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Song et al. Environ Sci Eur (2021) 33:91 https://doi.org/10.1186/s12302-021-00535-6 RESEARCH Open Access Distribution of antibiotic-resistant bacteria in aerobic composting of swine manure with diferent antibiotics Tingting Song1,2, Hongna Li1, Binxu Li1, Jiaxun Yang1, Muhammad Fahad Sardar1, Mengmeng Yan1, Luyao Li1, Yunlong Tian1, Sha Xue2,3* and Changxiong Zhu1* Abstract Background: Livestock manure is an important reservoir of antibiotic-resistant bacteria (ARB) and antibiotic- resistance genes (ARGs). The bacterial community structure and diversity are usually studied using high-throughput sequencing that cannot provide direct evidence for ARB changes. Thus, little is known about the distribution of ARB, especially in the presence of diferent antibiotics in composting process. In this study, the fate of ARB was investigated in aerobic composting of swine manure, using chlortetracycline, sulfamethoxazole, lincomycin, and ciprofoxacin as typical antibiotics. The abundance and species of ARB were analyzed systematically to evaluate their ecological risk at diferent stages of composting. Results: The absolute abundance of total ARB decreased, while the relative abundance increased on day 2. The rela- tive abundance of lincomycin-resistant bacteria was higher than other ARBs during the whole composting process. The absolute abundance of four ARBs was 9.42 ­106–2.51 ­102 CFU/g (lincomycin- > chlortetracycline- > sulfameth- oxazole- > ciprofoxacin- > multiple antibiotic-resistant× bacteria),× and they were not completely inactivated at the end of composting. Antibiotics led to a partial proliferation of ARBs including Corynebacterium, Sporosarcina, Solibacillus, and Acinetobacter. Especially, Corynebacterium, a pathogenic genus, was observed in chlortetracycline and lincomycin treatments. Conclusion: Among the antibiotics studied, lincomycin showed the highest ecological risk, due to it expanded the range of lincomycin-resistant bacteria at the phyla level (Firmicutes, Actinobacteria, and Proteobacteria). The principal co-ordinates analysis indicated that the bacterial community structure was primarily associated with the compost- ing stages rather than antibiotic types. Possible potential hosts and the related to the decrease of ARGs abundance were indicated based on the network analysis. The decrease of culturable Proteobacteria and the increase of cultur- able Firmicutes (Solibacillus, Bacillus) partially explained the high degradation rate of various ARGs with the progress of composting in this study. These results provided important information for the control of antibiotic resistance in composting. Keywords: Antibiotic-resistant bacteria, Lincomycin, Aerobic composting, Ecological risk Background *Correspondence: [email protected]; [email protected] Antibiotics have been widely utilized in animal hus- 1 Institute of Environment and Sustainable Development in Agriculture, Chinese Academy of Agricultural Sciences, Beijing 100081, People’s bandry, and their residual concentrations were reported Republic of China in the μg/kg ~ mg/kg level in livestock manure [1–3]. In 2 College of Forestry, Northwest A&F University, Yangling, Shaanxi 712100, addition, inadequate assimilation in the animal body has People’s Republic of China Full list of author information is available at the end of the article led to increase residual antibiotics in the manure, which © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Song et al. Environ Sci Eur (2021) 33:91 Page 2 of 13 could promote selection for antibiotic-resistant bacteria genes, was also observed during composting of cattle (ARB) and antibiotic-resistance genes (ARGs) and mak- manure [13, 14]. ARBs are the source and hosts for ARGs ing them a major reservoir of antibiotic resistance [4, 5]. [4]. Most of the previous studies only analyzed the abun- In recent decades, several techniques have been adopted dance of ARB and did not focus on the evolution of com- to determine the variations of microbial structure. Tra- munity structure. Besides, it is even little known that the ditional microbiological methods are essential and indis- infuence of antibiotic types on the abundance and com- pensable as a means to culture, and have continuously munity structure of ARB, as well as the potential relation- been used to successfully isolate various microbes [6]. ship of ARB