Transmission Routes of the Microbiome and Resistome from Manure to Soil and Lettuce

Sun, Yuepeng; Snow, Daniel D.; Walia, Harkamal; Xu, Lei

doi:10.1021/acs.est.1c02985

Cited by 52 publications

(34 citation statements)

References 53 publications

(113 reference statements)

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“…A growing concern about the application of untreated animal manure to agricultural soil is the possibility of contamination with pathogenic ARB and antibiotic resistance genes (ARGs), as animal manure is considered a significant reservoir of both enteric and pathogenic ARB and ARGs (Robins-Browne, 2005;Johnson et al, 2016). Previous studies that investigated the impact of animal manure on soil resistome demonstrated that fertilisation with animal manure resulted in the appearance or increased level and diversity of ARB and ARGs in soils (Jensen et al, 2013;Chen et al, 2016b;Fatoba et al, 2021;Sun et al, 2021). Jensen et al (2013) reported the appearance of E. coli in soil after the application of animal slurry to three Danish agricultural fields.…”

Section: Introductionmentioning

confidence: 99%

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Transmission of Antibiotic-Resistant Escherichia coli from Chicken Litter to Agricultural Soil

Fatoba

Amoako

Abia

et al. 2022

Front. Environ. Sci.

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A growing concern regarding the use of animal manure as fertilizer is the contamination of soil, plants, and the environment with a variety of antibiotic-resistant and pathogenic bacteria. This study quantified and characterized the antibiotic resistance profiles of Escherichia coli in soil before and after chicken litter application to determine the impact of manure on the soil resistome. Litter and soil samples were collected from a sugarcane field before and after litter application. E. coli was isolated and quantified using the Colilert®-18/Quanti-tray® 2000 and 10 randomly selected isolates from the positive wells of each Quanti-tray were putatively identified on eosin methylene blue agar. Real-time PCR was used to confirm the isolates by targeting the uidA gene. Antibiotic susceptibility test against 18 antibiotics was conducted using the disk diffusion method, and the multiple antibiotic resistance index was calculated. Soil amendment with chicken litter significantly increased the number of antibiotic-resistant E. coli in the soil. Among the 126 E. coli isolates purified from all the samples, 76% showed resistance to at least one antibiotic, of which 54.2% were multidrug-resistant (MDR). The highest percentage resistance was to tetracycline (78.1%), with the least percentage resistance (3.1%) to imipenem, tigecycline, and gentamicin. The isolates also showed resistance to chloramphenicol (63.5%), ampicillin (58.3%), trimethoprim-sulfamethoxazole (39.6%), cefotaxime (30.2%), ceftriaxone (26.0%), cephalexin (20.8%), cefepime (11.5%), amoxicillin-clavulanic acid (11.5%), cefoxitin (10.4%), Nalidixic acid (9.4%), amikacin (6.3%), and ciprofloxacin (4.2%). Of the 54.2% (52/96) MDR, the highest number was isolated from the litter-amended soil (61.5%) and the least isolates from soil samples collected before litter application (1.9%). The relatively higher mean MAR index of the litter-amended soil (0.14), compared to the soil before the amendment (0.04), suggests soil pollution with antibiotic-resistant E. coli from sources of high antibiotic use. E. coli could only be detected in the soil up to 42 days following manure application, making it a suitable short-term indicator of antibiotic resistance contamination. Notwithstanding its relatively short detectability/survival, the application of chicken litter appeared to transfer antibiotic-resistant E. coli to the soil, enhancing the soil resistome and highlighting the consequences of such agricultural practices on public health.

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Section: Introductionmentioning

confidence: 99%

“…in agricultural soil following chicken litter application. Another study from the United States showed that manure application significantly increased the diversity of surface soil microbiome and resistome and also introduced tetracycline and sulphonamide resistance genes to the soil (Sun et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

Transmission of Antibiotic-Resistant Escherichia coli from Chicken Litter to Agricultural Soil

Fatoba

Amoako

Abia

et al. 2022

Front. Environ. Sci.

