Antibiotic resistome mostly relates to bacterial taxonomy along a suburban transmission chain

Highlights

• 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.

Abstract

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.

Graphical abstract

Keywords

Antibiotic resistance genes / Resistome / Bacterial taxonomy / Transmission chain

References

[1] Alcock R E, Sweetman A, Jones K C (1999). Assessment of organic contanhnant fate in waste water treatment plants I: Selected compounds and physicochemical properties. Chemosphere, 38(10): 2247–2262

[2] Anderson M J (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26(1): 32–46

[3] Caméléna F, Pilmis B, Mollo B, Hadj A, Le Monnier A, Mizrahi A (2016). Infections caused by Tissierella praeacuta: A report of two cases and literature review. Anaerobe, 40: 15–17

[4] Cao R, Wang J, Ben W, Qiang Z (2020). The profile of antibiotic resistance genes in pig manure composting shaped by composting stage: Mesophilic-thermophilic and cooling-maturation stages. Chemosphere, 250: 126181

[5] Chen Q L, An X L, Zheng B X, Gillings M, Peñuelas J, Cui L, Su J Q, Zhu Y G (2019). Loss of soil microbial diversity exacerbates spread of antibiotic resistance. Soil Ecology Letters, 1(1–2): 3–13

[6] de Oliveira-Garcia D, Dall’agnol M, Rosales M, Azzuz A C, Martinez M B, Giron J A (2002). Characterization of flagella produced by clinical strains of Stenotrophomonas maltophilia. Emerging Infectious Diseases, 8(9): 918–923

[7] Fernandes T, Vaz-Moreira I, Manaia C M (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

[8] Forsberg K J, Patel S, Gibson M K, Lauber C L, Knight R, Fierer N, Dantas G (2014). Bacterial phylogeny structures soil resistomes across habitats. Nature, 509(7502): 612–616

[9] Forsberg K J, Reyes A, Wang B, Selleck E M, Sommer M O, Dantas G (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Science, 337(6098): 1107–1111

[10] Gao Q, Dong Q, Wu L, Yang Y, Hale L, Qin Z, Xie C, Zhang Q, Van Nostrand J D, Zhou J (2020). Environmental antibiotics drives the genetic functions of resistome dynamics. Environment International, 135: 105398

[11] Ghosh S, LaPara T M (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

[12] Ghosh S, Sadowsky M, Roberts M, Gralnick J, LaPara T (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

[13] Gillings M R, Stokes H W (2012). Are humans increasing bacterial evolvability? Trends in Ecology & Evolution, 27(6): 346–352

[14] Hong H J, Hutchings M I, Buttner M J (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] Huerta B, Marti E, Gros M, Lopez P, Pompeo M, Armengol J, Barcelo D, Balcazar J L, Rodriguez-Mozaz S, Marce R (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

[16] Jechalke S, Heuer H, Siemens J, Amelung W, Smalla K (2014). Fate and effects of veterinary antibiotics in soil. Trends in Microbiology, 22(9): 536–545

[17] Jechalke S, Kopmann C, Rosendahl I, Groeneweg J, Weichelt V, Krogerrecklenfort E, Brandes N, Nordwig M, Ding G C, Siemens J, Heuer H, Smalla K (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

[18] Ji Q K, Zhang C H, Li D (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] Klümper U, Riber L, Dechesne A, Sannazzarro A, Hansen L H, Sorensen S J, Smets B F (2015). Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community. ISME Journal, 9(4): 934–945

[20] Kusakizako T, Miyauchi H, Ishitani R, Nureki O (2020). Structural biology of the multidrug and toxic compound extrusion superfamily transporters. Biochimica et Biophysica Acta, 1862(12): 183154

[21] Leclercq S O, Wang C, Sui Z, Wu H, Zhu B, Deng Y, Feng J (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

