|
|
Antibiotic resistome mostly relates to bacterial taxonomy along a suburban transmission chain |
Ziyan Qin1, Qun Gao1(), Qiang Dong2, Joy D. Van Nostrand3, Qi Qi1, Yifan Su1, Suo Liu1, Tianjiao Dai1, Jingmin Cheng1, Jizhong Zhou3,4,5, Yunfeng Yang1() |
1. State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing 100084, China 2. Institute of Chemical Defense, Beijing 102205, China 3. Institute for Environmental Genomics, and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019, USA 4. School of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK 73019, USA 5. Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA |
|
|
Abstract • The α-diversities of resistome were lower in manure and compost than in soils. • There were significant correlations between the resistome and bacterial taxonomy. • Bacterial taxonomy was the highest in explaining resistome variances. Antibiotic resistance genes comprising antibiotic resistome are of great concern due to their increase in the environment. Recent evidence of shared resistomes between soils and animal husbandry has imposed potential risks to human health. However, the correlation between a given community’s resistome and bacterial taxonomic composition is controversial. Here, a transmission chain of resistomes from swine manure to compost and compost-amended soil were analyzed in five suburban areas of Beijing, China, with unamended agricultural soils as control soils. Antibiotic resistomes and bacterial taxonomic compositions were distinct between (I) manure and compost; and (II) compost-amended and control soils. In manure, compost, and compost-amended soils, the β-diversity of the resistome and bacterial taxonomic composition was significantly correlated, while no correlation was detected in control soils. Bacterial taxonomic composition explained 36.0% of total variations of the resistome composition, much higher than environmental factors. Together, those results demonstrated that antibiotic resistome was closely related to bacterial taxonomic composition along the suburban transmission chain.
|
Keywords
Antibiotic resistance genes
Resistome
Bacterial taxonomy
Transmission chain
|
Corresponding Author(s):
Qun Gao,Yunfeng Yang
|
Issue Date: 13 July 2021
|
|
1 |
R E Alcock, A Sweetman, K C Jones (1999). Assessment of organic contanhnant fate in waste water treatment plants I: Selected compounds and physicochemical properties. Chemosphere, 38(10): 2247–2262
https://doi.org/10.1016/S0045-6535(98)00444-5
|
2 |
M J Anderson (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26(1): 32–46
|
3 |
F Caméléna, B Pilmis, B Mollo, A Hadj, A Le Monnier, A Mizrahi (2016). Infections caused by Tissierella praeacuta: A report of two cases and literature review. Anaerobe, 40: 15–17
https://doi.org/10.1016/j.anaerobe.2016.04.015
|
4 |
R Cao, J Wang, W Ben, Z Qiang (2020). The profile of antibiotic resistance genes in pig manure composting shaped by composting stage: Mesophilic-thermophilic and cooling-maturation stages. Chemosphere, 250: 126181
https://doi.org/10.1016/j.chemosphere.2020.126181
|
5 |
Q L Chen, X L An, B X Zheng, M Gillings, J Peñuelas, L Cui, J Q Su, Y G Zhu (2019). Loss of soil microbial diversity exacerbates spread of antibiotic resistance. Soil Ecology Letters, 1(1–2): 3–13
https://doi.org/10.1007/s42832-019-0011-0
|
6 |
D de Oliveira-Garcia, M Dall’agnol, M Rosales, A C Azzuz, M B Martinez, J A Giron (2002). Characterization of flagella produced by clinical strains of Stenotrophomonas maltophilia. Emerging Infectious Diseases, 8(9): 918–923
https://doi.org/10.3201/eid0809.010535
|
7 |
T Fernandes, I Vaz-Moreira, C M Manaia (2019). Neighbor urban wastewater treatment plants display distinct profiles of bacterial community and antibiotic resistance genes. Environmental Science and Pollution Research International, 26(11): 11269–11278
https://doi.org/10.1007/s11356-019-04546-y
|
8 |
