi-
(NH+ 4 ), and total nitrogen (TN) as a group, rather than searching for each cochemical properties were inferred based on the Spearman correlation
parameter separately. The relevant articles were then manually exam- matrix using the R package psych (version 2.1.9), and then the re-
ined and the duplicated data were eliminated to avoid redundancy in the lationships with significant correlation (r > 0.6 or r < –0.6, p < 0.05)
final dataset. As a result, we collected 65 relevant studies with 318 were selected to visualize by R package pheatmap (version 1.0.12).
landfill leachate sites worldwide (Table S1). From the collected infor-
mation, it appears that most landfills generating leachate primarily 3. Results and discussion
receive municipal solid wastes (MSWs), whereas a few receive both
household waste and nonhazardous industrial waste due to the lack of 3.1. Temporal and geographical pattern of MSW production
strict waste sorting (Tables S3 and S4).
Landfill leachate is a dark-colored toxic liquid containing a complex
2.2. Microbial data collection of landfill leachate sites or plants mixture of chemical constituents, which are formed through the inter-
action between water (rainfall, groundwater, surface water, etc.) and
Bacterial and archaeal 16S rRNA gene sequences from the GenBank waste materials in landfills. Landfills receive the largest proportion of
database (data accessed by September 2022) were retrieved using the municipal solid wastes (MSWs) in most regions, especially in developed
SRA Toolkit. The keywords “landfill leachate” or “((landfill leachate) countries. The global amount of MSWs is projected to reach approxi-
AND heavy metal) AND microbial community” or “((landfill leachate) mately 2.2 billion tonnes by 2025 [27], and it appears that this esti-
AND pollutants) AND microbial community” or “landfill leachate mi- mated value may be surpassed much sooner than expected [63]. Over
crobial community” were searched in the SRA database to obtain raw the past few decades, the United States (US) has consistently produced a
reads. We also recorded the physicochemical parameters corresponding high volume of MSWs, reaching 243 million tonnes in 2017 (Fig. 1,
to the microbial data as much as possible in the sources of Web of Sci- Table S5). Similarly, China has also experienced significant increases in
ence, Google Scholar and Elsevier, because such information is generally the volumes of MSWs, reaching 215 million tonnes by 2017 due to rapid
unavailable in the GenBank database. In the end, a total of 339 microbial urbanization and development. Certain countries that generate rela-
SRAs (Sequence Read Archive) were retrieved from publicly available tively small amounts of MSWs, including Russia, Mexico, France,
datasets (Table S2). Among them, 68 microbial SRAs had corresponding Colombia, and Indonesia, have shown a consistent yearly increase
physicochemical properties, including general leachate parameters and (Fig. 1, Table S5). With more than half of the MSWs being sent to
heavy metal concentrations, but no information on toxic and hazardous landfills in many countries (e.g., 52.6 % in the US in 2014, 54 % in
pollutants was available (Table S3). Australia and 56 % in China in 2017) [78,87], a large volume of leachate
containing various toxic pollutants is generated, thus highlighting the
2.3. Bioinformatic analysis urgent need for effective treatment strategies.

