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Pathogens, Virulence and Resistance Genes Surveillance with Metagenomics Can Pre bioRxiv preprint doi: https://doi.org/10.1101/2021.06.30.450418; this version posted June 30, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Pathogens, Virulence and Resistance Genes Surveillance with Metagenomics Can Pre- 2 empt Dissemination and Escalation of Untreatable Infections: A Systematic Review and 3 Meta-analyses. 4 John Osei Sekyere1#, Sara Lino Faife2,3 5 1Department of Medical Microbiology, School of Medicine, Faculty of Health Sciences, University of Pretoria, 6 0084 Prinshof, Pretoria, South Africa. 7 2Department of Consumer and Food Science, Faculty of Agriculture and Natural Sciences, University of 8 Pretoria, 0002 Hatfield, Pretoria, South Africa. 9 3Training Area of Diagnostic Technology, Pedagogical Direction, High Institute of Health Sciences, Maputo 10 City, Mozambique. 11 #Address correspondence to Dr John Osei Sekyere, [email protected]; [email protected] 12 Tweet: “It is high time nations adopted periodic metagenomic surveillance of sewage, effluents, 13 ground and surface water to provide early warning systems that can pre-empt infectious disease 14 outbreaks and spikes in vaccine, bacteriophage and antibiotic resistance determinants.” 15 Running head: Metagenomic surveillance for infectious agents & ARGs. 16 Importance/significance 17 Global metagenomic analyses of drinking water, effluents, influents, un/-treated sewage, 18 WWTPs, sludge, rivers, lakes, soil, sediments, biosolid, air and plants. showed the global 19 distribution of diverse clinically important ARGs on mobile genetic elements, antimicrobial- 20 resistant bacteria (ARB) and pathogens, metal resistance genes, and virulence genes in almost 21 all environments. These depict the importance of shot-gun metagenomics as a surveillance 22 tool for AMR and infectious disease control to safeguard water & food quality as well as 23 public health from water- and food-borne outbreaks of pathogenic and ARB infections. More 24 concerning was the identification of ARGs to last-resort antibiotics i.e., carbapenems, 25 colistin, & tigecycline. 26 Abstract bioRxiv preprint doi: https://doi.org/10.1101/2021.06.30.450418; this version posted June 30, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 27 Background. The dissemination of pathogens carrying genetic elements such as 28 antimicrobial resistance genes (ARGs), mobile-genetic elements (MGEs), virulome and 29 methylome have a negative impact on food and environment safety, water quality and animal 30 and human health. The applications of metagenomics to monitor and identify the 31 prevalence/endemicity and emergence of these pathogenic agents from different sources were 32 examined. 33 Methods. Articles published in English language up to October 2020 were searched for on 34 PubMed. Qualitative and quantitative data extracted from the included articles were 35 translated into charts and maps. GraphPad Prism 9.0.2 was used to undertake statistical 36 analysis using descriptive and column statistics, Chi-square, ANOVA, Wilcoxon’s signed- 37 rank, and one-sample t-test. 38 Results. In all, 143 articles from 39 countries from Europe, America, Asia, and Africa were 39 quantitatively analysed. Metagenomes from sewage/wastewater, surface water samples 40 (ocean, sea, river lake, stream and tap water), WWTP, effluents and sludge samples contained 41 pathogenic bacteria (Aeromonas, Acinetobacter, Pseudomonas, Streptococcus, Bacteroides, 42 Escherichia coli, Salmonella enterica, Klebsiella pneumoniae and Acinetobacter baumannii), 43 viruses (Adenovirus, Enterovirus, Hepatovirus, Mamastrovirus and Rotavirus) and parasites 44 (Acanthamoeba, Giardia, Entamoeba, Blastocystis and Naegleria). Integrons, plasmids, 45 transposons, insertion sequences, prophages and integrative and conjugative elements were 46 identified. ARGs mediating resistance to important antibiotics, including β-lactams, 47 aminoglycosides, fluoroquinolones, and tetracycline, and virulence factors such as secretion 48 system, adherence, antiphagocytosis, capsule, invasion, iron uptake, hemolysin, and flagella. 