and ARGs. In this study, chlortetracycline Te survival ability of bacteria in the presence of antibi- (CTC), sulfamethoxazole (SMX), ciprofoxacin (CIP), and otics is the only way to evaluate whether they are anti- LIN were selected according to their types and residual biotic-resistant or not, with the minimum inhibitory concentrations in our previous study [12]. Tese four concentration quantifed by agar dilution or broth micro- antibiotics are frequently used in veterinary and human dilution assays [7]. Salmonella and Campylobacter, path- treatments worldwide, and have been detected in difer- ogenic genera, have been detected at 105 colony-forming ent environmental matrices [15]. Te objectives of this units (CFU/mL) and most of which were antibiotic resist- research are to determine how (1) diferent antibiotics ance in the pig farm lagoons [8]. Numerous antibiotic- afect ARB abundance, (2) composting stage afects ARB resistant human pathogenic genera, Escherichia coli, communities, and (3) what relationships exist between Alcaligenes faecalis, and Enterococcus, have been found in ARB and ARGs to better mitigate public health risk. Tis chicken manure [9]. Extensive use of antibiotics in animal study provides a better understanding on the fate of ARB husbandry signifcantly increased ARB and ARGs in live- abundances and community structure, and ARGs in aer- stock settings [10]. Tis would lead to deleterious impli- obic composting. cations on human health and environmental quality [5]. Consequently, it is particularly important to reduce the spread and difusion of ARB and ARGs. Materials and methods Microorganisms are essential for composting, and the Composting and sampling procedures compositions of these microbial communities are altered Te detailed experimental design was the same as in our during this process. For example, lincomycin (LIN) resi- previous article [12]. Briefy, the treatment without added dues promoted the abundance of Firmicutes, Actinobac- antibiotic was used as the control (CK). Composting was teria, Proteobacteria, Chlorofexi, and Bacteroidetes in performed in rectangular foam boxes (55 × 45 × 45 cm) composting [2]. Previous studies found that the propor- with 2 × 2 cm diameter holes spaced 15 cm apart in all tion of Chlorofexi was higher than other phyla, and the 4 walls to allow facilitate ventilation. Te basic physical composting process also resulted in increases of Bacte- and chemical properties of the composting materials are roidetes abundance. Te increase paralleled the antibi- shown in Additional fle 1: Table S1. Composting materi- otic concentration, indicating that Bacteroidetes were als were composed of 14.28 kg pig manure:straw:coconut tolerant to high levels of tetracycline [1, 11, 12]. Bacterial shell powder (6.67:4.94:2.67) with the C:N ratio of 30:1. community structure and diversity have been reported Moisture content was set at 65%. Te residual concen- using high-throughput sequencing. However, there is a trations of various antibiotics varied, but 50 mg/kg was lack of research on ARB community structure. Besides, selected as a standardized antibiotic concentration to this type of metagenomic sequencing data cannot pro- ensure study comparability. vide direct evidence for ARB changes [7]. Even culturable CTC, SMX, CIP and LIN obtained from Beijing DHLH bacteria also accounted for a low proportion of the total Biotechnology Co. Ltd. China. CTC and LIN were mixed bacteria; the traditional pure culture method is the most by methanol; SMX and CIP were dissolved in hydrochlo- direct method to understand ARB at present. Terefore, ric acid. Treatments were named as T0 (CK), T1 (CTC), it is very meaningful that the development of antibiotic T2 (SMX), T3 (LIN), T4 (CIP) and T5 (the four mixed resistance of specifc bacteria during composting should antibiotics). All treatments were replicated for three be monitored dynamically and analyzed comprehensively times. Te boxes were set in a row and ventilated for the in combination with the traditional pure cultures. duration of the 35-day experiment. Samples were col- Aerobic composting can efectively remove ARB from lected on days 2, 7, 14, 21, 28 and 35, and at the top, mid- livestock manure. Previous studies concluded that cul- dle and bottom of the reactor, then combined and mixed. tured bacteria resistant to tetracycline and
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