The raw sequence reads were processed and analyzed using a pre- 3.2. Conventional physicochemical characteristics in landfill leachates
viously described bioinformatics pipeline [65] with the open-source
QIIME (Quantitative Insights Into Microbial Ecology) software [13]. This analysis was based on landfill leachate data from 318 landfill
First, the raw data were filtered to remove low-quality reads and sites in 24 countries (Table S1). Leachates exhibited a wide range of pH
generate amplicon sequence variants (ASVs) using the DADA2 denoising values, typically between 4.5 and 10.8 (Table S4), which was likely
algorithm [11] as implemented in QIIME2. To maximize the data influenced by the landfill age [89]. For example, leachate from fresh
available for downstream analyses, a re-sampling depth of 30.052 × 103 landfills (less than 5 years old), characterized by active fermentation and
reads per sample was applied for bacterial analysis. Taxonomic assign- acetogenic activity, typically displayed acidic pH values, whereas
ments of the presentive bacterial ASV sequences were conducted using leachate from active and mature landfills (over 10 years old) with
the classifier of SILVA database (version 138) [66]. However, comam- methanogenic activity tended to have alkaline pH values [87]. There-
mox bacteria could not be fully classified because the SILVA database fore, the pH condition can be generally used to estimate the develop-
was incomplete. Sequences belonging to the Nitrospirota phylum were mental stage of landfills, thus enabling adjustments to enhance
extracted from the QIIME2 output sequence table using Python (version microbial fermentation and methanogenesis for leachate treatment.
3.9) and manually re-assigned based on BLAST using the 16S rRNA gene Chemical oxygen demand (COD) content was notably high, partic-
of the four currently available species (Candidatus Nitrospira nitrosa, ularly in China (0.5–75.9 g/L), the US (0.33–10.10 g/L), and India
Candidatus Nitrospira inopinata, Candidatus Nitrospira nitrificans, and (0.44–15.42 g/L) (Fig. 2A). Generally, the contents of biological oxygen
Candidatus Nitrosoglobus). Denitrifiers, ammonia-oxidizing bacteria demand (BOD), total organic carbon (TOC), and dissolved organic car-
(AOB), ammonia-oxidizing archaea (AOA), and anammox bacteria were bon (DOC) followed a similar trend to the COD level. The content of
manually confirmed from the ASV tables using information from liter- organic compounds in landfill leachate depends on various factors,
ature reports. The microbial community compositions were visualized including the types of waste materials, waste moisture, landfill design,
using the barplot module in HUMAnN 3.0 [7]. compaction rate, waste decomposition rate, operational management,
and landfill age [58,89,90]. As the landfill ages, the BOD content de-
2.4. Compilation of physicochemical parameters and correlation analysis creases more rapidly than the COD content due to the accelerated
degradation of biodegradable waste. Consequently, the BOD/COD ratio
The concentrations of per- and poly-fluoroalkyl substances (PFAS), in the leachate of young landfills (0.4–0.6 or higher) is higher than that
endocrine-disrupting compounds (EDCs), pharmaceuticals and personal of older landfills (0.05–0.20) [2]. Additionally, regional differences in
care products (PPCPs), heavy metals, and metalloids, along with their organic compounds may also be attributed to economic development (e.
corresponding general parameters, are summarized in Table S4. To g., industrial expansion), population density, and consumption patterns
visualize the global distribution of each pollutant in landfill leachate, the [25,95]. Consumption patterns are reflected in variables such as average

3
Y. Qian et al. Journal of Hazardous Materials 461 (2024) 132446

Fig. 1. Global production trends of municipal solid wastes (MSWs) in different countries. Specific values are provided in Table S5.