K J Forsberg, S Patel, M K Gibson, C L Lauber, R Knight, N Fierer, G Dantas (2014). Bacterial phylogeny structures soil resistomes across habitats. Nature, 509(7502): 612–616
https://doi.org/10.1038/nature13377
|
9 |
K J Forsberg, A Reyes, B Wang, E M Selleck, M O Sommer, G Dantas (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Science, 337(6098): 1107–1111
https://doi.org/10.1126/science.1220761
|
10 |
Q Gao, Q Dong, L Wu, Y Yang, L Hale, Z Qin, C Xie, Q Zhang, J D Van Nostrand, J Zhou (2020). Environmental antibiotics drives the genetic functions of resistome dynamics. Environment International, 135: 105398
https://doi.org/10.1016/j.envint.2019.105398
|
11 |
S Ghosh, T M LaPara (2007). The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME Journal, 1(3): 191–203
https://doi.org/10.1038/ismej.2007.31
|
12 |
S Ghosh, M Sadowsky, M Roberts, J Gralnick, T LaPara (2009). Sphingobacterium sp. strain PM2‐P1‐29 harbours a functional tet (X) gene encoding for the degradation of tetracycline. Journal of Applied Microbiology, 106(4): 1336–1342
https://doi.org/10.1111/j.1365-2672.2008.04101.x
|
13 |
M R Gillings, H W Stokes (2012). Are humans increasing bacterial evolvability? Trends in Ecology & Evolution, 27(6): 346–352
https://doi.org/10.1016/j.tree.2012.02.006
|
14 |
H J Hong, M I Hutchings, M J Buttner (2008).Vancomycin resistance VanS/VanR two-component systems. In: Utsumi R, ed. Bacterial Signal Transduction: Networks and Drug Targets. New York: Springer New York, 200–213
|
15 |
B Huerta, E Marti, M Gros, P Lopez, M Pompeo, J Armengol, D Barcelo, J L Balcazar, S Rodriguez-Mozaz, R Marce (2013). Exploring the links between antibiotic occurrence, antibiotic resistance, and bacterial communities in water supply reservoirs. Science of the Total Environment, 456–457: 161–170
https://doi.org/10.1016/j.scitotenv.2013.03.071
|
16 |
S Jechalke, H Heuer, J Siemens, W Amelung, K Smalla (2014). Fate and effects of veterinary antibiotics in soil. Trends in Microbiology, 22(9): 536–545
https://doi.org/10.1016/j.tim.2014.05.005
|
17 |
S Jechalke, C Kopmann, I Rosendahl, J Groeneweg, V Weichelt, E Krogerrecklenfort, N Brandes, M Nordwig, G C Ding, J Siemens, H Heuer, K Smalla (2013). Increased abundance and transferability of resistance genes after field application of manure from sulfadiazine-treated pigs. Applied and Environmental Microbiology, 79(5): 1704–1711
https://doi.org/10.1128/AEM.03172-12
|
18 |
Q K Ji C H , Zhang D , Li (2020). Influences and mechanisms of nanofullerene on the horizontal transfer of plasmid-encoded antibiotic resistance genes between E. coli strains. Frontiers of Environmental Science & Engineering, 14(6): 108
|
19 |
U Klümper, L Riber, A Dechesne, A Sannazzarro, L H Hansen, S J Sorensen, B F Smets (2015). Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community. ISME Journal, 9(4): 934–945
https://doi.org/10.1038/ismej.2014.191
|
20 |
T Kusakizako, H Miyauchi, R Ishitani, O Nureki (2020). Structural biology of the multidrug and toxic compound extrusion superfamily transporters. Biochimica et Biophysica Acta, 1862(12): 183154
https://doi.org/10.1016/j.bbamem.2019.183154
|
21 |
S O Leclercq, C Wang, Z Sui, H Wu, B Zhu, Y Deng, J Feng (2016). A multiplayer game: Species of Clostridium, Acinetobacter, and Pseudomonas are responsible for the persistence of antibiotic resistance genes in manure-treated soils. Environmental Microbiology, 18(10): 3494–3508
https://doi.org/10.1111/1462-2920.13337
|
22 |
P Legendre, L Legendre (2012). Numerical Ecology. Amsterdam,AE: Elsevier
|
23 |
H Liao, V P Friman, S Geisen, Q Zhao, P Cui, X Lu, Z Chen, Z Yu, S Zhou (2019). Horizontal gene transfer and shifts in linked bacterial community composition are associated with maintenance of antibiotic resistance genes during food waste composting. Science of the Total Environment, 660: 841–850
https://doi.org/10.1016/j.scitotenv.2018.12.353
|
24 |