[22] Legendre P, Legendre L (2012). Numerical Ecology. Amsterdam,AE: Elsevier

[23] Liao H, Friman V P, Geisen S, Zhao Q, Cui P, Lu X, Chen Z, Yu Z, Zhou S (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

[24] Lichstein J W (2007). Multiple regression on distance matrices: a multivariate spatial analysis tool. Plant Ecology, 188(2): 117–131

[25] Liu T, Awasthi S K, Duan Y, Zhang Z, Awasthi M K (2020). Effect of fine coal gasification slag on improvement of bacterial diversity community during the pig manure composting. Bioresource Technology, 304: 123024

[26] Looft T, Johnson T A, Allen H K, Bayles D O, Alt D P, Stedtfeld R D, Sul W J, Stedtfeld T M, Chai B, Cole J R, Hashsham S A, Tiedje J M, Stanton T B (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

[27] Ma X, Zhang Q, Zheng M, Gao Y, Yuan T, Hale L, Van Nostrand J D, Zhou J, Wan S, Yang Y (2019). Microbial functional traits are sensitive indicators of mild disturbance by lamb grazing. ISME Journal, 13(5): 1370–1373

[28] Magoč T, Salzberg S L (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics (Oxford, England), 27(21): 2957–2963

[29] Mannanov R N, Sattarova R K (2001). Antibiotics produced by Bacillus bacteria. Chemistry of Natural Compounds, 37(2): 117–123

[30] Marshall B M, Levy S B (2011). Food animals and antimicrobials: impacts on human health. Clinical Microbiology Reviews, 24(4): 718–733

[31] Martinez E, Djordjevic S, Stokes H, Chowdhury P R (2013).Lateral Gene Transfer in Evolution. RamatAviv: Springer, 79–103

[32] Mendez M, Huang I H, Ohtani K, Grau R, Shimizu T, Sarker M R (2008). Carbon catabolite repression of type IV pilus-dependent gliding motility in the anaerobic pathogen Clostridium perfringens. Journal of Bacteriology, 190(1): 48–60

[33] Neubauer V, Humer E, Mann E, Kroger I, Reisinger N, Wagner M, Zebeli Q, Petri R M (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

[34] Pao S S, Paulsen I T, Saier M H Jr (1998). Major facilitator superfamily. Microbiology and Molecular Biology Reviews, 62(1): 1–34

[35] Peng F, Guo Y, Isabwe A, Chen H, Wang Y, Zhang Y, Zhu Z, Yang J (2020). Urbanization drives riverine bacterial antibiotic resistome more than taxonomic community at watershed scale. Environment International, 137: 105524

[36] Pruden A, Arabi M, Storteboom H N (2012). Correlation between upstream human activities and riverine antibiotic resistance genes. Environmental Science & Technology, 46(21): 11541–11549

[37] Qiao M, Chen W, Su J, Zhang B, Zhang C (2012). Fate of tetracyclines in swine manure of three selected swine farms in China. Journal of Environmental Sciences-China, 24(6): 1047–1052

[38] Schweizer M, Bloemberg G V, Graf C, Falkowski A L, Ochsner P, Graber P, Urffer S, Goldenberger D, Hinic V, Graf S, Tarr P E (2016). Chronic osteomyelitis due to Tissierella carlieri: First case. Open Forum Infectious Diseases, 3(1): ofw012

[39] Siqueira J F Jr, Rôças I N (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

[40] Siqueira J F Jr, Rôças I N (2008). Update on endodontic microbiology: candidate pathogens and patterns of colonisation. Endodontic Practice Today, 2(1): 7–20

[41] Smillie C S, Smith M B, Friedman J, Cordero O X, David L A, Alm E J (2011). Ecology drives a global network of gene exchange connecting the human microbiome. Nature, 480(7376): 241–244

[42] Stokes H W, Gillings M R (2011). Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS Microbiology Reviews, 35(5): 790–819