annual per capita consumption expenditures of urban households on in humid and rainy areas, whereas they may be elevated in less rainy and
food, clothing, housing, and services, which contribute to variations in arid regions [2].
waste generation and contaminant composition in leachates [48,64]. Given that K+ and Na+ are typically retained in the leachate in their
Moreover, the generation rates of organic waste (e.g., plastics, paper, soluble forms, they are rarely precipitated or adsorbed onto other sub-
textiles, and discarded food) are significantly correlated with population stances [6] and exhibit extremely high concentrations, even up to
density and household size [69,79]. 1.26–4.20 g/L and 1.0–13.0 g/L in Croatia (Fig. 2B, Table S7). Besides,
- - 2- - 3-
Inorganic ions, generally including NH+ 4 , NO3, NO2, SO4 , Cl , PO4 , some leachates also contain substantial quantities of Ca2+, such as in
HCO-3, K+, Ca2+, Na+, Mg2+, and soluble Fe2+/ Fe3+ species are typical Lebanon (12.01 × 103–230.23 × 103 mg/L) and the US (2.0–4.1 × 103
constituents in landfill leachates [34] (Fig. 2). During the anaerobic mg/L) (Fig. 2B, Table S7). The high concentrations of these inorganic
degradation of landfill waste, different functional microorganisms cations and anions pose challenges to the biological processes involved
convert insoluble biological polymers (e.g., paper, garden and vegetable in leachate treatment.
waste), as well as proteins and fats (animal matter) into soluble sugars
and amino acids. These are then hydrolyzed and fermented to fatty 3.3. Geographical distribution of metals and metalloids in landfill
acids, alcohol, and NH+ 4 , which accumulate in the leachate [9]. Among leachates
these compounds, NH+ 4 is the most predominant and universal inorganic
species. High concentrations of NH+ 4 are observed in China (110.0–5.9 × The concentrations of metals and metalloids in landfill leachates
103 mg/L), India (0.5–2.6 × 103 mg/L), the US (13.0–1.8 × 103 mg/L), vary on a global scale, and their concentrations are generally low
Portugal (~3.05 × 103 mg/L), Croatia (480.0–1.8 × 103 mg/L), the compared to the aforementioned NH+ 4 and COD (Fig. 2). However, the
Netherlands (0.03–8.10 × 103 mg/L) and Italy (~2.34 × 103 mg/L) non-biodegradable nature of metal and metalloid elements allows them
(Fig. 2A, Table S6). Additionally, SO2- -
4 and Cl contribute a substantial to persist in landfill leachate for a long time, thus hindering effective
portion of anions to landfill leachates. For example, high concentrations biological activity and treatment processes [88]. At first glance, China,
of SO2- 3 3
4 are observed in India (3.30 × 10 –4.74 × 10 mg/L), China Japan, and the US exhibit relatively high concentrations of manganese
3 3
(48.0–5.2 × 10 mg/L), the US (0.03–3.43 × 10 mg/L), Japan (Mn) (>10 mg/L) (Fig. 2B). This can be attributed to the large popula-
(58.0–1.5 × 103 mg/L), and Lebanon (6.0–1.5 × 103 mg/L). The pres- tion and low recovery rates in these countries, where e-waste containing
ence of SO2-4 in the leachate may be partly attributed to the addition of batteries are discarded into landfills instead of proper recycling, leading
sulfuric acid used in wastewater membrane treatment (e.g., nano- to the release of significant amounts of Mn into the leachate [60].
filtration and reverse osmosis systems) to prevent clogs [23,41]. In this Typical heavy metal species such as Cr, Ni, Cu, Cd, and Pb, with con-
process, most of the SO2- 4 is then transported into the concentrated centrations below 182.8 mg/L are ubiquitous in the landfill leachates
compartments and subsequently sprinkled on the surface of landfill analyzed in this study (Fig. 2B, Table S7) due to non-segregated waste
waste, leading to the gradual accumulation of SO2- 4 in landfill leachate dumping in many countries [39]. Regarding metalloids such as As and
[49,81]. Similarly, Cl- is also widely distributed in leachates, with the Se, much lower concentrations below 7.7 mg/L were observed in landfill
most notable examples being the US (3.0–7.2 × 103 mg/L), China leachates across multiple countries (Fig. 2B, Table S7), with Hg and Co
(1.69 × 103–2.52 × 103 mg/L), Portugal (~2.6 × 103 g/L), Nigeria exhibiting similar levels. It should be noted that data on the distribution
(30.0–3.1 × 103 mg/L), Malaysia (130–2 × 103 mg/L), Japan of metals and metalloids in African countries are scarce or absent, which
(50.0–7.8 × 103 mg/L) and Poland (< 1.21 × 103 mg/L) (Fig. 2A, is likely due to the limited acquisition of analytical techniques for
Table S6). Regional variations in anion concentrations of landfill analysis and reporting rather than the actual absence of contaminants in
leachate among countries may be influenced by local conditions, con- landfill leachates in these regions [31].
sumption patterns, and waste management practices [80]. The income
levels of a country can also influence the composition of solid waste and
waste generation per capita, and further affect the distribution of anion
components in leachate. Moreover, anion concentrations may be diluted

