Review
Key factors driving the fate of antibiotic resistance genes and controlling strategies during aerobic composting of animal manure: A review

https://doi.org/10.1016/j.scitotenv.2021.148372Get rights and content

Highlights

  • Fate of antibiotic resistance genes (ARGs) is intricate in animal manure composting.

  • Dynamic variations of biotic factors are the direct driving factors of ARGs.

  • Most key abiotic indicators interference with ARGs indirectly.

  • Controlling strategies mainly have four ways to improve the removal of ARGs.

Abstract

Occurrence of antibiotic resistance genes (ARGs) in animal manure impedes the reutilization of manure resources. Aerobic composting is potentially effective method for resource disposal of animal manure, but the fate of ARGs during composting is complicated due to the various material sources and different operating conditions. This review concentrates on the biotic and abiotic factors influencing the variation of ARGs in composting and their potential mechanisms. The dynamic variations of biotic factors, including bacterial community, mobile genetic elements (MGEs) and existence forms of ARGs, are the direct driving factors of the fate of ARGs during composting. However, most key abiotic indicators, including pH, moisture content, antibiotics and heavy metals, interfere with the richness of ARGs indirectly by influencing the succession of bacterial community and abundance of MGEs. The effect of temperature on ARGs depends on whether the ARGs are intracellular or extracellular, which should be paid more attention. The emergence of various controlling strategies renders the composting products safer. Four potential removal mechanisms of ARGs in different controlling strategies have been concluded, encompassing the attenuation of selective/co-selective pressure on ARGs, killing the potential host bacteria of ARGs, reshaping the structure of bacterial community and reducing the cell-to-cell contact of bacteria. With the effective control of ARGs, aerobic composting is suggested to be a sustainable and promising approach to treat animal manure.

Introduction

The propagation and prevalence of antibiotic resistance genes (ARGs) have become a major concern of the 21st century with the abuse of antibiotics (Pei et al., 2019). The ARGs and antibiotic resistant bacteria (ARB) have been frequently detected in different environmental compartments, such as rivers, soils, and even air (Ben et al., 2019; Huang et al., 2020). ARGs can be transferred to human pathogenic bacteria (HPB) via horizontal gene transfer (HGT) including conjugation, transformation and transduction (Allen et al., 2010; Huddleston, 2014). Antibiotic therapies could be ineffective once the ARGs enter human bodies via human pathogens (Karkman et al., 2016), posing potential adverse effects on global public health and ecological safety.

Animal manure has become important reservoirs of ARGs because of worldwide usage of antibiotics and heavy metals in concentrated animal husbandry, for therapy and growth-promoting purposes (Ji et al., 2012). Whereas, the annual production of livestock manure only in China has reached 3.8 billion tons (Guo et al., 2020). Animal manure is valuable renewable resource because of having the abundant organic matter. It is estimated that nearly a third of chemical fertilizer usage could be saved each year by converting the manure from pigs, cows and chickens into fertilizer (Zhou et al., 2019). If animal manure can be transformed into low-risk (even risk-free) organic fertilizer, it will be of great significance to improve land productivity and alleviate the global resource crisis. However, the occurrence of ARGs in animal manure needs to be considered seriously. For example, in fresh swine manure, absolute abundances (AAs) of ARGs have been reported up to 1011 - 1013 copies/g dry weight (Cao et al., 2020b; Sardar et al., 2021).

Aerobic composting, which can convert various organic materials into more stable and eco-friendly substances, is a promising method to reduce the ecological risk of multiple pollutants (Liao et al., 2019). Recent researches have confirmed the positive effect of aerobic composting on ARGs removal (Xie et al., 2019; Deng et al., 2020). The composition and succession of bacterial communities play a crucial role in eliminating the ARGs (Ben et al., 2017). Several studies have proposed that composting has different effects on ARGs which may increase the diversity and abundances of ARGs (Sharma et al., 2009; Qian et al., 2016b; Cheng et al., 2019). The complicated fate of ARGs depends on the diverse composition of raw materials and various operating conditions during composting (Baker-Austin et al., 2006; Qian et al., 2016a; Liao et al., 2018; Fan et al., 2020). However, during composting, the operating conditions and effects of external stresses on ARGs and their mechanisms behind the variations are still unclear. Whereas, the influence of controlling strategies on ARGs also need further investigation to safely reutilize the composting products of animal manure.