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.30.450418; this version posted June 30, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 49 Conclusion. Clinically important pathogens, ARGs, and MGEs were identified in diverse 50 clinical, environmental, and animal sources through metagenomics, which can be used to 51 determine the prevalence and emergence of known and unknown pathogens and ARGs. 52 Keywords: Resistome; methylome; virulome; pathogens; microbiome; next-generation 53 sequencing; shot-gun metagenomics. 54 1. Introduction 55 Food security, water quality, environmental safety/health, animal (veterinary), and public 56 health are affected negatively by the presence of pathogens as well as by virulence, DNA 57 methylase and resistance genes in both commensals and pathogens (1–3). Whilst pathogenic 58 but non-resistant infectious agents can cause diseases, they are treatable. However, 59 antimicrobial-resistance genes (ARGs) in these pathogens, or in commensals that can transfer 60 ARGs into pathogens, make these pathogens untreatable with many antimicrobials (4–7). 61 Further, the presence of mobile genetic elements (MGEs) and DNA methylases (MTases) can 62 aggravate both infection and resistance by enhancing the dissemination of ARGs and 63 virulence determinants within and between species, and regulating resistance and virulence 64 gene expression in pathogens, respectively (8–13). Hence, although pathogens are deadly, 65 antimicrobial-resistant pathogens are even more fatal and to be dreaded. Furthermore, the 66 virulence and resistance levels of these pathogens are determinable by the presence of MGEs 67 and MTases, making them important molecular determinants of pathogenicity and resistance 68 (14–17). 69 This panoramic picture of the interconnected relationship between these molecular 70 determinants of resistance and virulence is even more graphic when the possibility of these 71 virulent and resistant pathogens moving from environment to animals and humans through 72 food and water, and subsequently between animals and humans (zoonoses and 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.30.450418; this version posted June 30, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 73 anthroponoses), are contemplated (3,18–20). Indeed, real-world occurrences, specifically 74 with the current ongoing coronavirus outbreak (21), as well as the Ebola virus (22), H1N1 flu 75 (23), cholera (24), and polio epidemics(25,26), are testament to the interconnected nature of 76 humans, animals, and the environment. An appreciation of this interconnectedness has 77 birthed the One Health concept in biomedical and epidemiological research (27–29). Using 78 the One Health approach, the transmission of infections from the environment to animals and 79 humans can be easily identified and checked (3,30,31). 80 The emergence of next-generation sequencing and subsequently, shotgun metagenomics, is 81 revolutionizing infectious diseases research as scientists can now sequence the whole 82 genomes of single and multiple species in single and diverse environments or hosts (either 83 animal or human)(11). For instance, long-read sequencing using PacBio and Oxford 84 Nanopore platforms can enable species- and strain-resolved binning of genomes obtained 85 from sequencing DNA obtained directly from animal, human, and environmental specimen 86 (32–34). This means that the species and strains found in the specimen can be identified 87 without having to culture them directly on plates. Efforts are being made to use methylation 88 signatures to enable the association of plasmids found in metagenomes with their host 89 cells/species (11). Due to these applications, metagenomics can be used to survey 90 environments, foods, sewage, water, animal, and human specimens for disease-causing 91 pathogens, antimicrobial resistance, and virulence determinants (11). Already, sewage-based 92 surveillance of antimicrobial resistance, polio and coronavirus genes have been undertaken 93 using metagenomics(35–37). 94 However, the applications of shotgun metagenomics for a One Health monitoring of ARGs 95 and pathogens remain to be fully adopted globally. The current covid-19 pandemic has shown 96 the benefits of using metagenomics as an epidemiological and research tool to trace the levels 97 of pathogens in sewage samples (38–43). This can be translated to identify plasmids, MTases, 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.30.450418; this version posted June 30, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is
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