4
Y. Qian et al. Journal of Hazardous Materials 461 (2024) 132446

Fig. 2. The distributions of conventional parameters (A) and metal elements (B) in landfill leachates from different countries. The numbers in the circles represent
specific parameters. Maximum concentrations are indicated by a color gradient. A detailed list of concentrations is provided in Table S6 and Table S7.

3.4. Occurrence and abundance of emerging contaminants in landfill (Fig. 3A), with Australia (0.02–7.50 × 103 μg/L) and the US
leachates (0.03–4.80 × 103 μg/L) exhibiting the highest concentrations, followed
by China (0.3–214.0 μg/L) and Finland (~76.2 μg/L) (Fig. 3A,
Per- and poly-fluoroalkyl substances (PFAS). The occurrence of PFAS in Table S8). Additionally, since these contaminants were extracted from
landfill leachates varies across different countries. From a regional non-filtration leachates [24], other PFAS pollutants are also very serious
perspective, perfluorooctanoic acid (PFOA) is the most frequently in Australia, with generally higher concentrations than in other coun-
detected PFAS in landfill leachate samples from all eight countries tries. Moreover, some countries need to pay more attention to the hazard

5
Y. Qian et al. Journal of Hazardous Materials 461 (2024) 132446

Fig. 3. The occurrences of emerging contaminants (ECs) in landfill leachates from different countries. The concentrations of per- and poly-fluoroalkyl substances
(PFAS) (A), endocrine-disrupting compounds (EDCs) (B), and pharmaceuticals and personal care products (PPCPs) (C) in landfill leachates worldwide. Detailed
concentrations of these three types of pollutants are available in Table S7, Table S8, and Table S9.

of short-chain PFAS. For example, landfill leachates in China contain a tumors [20,86]. However, conventional activated sludge processes in
high concentration of perfluorobutane sulfonic acid (PFBS), while leachate treatment plants are ineffective for PFAS degradation due to
leachates in the US exhibit high concentrations of short-chain PFAS, their unique molecular structure and strong C-F bond energy
including perfluorobutanoic acid (PFBA), perfluoropentanoic acid (536 kJ/mol), which hinders biotransformation [56]. Therefore, addi-
(PFPeA), perfluorohexanoic acid (PFHxA), perfluoroheptanoic acid tional effective treatment methods, including physical adsorption,
(PFHpA), and 3-perfluoropentyl propanoic acid (5:3 FTCA) (Fig. 3A). chemical catalysis, and membrane technology [4,10], can be imple-
Generally, exposure to PFAS leads to various adverse health effects, such mented in current treatment systems to effectively remove and/or
as immunotoxicity, neurotoxicity, reproductive deficits, and pancreatic degrade PFAS.