J W Lichstein (2007). Multiple regression on distance matrices: a multivariate spatial analysis tool. Plant Ecology, 188(2): 117–131
https://doi.org/10.1007/s11258-006-9126-3
|
25 |
T Liu, S K Awasthi, Y Duan, Z Zhang, M K Awasthi (2020). Effect of fine coal gasification slag on improvement of bacterial diversity community during the pig manure composting. Bioresource Technology, 304: 123024
https://doi.org/10.1016/j.biortech.2020.123024
|
26 |
T Looft, T A Johnson, H K Allen, D O Bayles, D P Alt, R D Stedtfeld, W J Sul, T M Stedtfeld, B Chai, J R Cole, S A Hashsham, J M Tiedje, T B Stanton (2012). In-feed antibiotic effects on the swine intestinal microbiome. Proceedings of the National Academy of Sciences of the United States of America, 109(5): 1691–1696
https://doi.org/10.1073/pnas.1120238109
|
27 |
X Ma, Q Zhang, M Zheng, Y Gao, T Yuan, L Hale, J D Van Nostrand, J Zhou, S Wan, Y Yang (2019). Microbial functional traits are sensitive indicators of mild disturbance by lamb grazing. ISME Journal, 13(5): 1370–1373
https://doi.org/10.1038/s41396-019-0354-7
|
28 |
T Magoč, S L Salzberg (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics (Oxford, England), 27(21): 2957–2963
https://doi.org/10.1093/bioinformatics/btr507
|
29 |
R N Mannanov, R K Sattarova (2001). Antibiotics produced by Bacillus bacteria. Chemistry of Natural Compounds, 37(2): 117–123
https://doi.org/10.1023/A:1012314516354
|
30 |
B M Marshall, S B Levy (2011). Food animals and antimicrobials: impacts on human health. Clinical Microbiology Reviews, 24(4): 718–733
https://doi.org/10.1128/CMR.00002-11
|
31 |
E Martinez, S Djordjevic, H Stokes, P R Chowdhury (2013).Lateral Gene Transfer in Evolution. RamatAviv: Springer, 79–103
|
32 |
M Mendez, I H Huang, K Ohtani, R Grau, T Shimizu, M R Sarker (2008). Carbon catabolite repression of type IV pilus-dependent gliding motility in the anaerobic pathogen Clostridium perfringens. Journal of Bacteriology, 190(1): 48–60
https://doi.org/10.1128/JB.01407-07
|
33 |
V Neubauer, E Humer, E Mann, I Kroger, N Reisinger, M Wagner, Q Zebeli, R M Petri (2019). Effects of clay mineral supplementation on particle-associated and epimural microbiota, and gene expression in the rumen of cows fed high-concentrate diet. Anaerobe, 59: 38–48
https://doi.org/10.1016/j.anaerobe.2019.05.003
|
34 |
S S Pao, I T Paulsen, M H Saier Jr (1998). Major facilitator superfamily. Microbiology and Molecular Biology Reviews, 62(1): 1–34
https://doi.org/10.1128/MMBR.62.1.1-34.1998
|
35 |
F Peng, Y Guo, A Isabwe, H Chen, Y Wang, Y Zhang, Z Zhu, J Yang (2020). Urbanization drives riverine bacterial antibiotic resistome more than taxonomic community at watershed scale. Environment International, 137: 105524
https://doi.org/10.1016/j.envint.2020.105524
|
36 |
A Pruden, M Arabi, H N Storteboom (2012). Correlation between upstream human activities and riverine antibiotic resistance genes. Environmental Science & Technology, 46(21): 11541–11549
https://doi.org/10.1021/es302657r
|
37 |
M Qiao, W Chen, J Su, B Zhang, C Zhang (2012). Fate of tetracyclines in swine manure of three selected swine farms in China. Journal of Environmental Sciences-China, 24(6): 1047–1052
https://doi.org/10.1016/S1001-0742(11)60890-5
|
38 |
M Schweizer, G V Bloemberg, C Graf, A L Falkowski, P Ochsner, P Graber, S Urffer, D Goldenberger, V Hinic, S Graf, P E Tarr (2016). Chronic osteomyelitis due to Tissierella carlieri: First case. Open Forum Infectious Diseases, 3(1): ofw012
https://doi.org/10.1093/ofid/ofw012
|
39 |
J F Jr Siqueira, I N Rôças (2006).Catonella morbi and Granulicatella adiacens: new species in endodontic infections. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics, 102(2): 259–264
https://doi.org/10.1016/j.tripleo.2005.09.021
|
40 |
J F Jr Siqueira, I N Rôças (2008). Update on endodontic microbiology: candidate pathogens and patterns of colonisation. Endodontic Practice Today, 2(1): 7–20
|
41 |