[43] Su J Q, An X L, Li B, Chen Q L, Gillings M R, Chen H, Zhang T, Zhu Y G (2017). Metagenomics of urban sewage identifies an extensively shared antibiotic resistome in China. Microbiome, 5(1): 1–15

[44] Tao W, Zhang X X, Zhao F, Huang K, Ma H, Wang Z, Ye L, Ren H (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

[45] Towner K J (2009). Acinetobacter: an old friend, but a new enemy. Journal of Hospital Infection, 73(4): 355–363

[46] Udikovic-Kolic N, Wichmann F, Broderick N A, Handelsman J (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

[47] Wang Q, Garrity G M, Tiedje J M, Cole J R (2007). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16): 5261–5267

[48] Wu L, Yang Y, Chen S, Jason Shi Z, Zhao M, Zhu Z, Yang S, Qu Y, Ma Q, He Z, Zhou J, He Q (2017). Microbial functional trait of rRNA operon copy numbers increases with organic levels in anaerobic digesters. ISME Journal, 11(12): 2874–2878

[49] Wu N, Zhang W Y, Xie S Y, Zeng M, Liu H X, Yang J H, Liu X Y, Yang F (2020). Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China. Frontiers of Environmental Science & Engineering, 14(1): 1

[50] Yan N (2013). Structural advances for the major facilitator superfamily (MFS) transporters. Trends in Biochemical Sciences, 38(3): 151–159

[51] Zhang H, He H, Chen S, Huang T, Lu K, Zhang Z, Wang R, Zhang X, Li H (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

[52] Zhang J, Gao Q, Zhang Q, Wang T, Yue H, Wu L, Shi J, Qin Z, Zhou J, Zuo J, Yang Y (2017). Bacteriophage–prokaryote dynamics and interaction within anaerobic digestion processes across time and space. Microbiome, 5(1): 1–10

[53] Zhang M, He L Y, Liu Y S, Zhao J L, Zhang J N, Chen J, Zhang Q Q, Ying G G (2020). Variation of antibiotic resistome during commercial livestock manure composting. Environment International, 136: 105458

[54] Zhang T, Zhang M, Zhang X, Fang H H (2009). Tetracycline resistance genes and tetracycline resistant lactose-fermenting Enterobacteriaceae in activated sludge of sewage treatment plants. Environmental Science & Technology, 43(10): 3455–3460

[55] Zhu D, Wang H T, Zheng F, Yang X R, Christie P, Zhu Y G (2019). Collembolans accelerate the dispersal of antibiotic resistance genes in the soil ecosystem. Soil Ecology Letters, 1(1–2): 14–21

[56] Zhu Y G, Johnson T A, Su J Q, Qiao M, Guo G X, Stedtfeld R D, Hashsham S A, Tiedje J M (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

Acknowledgements

This work was sponsored by the National Key R&D Program of China (No. 2019YFC1806204) and the National Natural Science Foundation of China (Grant Nos. 41825016 and 41430856).

Authorship Contribution Statement

Ziyan Qin: Conceptualization, Methodology, Investigation, Visualization, Writing- original draft, Writing- review and editing. Qun Gao: Conceptualization, Investigation, Methodology, Writing- original draft, Writing- review and editing. Qiang Dong: Investigation, Formal analysis. Joy D. Van Nostrand: Writing- review and editing. Qi Qi: Writing- review and editing. Tianjiao Dai: Writing- review and editing. Jingmin Cheng: Writing- review and editing. Jizhong Zhou: Resources, Supervision, Funding acquisition. Yunfeng Yang: Validation, Writing- review and editing, Supervision, Funding acquisition.

Declaration of Competing Interest

The authors declare no conflicts of interest.

Data Availability

GeoChip data are available in the NCBI GEO database under project no. GSE132839. DNA sequences of the 16S rRNA gene are available in the NCBI Sequence Read Archive under project no. PRJNA516026.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-021-1466-7org/?? and is accessible for authorized users.

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