6
Y. Qian et al. Journal of Hazardous Materials 461 (2024) 132446

Endocrine-disrupting compounds (EDCs). The concentrations of EDCs 3.5. Microbial composition and nitrogen-transforming networks
in landfill leachates are high and vary significantly between countries
(Fig. 3B). Bisphenol A (BPA), which has been linked to estrogenic effects We analyzed the prevalence and abundance of taxa based on mi-
and symptoms of attention-deficit/hyperactivity disorder in humans crobial raw sequences obtained from 339 landfill leachate samples from
[36,42], is the most frequently detected and abundant pollutant in the different countries (Table S2). The data revealed that most leachate
US (0.63–6.38 × 103 μg/L), China (0.98–3.27 × 103 μg/L), Germany samples contained species from the four dominant phyla: Proteobac-
(110–25 × 103 μg/L), Greece (~2.19 × 103 μg/L), and Italy (~33.46 × teria, Bacteroidota, Firmicutes, and Chloroflexi. However, the relative
103 μg/L) (Fig. 3B, Table S9). The high concentration of BPA is attrib- abundances of these phyla varied significantly among the samples
uted to its release from synthetic polymers/plastics and thermal paper in (Fig. 4A). Consistent with previous studies [32,102], these four phyla
landfills [55]. Additionally, the leachate samples collected from a were found to be the predominant bacteria in landfill leachates
membrane process in China contained relatively high concentrations of regardless of geographical location. Additionally, certain microorgan-
di-ethyl phthalate (DEP) and dimethyl phthalate (DMP), with concen- isms appeared to be specific to particular landfill leachate types or lo-
tration ranges of 1.0–1.4 × 103 μg/L and 1.0–1.7 × 103 μg/L, respec- cations. For instance, Actinobacteriota and Patescibacteria exhibited a
tively (Fig. 3B, Table S9). These compounds are common plasticizers higher proportion in several leachates from Norway and Greece
used in plastic products, and their concentration can be as high as 40 % compared to other regional leachates (Fig. 4A). These results suggest
by weight in commercial PVC. Previous studies have shown that that, although typical microorganisms are ubiquitously present in all
long-term exposure to DEP induces reproductive toxicity, develop- landfill leachates, their abundance can vary depending on the properties
mental toxicity, and hepatic effects in organisms even at low doses of the landfill leachates [70].
(0.173 mg/kg-day) [85]. Likewise, DMP has been linked to neurotoxic, Leachate treatment systems harbor a significant number of micro-
reproductive, and endocrine-disruptive responses [18]. These results organisms [93], but their metabolism and functions are often poorly
emphasize the need for comprehensive removal of EDCs during landfill understood. However, based on our previous findings in wastewater and
leachate treatment to prevent unpredictable risks upon discharge into leachate treatment plants [5,52,92], we can speculate the role of mi-
the surrounding environment [95,101]. croorganisms in nitrogen cycling. Ammonium, a common pollutant in
Pharmaceuticals and personal care products (PPCPs). The concentra- landfill leachates, can reach concentration as high as 8.1 × 103 mg/L
tions of PPCPs in landfill leachates also vary considerably among (Fig. 2A, Table S6). Therefore, we analyzed the microorganisms
different countries. The three most abundant compounds identified in involved in ammonium transformation, including denitrifiers,
US landfill leachates are diethyltoluamide (DEET, 7.0–1.0 × 103 μg/L), ammonia-oxidizing archaea (AOA), ammonia-oxidizing bacteria (AOB),
acetaminophen (< 117 μg/L), and nicotine (0.06–61.40 μg/L) (Fig. 3C, nitrite-oxidizing bacteria (NOB), complete ammonia oxidation
Table S10). Similarly, landfill leachates in Germany exhibit relatively (comammox) bacteria, and anaerobic ammonia oxidation (anammox)
high concentrations of nicotine (110–960 μg/L), caffeine (5–430 μg/L), bacteria (Fig. 4B–E). Notably, in these leachate treatment systems, the
cotinine (88–180 μg/L), and propyphenazone (1–140 μg/L). Singapor- main process of ammonium oxidation to nitrite is carried out by AOB,
ean landfill leachates also show a significantly higher concentration of such as Nitrosomonas and Nitrosospira, rather than AOA (Fig. 4C, and E).