Nonetheless, only few review articles focused on the fate of ARGs and potential mechanisms behind controlling strategies. Actually, it is of little practical significance to simply review the change (increase/decrease) of ARGs but it is very necessary to explore the deep reasons behind variations of ARGs in order to get safer products. Thus, this review begins with the reasons that affect the fate of ARGs during composting, and discusses their specific mechanisms based on diverse influencing factors, aiming to provide a fundamental basis for the effective control of ARGs. The main contents of this review are as follows: 1) The diverse occurrence of ARGs in initial manure and its complicated fate in composting. 2) Biotic factors determine the fate of ARGs during composting. 3) Most key abiotic indicators affecting ARGs indirectly. 4) Potential mechanisms of controlling strategies on removal of ARGs.

Section snippets

Occurrence and fate of ARGs during composting

The ARGs in different animal manure composting have various abundance and diversity, as depicted in Fig. 1. Fig. 1(a) shows the distribution of relative abundances (RAs) of ARGs in initial manure composting. For example, the initial RAs of total ARGs in poultry manure composting materials ranged from 0.375 to 3.300 (median value at 1.546), while swine manure consists of 0.010 to 2.300 (median value at 0.833) and herbivore (e.g., cattle and sheep) manure range from 0.080 to 0.400 (median value

Biotic factors drive the fate of ARGs more directly during composting

In composting, biological factors play a decisive role in the variation of ARGs. Non-random co-occurrence of potential bacteria, MGEs, and ARGs is common during composting. Composition and succession of bacterial community, as well as the fate of MGEs, directly determine the occurrence and propagation ability of ARGs (Qian et al., 2016a; Chen et al., 2018; Lu et al., 2018; Qian et al., 2018; Guo et al., 2019a; Hu et al., 2019; Bao et al., 2020; Cao et al., 2020b; Wang et al., 2021). However, it

Most abiotic factors influence the fate of ARGs indirectly during composting

The dynamic variations of biotic factors, especially the bacterial community and MGEs, are the direct driving factors of the fate of ARGs during composting (Qian et al., 2016a; Lu et al., 2018; Song et al., 2020; Zhou et al., 2021; Gou et al., 2021). However, as shown in Fig. 3, most abiotic indicators interference with the abundance of ARGs indirectly by influencing succession of bacterial community and abundance of MGEs (Duan et al., 2019; Qian et al., 2019; Peng et al., 2020; Song et al.,

Potential ecological risks of ARGs during composting

As mentioned above, thermophilic and cooling phases have a strong shaping effect on the fate of ARGs in composting. Although most ARGs can be removed during the thermophilic period, the rebound of ARGs during the cooling period, possibly due to HGT, should not be underestimated. In the absence of effective control of HGT, the environmental health risk of ARGs in soil will increase when composting products are applied to soil.

Therefore, more attention should be paid to the risk assessment of

Controlling strategies on ARGs during composting

Considering the health risk of the reutilization of composting products, numerous studies have modified the composting processes via changing the basic conditions of composting and adding biological agents and abiotic additives in order to obtain safer products. Common controlling strategies of composting and influencing mechanisms on ARGs are shown in Table 3 and Fig. 4, respectively.

As it is shown in Table 3, thermophilic composting is effective for controlling ARGs (Qian et al., 2016a),

Conclusions and perspectives

Future recommendations derived from the present work are as follows: (1) When focusing on the removal efficacy of ARGs in composting, the differences between distinct raw materials should be clearly identified to investigate their specific mechanisms. (2) Multiple factors influencing the fate of ARGs are closely related to biotic factors, mainly including bacterial community and MGEs. (3) Most abiotic factors indirectly affect the ARGs in composting mainly by affecting the biological factors,

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This work was supported by the National Key Research & Development Program of China (2019YFC1906404) and National Research Foundation (NRF), Prime Minister's office, Singapore under its Campus for Research Excellence and Technological Enterprise (CREATE) program.

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