C S Smillie, M B Smith, J Friedman, O X Cordero, L A David, E J Alm (2011). Ecology drives a global network of gene exchange connecting the human microbiome. Nature, 480(7376): 241–244
https://doi.org/10.1038/nature10571
|
42 |
H W Stokes, M R Gillings (2011). Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS Microbiology Reviews, 35(5): 790–819
https://doi.org/10.1111/j.1574-6976.2011.00273.x
|
43 |
J Q Su, X L An, B Li, Q L Chen, M R Gillings, H Chen, T Zhang, Y G Zhu (2017). Metagenomics of urban sewage identifies an extensively shared antibiotic resistome in China. Microbiome, 5(1): 1–15
https://doi.org/10.1186/s40168-017-0298-y
|
44 |
W Tao, X X Zhang, F Zhao, K Huang, H Ma, Z Wang, L Ye, H Ren (2016). High levels of antibiotic resistance genes and their correlations with bacterial community and mobile genetic elements in pharmaceutical wastewater treatment bioreactors. PLoS One, 11(6): e0156854
https://doi.org/10.1371/journal.pone.0156854
|
45 |
K J Towner (2009). Acinetobacter: an old friend, but a new enemy. Journal of Hospital Infection, 73(4): 355–363
https://doi.org/10.1016/j.jhin.2009.03.032
|
46 |
N Udikovic-Kolic, F Wichmann, N A Broderick, J Handelsman (2014). Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proceedings of the National Academy of Sciences of the United States of America, 111(42): 15202–15207
https://doi.org/10.1073/pnas.1409836111
|
47 |
Q Wang, G M Garrity, J M Tiedje, J R Cole (2007). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16): 5261–5267
https://doi.org/10.1128/AEM.00062-07
|
48 |
L Wu, Y Yang, S Chen, Z Jason Shi, M Zhao, Z Zhu, S Yang, Y Qu, Q Ma, Z He, J Zhou, Q He (2017). Microbial functional trait of rRNA operon copy numbers increases with organic levels in anaerobic digesters. ISME Journal, 11(12): 2874–2878
https://doi.org/10.1038/ismej.2017.135
|
49 |
N Wu, W Y Zhang, S Y Xie, M Zeng, H X Liu, J H Yang, X Y Liu, F Yang (2020). Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China. Frontiers of Environmental Science & Engineering, 14(1): 1
|
50 |
N Yan (2013). Structural advances for the major facilitator superfamily (MFS) transporters. Trends in Biochemical Sciences, 38(3): 151–159
https://doi.org/10.1016/j.tibs.2013.01.003
|
51 |
H Zhang, H He, S Chen, T Huang, K Lu, Z Zhang, R Wang, X Zhang, H Li (2019). Abundance of antibiotic resistance genes and their association with bacterial communities in activated sludge of wastewater treatment plants: Geographical distribution and network analysis. Journal of Environmental Sciences-China, 82: 24–38
https://doi.org/10.1016/j.jes.2019.02.023
|
52 |
J Zhang, Q Gao, Q Zhang, T Wang, H Yue, L Wu, J Shi, Z Qin, J Zhou, J Zuo, Y Yang (2017). Bacteriophage–prokaryote dynamics and interaction within anaerobic digestion processes across time and space. Microbiome, 5(1): 1–10
https://doi.org/10.1186/s40168-017-0272-8
|
53 |
M Zhang, L Y He, Y S Liu, J L Zhao, J N Zhang, J Chen, Q Q Zhang, G G Ying (2020). Variation of antibiotic resistome during commercial livestock manure composting. Environment International, 136: 105458
https://doi.org/10.1016/j.envint.2020.105458
|
54 |
T Zhang, M Zhang, X Zhang, H H Fang (2009). Tetracycline resistance genes and tetracycline resistant lactose-fermenting Enterobacteriaceae in activated sludge of sewage treatment plants. Environmental Science & Technology, 43(10): 3455–3460
https://doi.org/10.1021/es803309m
|
55 |
D Zhu, H T Wang, F Zheng, X R Yang, P Christie, Y G Zhu (2019). Collembolans accelerate the dispersal of antibiotic resistance genes in the soil ecosystem. Soil Ecology Letters, 1(1–2): 14–21
https://doi.org/10.1007/s42832-019-0002-1
|
56 |
Y G Zhu, T A Johnson, J Q Su, M Qiao, G X Guo, R D Stedtfeld, S A Hashsham, J M Tiedje (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proceedings of the National Academy of Sciences of the United States of America, 110(9): 3435–3440
https://doi.org/10.1073/pnas.1222743110
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|