acetaminophen (~2.204 × 103 μg/L). In China, the dominant com- The resulting nitrite is then utilized through three primary biochemical
pounds in landfill leachates are caffeine (0.03–586.0 μg/L), sulpiride pathways: denitrification of nitrite to dinitrogen by Thauera (Fig. 4D,
(1.6–546.0 μg/L), and ibuprofen (0.3–137.8 μg/L), with many other and E), the oxidation of nitrite to nitrate by Nitrospira ( Fig. 4D, and E),
pharmaceuticals present at concentrations higher than 20 μg/L, and the coupling of nitrite with ammonium to form dinitrogen (N2) by
including clofibric acid, diethyltoluamide, erythromycin, sulfadiazine, Candidatus Brocadia (anammox) (Fig. 4C, and E). Additionally,
ofloxacin, norfloxacin, and diclofenac (Fig. 3C, Table S10). The regional comammox species, such as Candidatus Nitrospira nitrosa, Candidatus
variations in PPCPs in landfill leachate are closely related to the complex Nitrospira inopinata, and Candidatus Nitrospira nitrificans, can directly
of physical absorption, chemical transformation, and biodegradation convert ammonium to nitrate, but their abundance in the leachate
processes that occur in landfills [1,87]. Physical absorption, which is treatment systems is much lower compared to other
influenced by the hydrophilic and hydrophobic properties of PPCPs, nitrogen-transforming members (Fig. 4D). These findings suggest that
affects the fate and mobility of these compounds in the landfill envi- the removal of ammonium in landfill leachate primarily occurs through
ronment, causing them to either bind selectively to waste or enter the the combined action of AOB, NOB, denitrifiers, and the anammox pro-
leachate with water [45,74]. Redox or chelating reactions between cess. Thus, a complex network of nitrogen transformation reactions
PPCPs and metal elements in landfills can also influence the chemical involving multiple microorganisms [40] is responsible for ammonium
transformation and mobilization of contaminants [15]. The resistance of removal in landfill leachates (Fig. 4E).
PPCPs to microbial biodegradation in waste may determines the extent The anammox process has garnered considerable attention due to its
to which they migrate into leachate. For example, compounds like gli- potential for energy savings, low sludge generation, and low greenhouse
clazide and glyburide are difficult to decompose in landfills [50,96]. gas emission rates compared to conventional nitrification/denitrifica-
PPCPs have been detected in various environmental matrices such as tion processes [53]. However, this technology still faces several note-
streams [3], domestic wastewater [91], and sewage treatment plants worthy challenges, including the slow growth rate of anammox bacteria
[76]. The wide distribution of PPCPs in leachate can be attributed to two (about one week) and their sensitivity to environmental conditions such
reasons: (i) waste from hospitals and pharmaceutical manufacturers as temperature, pH, organic matter, dissolved oxygen (DO), as well as
being transferred to landfills without following public health regula- their affinity for ammonium and nitrite [51,83]. Various strategies have
tions, and (ii) the disposal of unused and expired PPCPs in landfills been implemented to maintain the biomass of anammox bacteria and
alongside regular household waste, where long-term chemical and bio- render them less sensitive to adverse environmental conditions, thus
logical processes lead to the release of PPCPs from solid waste into ultimately improving nitrogen removal. These strategies include gran-
leachate [47]. Due to the widespread use of PPCPs and the challenges in ulation [75], anoxic moving bed reactors [46], gel entrapment [30], and
regulating and controlling strategies, their occurrence and distribution membrane technology [37]. Given that landfill leachate contains humic
in the ecosystem can have pronounced impacts on both ecosystem and acid, heavy metals, and refractory compounds, these strategies should
human health [17]. Moreover, some transformation intermediates of be further tested and improved through field engineering practices.
PPCPs exhibit higher toxicity than the parent compounds, even at low
concentrations (ng/L) they have high biological activity to affect health
of living organisms and also to induce antibiotic resistance in native
microbial populations [38].