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“…Microorganisms in the soil play significant roles in plant development(Sheng et al, 2021; Sun et al, 2021; Warmink and van Elsas, 2009; Zhao et al, 2014). They are an essential component of soil ecology and serve as an important mechanism for soil regeneration.…”

Section: Discussionmentioning

confidence: 99%

“…Morphological variations in plants may result from growth in soil with different fertilizer concentrations (Sun et al 2021).…”

Section: Nitrogen Influenced Plant Growth By Hitchhikingmentioning

confidence: 99%

The synergistic effects of plants and nitrogen on microbial hitchhiking

Liu

Wang

Xia

et al. 2022

Preprint

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Microbial hitchhiking demonstrates that some nonmotile microbes utilize trans-species motility to traverse their environment; however, whether driving forces, such as plants and nitrogen, affect microbial hitchhiking is not clear. In our study, we explored the effects of plants and nitrogen fertilizer on Bacillus- hitchhiking by setting filter membranes and different nitrogen fertilizer concentration gradients. In the experimental treatment, we added a filter membrane to the soil to prevent hitchhiking. In the absence of plants, nitrogen alone had little influence on motile bacteria and hitchhiking. However, Bacillus contents were significantly impacted by the nitrogen concentration when the plants were rooted, leading to a great variation in cell motility function according to the functional analysis in the soil microbial community. After applying the filter membrane, there were no significant differences in Bacillus contents, microbial community structure or cell motility functional abundance, which illustrated that hitchhiking impacted the microbial community. Our analysis of co-occurrence between bulk soil motile bacteria (Bacillus) and rhizosphere bacteria also confirmed this. The correlation between bulk soil motile bacteria and the rhizosphere microbial community was strong in the groups with suitable nitrogen concentrations without filter membranes and was weak at all nitrogen levels in the no-membrane treatments. Thus, we concluded that plants and different nitrogen doses synergistically altered the soil microbiome by hitchhiking, whose effect depends on nitrogen.

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“…Recently, it was reported that microbes could be transmitted not only from plants to animals, but also from animals to plants. Lettuce grown in soil containing cattle manure, acquired in their leaves manure-borne microbes that include antibiotic resistance genes, which may assist in protection against infection [215]. Moreover, antibiotic resistance genes, acquired from poultry litter was present in the roots of lettuce [216].…”

Section: Horizontal Transmissionmentioning

confidence: 99%

Reconstitution and Transmission of Gut Microbiomes and Their Genes between Generations

Rosenberg

Zilber‐Rosenberg

2021

Microorganisms

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Microbiomes are transmitted between generations by a variety of different vertical and/or horizontal modes, including vegetative reproduction (vertical), via female germ cells (vertical), coprophagy and regurgitation (vertical and horizontal), physical contact starting at birth (vertical and horizontal), breast-feeding (vertical), and via the environment (horizontal). Analyses of vertical transmission can result in false negatives (failure to detect rare microbes) and false positives (strain variants). In humans, offspring receive most of their initial gut microbiota vertically from mothers during birth, via breast-feeding and close contact. Horizontal transmission is common in marine organisms and involves selectivity in determining which environmental microbes can colonize the organism’s microbiome. The following arguments are put forth concerning accurate microbial transmission: First, the transmission may be of functions, not necessarily of species; second, horizontal transmission may be as accurate as vertical transmission; third, detection techniques may fail to detect rare microbes; lastly, microbiomes develop and reach maturity with their hosts. In spite of the great variation in means of transmission discussed in this paper, microbiomes and their functions are transferred from one generation of holobionts to the next with fidelity. This provides a strong basis for each holobiont to be considered a unique biological entity and a level of selection in evolution, largely maintaining the uniqueness of the entity and conserving the species from one generation to the next.

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Transmission Routes of the Microbiome and Resistome from Manure to Soil and Lettuce

Cited by 52 publications

References 53 publications

Transmission of Antibiotic-Resistant Escherichia coli from Chicken Litter to Agricultural Soil

Transmission of Antibiotic-Resistant Escherichia coli from Chicken Litter to Agricultural Soil

The synergistic effects of plants and nitrogen on microbial hitchhiking

Reconstitution and Transmission of Gut Microbiomes and Their Genes between Generations

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