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Y. Qian et al. Journal of Hazardous Materials 461 (2024) 132446

Fig. 4. Microbial community composition in global landfill leachate and specific microorganisms involved in the nitrogen cycle. (A) Relative abundance of microbes
at the phylum level, grouped by countries. (B) Relative abundance of denitrifiers in landfill leachates at the genus level. (C) Relative abundance of comammox
bacteria, ammonia-oxidizing bacteria (AOB), ammonia-oxidizing archaea (AOA), and anammox bacteria in landfill leachate systems. (D) Average relative abundance
of microorganisms involved in the nitrogen turnover. (E) Summary of microorganisms most likely to participate in the nitrogen cycle, which is important for the
removal of ammonium from landfill leachates.

3.6. Correlation between environmental variables and microbial properties and metal elements without any ECs (Table S3), we focused
communities on the relationship between the microbial community and the first two
types of leachate parameters (conventional physicochemical properties
Spearman’s rank-order correlation test was conducted to statistically and metal elements). In total, 185 bacteria were associated with pH, 16
- 2- -
analyze the relationships between leachate parameters and microbial with NH+ 4 , 93 with NO3, 22 with TN, 5 with SO4 , and 13 with Cl
communities based on the abundance of genera. Since the microbial (Table S11). Among these, Candidatus_Megaira (r = –0.66, p < 0.05),
data from the literature only included conventional physicochemical Mitochondria (r = –0.67, p < 0.05), Candidatus Komeilibacteria

8
Y. Qian et al. Journal of Hazardous Materials 461 (2024) 132446

(r = –0.63, p < 0.05) exhibited a negative correlation with ammonium, correlations with pH (r = 0.64, p < 0.05) in landfill leachates (Fig. 5,
suggesting that these bacteria are sensitive to the available NH+ 4 . An Table S11). This phenomenon is consistent with previous reports in the
NH+ 4 concentration between 0.05 and 0.20 g/L favors microbial meta- ocean [77] and soil [99]. Although a relatively high pH (> 9.0) would
bolism, whereas concentrations between 1.5 and 3.0 g/L have an inhibit the growth of Nitrospira, many findings have shown that the
inhibitory effect on the microbial anaerobic process, and concentrations optimal pH for Nitrospira is slightly alkaline, such as the 8.0–8.3 range in
above 3.0 g/L have a toxic effect on microbial growth [33,87]. The high membrane bioreactors [100], 7.6–7.8 in nitrifying intermittently
NH+ 4 concentrations that typically occur in landfill leachates may aerated reactors [59], and 7.6–8.0 in pure culture media for isolation of
adversely affect the biochemical reaction of some microorganisms. Nitrospira moscoviensis sp. Ehrich et al., ($year$) [21]. These results
Additionally, NO-3 is generally considered less toxic to living organisms indicate that Nitrospira may tend to grow more readily in medium-aged
than NH+ 4 [12], and the NH4 concentration (Max. 8.1 g/L) is much
+
leachate (5–10 years old, pH 7.55–7.85) compared to young leachate
-
higher than NO3 (Max. 0.254 g/L) (Fig. 2A), suggesting that NH+ 4 (less than 5 years old, pH 5–6) [87].
toxicity is further exacerbated by its extremely high concentration in Among the evaluated metal elements (Fig. 5, Table S11), Ca2+ was
landfill leachate. The concentration of SO2-
4 is positively correlated with positively correlated with Dechlorobacter (r = 0.66, p < 0.05) and Pseu-
Dechlorobacter (r = 0.60, p < 0.05), Halocella (r = 0.61, p < 0.05), darcobacter (r = 0.62, p < 0.05), which was attributed to the influence
Arcobacter (r = 0.81, p < 0.05), Comamonas (r = 0.60, p < 0.05), and of calcium on the adhesion behavior of microorganisms and the
Petrimonas (r = 0.61, p < 0.05) (Fig. 5, Table S11). Our previous find- enhancement of EPS structural stability [82]. Moreover, Mg2+ was
ings demonstrated that Petrimonas can work synergistically with Desul- positively associated with Sulfurospirillum (r = 0.71, p < 0.05) and sol-
fovibrio to promote the degradation of organic pollutants with sulfate as uble Fe was moderately correlated with UCG_012 belonged to Syn-
the sole electron acceptor [65]. ergistotam (r = 0.64, p < 0.05) and BBMC_4 belonged to Fibrobacterota
The composition of microbial communities and dominant bacteria (r = 0.62, p < 0.05). Additionally, Na+ exhibited a positive relationship
exhibit distinct variations with changes in pH at different landfill ages with 22 genera including halophilic bacteria [57,73], such as Halocella
[89]. Nitrospira, a nitrite-oxidizing bacteria, exhibited positive (r = 0.65, p < 0.05), Ectothiorhodospira (r = 0.61, p < 0.05), and

Fig. 5. Spearman rank correlation between environmental parameters and microbial species richness. The corresponding ‘r’ value ranges from –0.76–0.89
(Table S11); the red squares represent significantly positive correlations (r > 0.6, p < 0.05), whereas the blue squares represent significantly (r < –0.6, p < 0.05)
negative correlations. The genera within each phylum are represented by different colored ellipses and pentagrams.

9
Y. Qian et al. Journal of Hazardous Materials 461 (2024) 132446

Pseudomonas (r = 0.72, p < 0.05) in these high salinity leachates [61]. CRediT authorship contribution statement
Regarding heavy metals, the only observed relationship was between Cr
and microorganisms. Specifically, Cr showed a positive correlation with Youfen Qian: Investigation, Data curation, Formal analysis, Writing
Aequorivita (r = 0.605, p < 0.05) but was negatively correlated with – original draft. Pengfei Hu: Validation, Investigation, Methodology.
Babeliales (r = –0.66, p < 0.05), Candidatus_Komeilibacteria Naama Lang-Yona: Writing – review & editing, Conceptualization,
(r = –0.609, p < 0.05), and BSV26 affiliated with Bacteroidota Supervision. Meiying Xu: Methodology, Writing – review & editing.
(r = –0.63, p < 0.05) (Fig. 5, Table S11). The positive correlation in- Changhong Guo: Methodology, Conceptualization. Ji-Dong Gu:
dicates that the presence of Cr enhances microbial abundance [54], Formal analysis, Writing – review & editing, Supervision.
implying that Aequorivita may survive under Cr stress. However, infor-
mation on the Cr tolerance of this genus is currently unavailable. In Declaration of Competing Interest
contrast, Cr contamination in leachate treatment systems may adversely
affect the survival of selective microorganisms, e.g., inhibition of bio- The authors declare that they have no known competing financial
logical dehydrogenase activity [29]. interests or personal relationships that could have appeared to influence
the work reported in this paper.
4. Conclusion and future prospects
Data Availability
This study provides the first detailed analysis of conventional pa-
rameters, heavy metals, ECs, and microbial community traits in leach- Data will be made available on request.
ates collected from 381 landfills worldwide. Landfill leachates
commonly exhibit alarmingly high concentrations of COD and ammo-
2- - Acknowledgements
nium (NH+ 4 ), followed by sulfate (SO4 ), chloride (Cl ), potassium (K ),
+
2+
sodium (Na ), and calcium (Ca ), while the concentrations of heavy
+
This work was supported by the National Key Research and Devel-
metals and metalloids are relatively low. Moreover, ECs in landfill
opment Program of China (No. 2021YFA0910300), and National Natu-
leachates exhibit high spatial variability, with PFOA, BPA, and DEET
ral Science Foundation of China (No. 92051103).
being the most frequently detected compounds in the majority of land-
fills in different countries. Additionally, the dominant microorganisms
Appendix A. Supporting information
in landfill leachates are Proteobacteria, Bacteroidota, Firmicutes and
Chloroflexi, some of which are affected by the concentrations of
- - Supplementary data associated with this article can be found in the
ammonium (NH+ 4 ), nitrate (NO3), chloride (Cl ), sodium (Na ), chro-
+
online version at doi:10.1016/j.jhazmat.2023.132446.
mium (Cr), and others. Nitrogen removal is mainly carried out by Can-
didatus Brocadia (anammox), Thauera (denitrifier), and Nitrospira
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