Toward a Metagenomic Understanding on the Bacterial Composition and Resistome in Hong Kong Banknotes

Currency is possibly one of the main media transmitting pathogens and drug resistance due to its wide circulation in daily life. In this study, we made a comprehensive characterization of the bacterial community present on banknotes collected from different geographical regions of Hong Kong (HK) by performing in vitro characterization of the bacterial presence and resistome profile, as well as metagenomic analysis including microbial diversity, the prevalence of potential pathogens, the dissemination potential of antibiotic-resistance genes (ARGs), among others. When comparing the bacterial community of HK banknotes with other HK environmental samples, including water and marine sediment, we revealed that HK banknotes cover nearly 50% of total genera found in all the environmental samples, implying that banknotes harbor diverse bacteria originated from a variety of environments. Furthermore, the banknotes have higher abundance of potential pathogenic species (~5 times more) and ARGs (~5 times more) with higher dissemination potential (~48 times more) compared with other environmental samples. These findings unveiled the capabilities of this common medium of exchange to accommodate various bacteria, and transmit pathogens and antibiotic resistance. Furthermore, the observed independence of microbiome profile from the city's topological indices led us to formulate a hypothesis that due to their high circulation banknotes may harbor a homogenized microbiome.

[1]  Bing Li,et al.  Exploring variation of antibiotic resistance genes in activated sludge over a four-year period through a metagenomic approach. , 2013, Environmental science & technology.

[2]  M. Ellabaan,et al.  Limited dissemination of the wastewater treatment plant core resistome , 2015, Nature Communications.

[3]  Peter Cimermancic,et al.  A Systematic Analysis of Biosynthetic Gene Clusters in the Human Microbiome Reveals a Common Family of Antibiotics , 2014, Cell.

[4]  J. Corbeil,et al.  Nevirapine resistance mutations of human immunodeficiency virus type 1 selected during therapy , 1994, Journal of virology.

[5]  S. Hallam,et al.  Non-symbiotic Bradyrhizobium ecotypes dominate North American forest soils , 2015, The ISME Journal.

[6]  Benjamin J. Cowling,et al.  School Closure and Mitigation of Pandemic (H1N1) 2009, Hong Kong , 2010, Emerging infectious diseases.

[7]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[8]  P. Tambyah,et al.  The global spread of healthcare-associated multidrug-resistant bacteria: a perspective from Asia. , 2013, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[9]  L. S. Hung The SARS Epidemic in Hong Kong: What Lessons have we Learned? , 2003, Journal of the Royal Society of Medicine.

[10]  Jun Cheng,et al.  Drug-Resistant and Genetic Evolutionary Analysis of Influenza Virus from Patients During the 2013 and 2014 Influenza Season in Beijing. , 2017, Microbial drug resistance.

[11]  Patrick K. H. Lee,et al.  Indoor-Air Microbiome in an Urban Subway Network: Diversity and Dynamics , 2014, Applied and Environmental Microbiology.

[12]  Patrick K. H. Lee,et al.  Indoor air bacterial communities in Hong Kong households assemble independently of occupant skin microbiomes. , 2016, Environmental microbiology.

[13]  P. Chan,et al.  Outbreak of avian influenza A(H5N1) virus infection in Hong Kong in 1997. , 2002, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[14]  Duy Tin Truong,et al.  Strain-level microbial epidemiology and population genomics from shotgun metagenomics , 2016, Nature Methods.

[15]  Alison F. Takemura,et al.  Associations and dynamics of Vibrionaceae in the environment, from the genus to the population level , 2013, Front. Microbiol..

[16]  H. Sokol,et al.  Faecalibacterium prausnitzii and human intestinal health. , 2013, Current opinion in microbiology.

[17]  Gianni Panagiotou,et al.  Probiotics modulated gut microbiota suppresses hepatocellular carcinoma growth in mice , 2016, Proceedings of the National Academy of Sciences.

[18]  C. Jeon,et al.  Halomonas cibimaris sp. nov., isolated from jeotgal, a traditional Korean fermented seafood , 2013, Antonie van Leeuwenhoek.

[19]  The UniProt Consortium,et al.  The Universal Protein Resource (UniProt) 2009 , 2008, Nucleic Acids Res..

[20]  D. Leffler,et al.  Clostridium difficile outbreaks: prevention and treatment strategies , 2012 .

[21]  J. Akoachere,et al.  Public health implications of contamination of Franc CFA (XAF) circulating in Buea (Cameroon) with drug resistant pathogens , 2014, BMC Research Notes.

[22]  Jeff Kline,et al.  Architectural design influences the diversity and structure of the built environment microbiome , 2012, The ISME Journal.

[23]  A. Coffey,et al.  Investigation into the prevalence, persistence and antibiotic resistance profiles of staphylococci isolated from euro currency , 2013, Journal of applied microbiology.

[24]  S. Canizales-Quinteros,et al.  Combining metagenomics, metatranscriptomics and viromics to explore novel microbial interactions: towards a systems-level understanding of human microbiome , 2015, Computational and structural biotechnology journal.

[25]  Heebal Kim,et al.  HGTree: database of horizontally transferred genes determined by tree reconciliation , 2015, Nucleic Acids Res..

[26]  M. Cerquetti,et al.  Genital carriage of the genus Haemophilus in pregnancy: species distribution and antibiotic susceptibility. , 2015, Journal of medical microbiology.

[27]  Jen-Her Lu,et al.  Clinical analysis of Enterobacter bacteremia in pediatric patients: a 10-year study. , 2014, Journal of microbiology, immunology, and infection = Wei mian yu gan ran za zhi.

[28]  Melissa J. Landrum,et al.  RefSeq: an update on mammalian reference sequences , 2013, Nucleic Acids Res..

[29]  Tetsuya Hayashi,et al.  Complete Genome Sequence of a Propionibacterium acnes Isolate from a Sarcoidosis Patient , 2013, Genome Announcements.

[30]  Bevin Cohen,et al.  A Review of Antibiotic Use in Food Animals: Perspective, Policy, and Potential , 2012, Public health reports.

[31]  J. Qiu,et al.  Impacts of human activities on distribution of sulfate-reducing prokaryotes and antibiotic resistance genes in marine coastal sediments of Hong Kong. , 2016, FEMS microbiology ecology.

[32]  S. Sanabani,et al.  Molecular Analysis of Bacterial Microbiota on Brazilian Currency Note Surfaces , 2015, International journal of environmental research and public health.

[33]  Rob Knight,et al.  ConStrains identifies microbial strains in metagenomic datasets , 2015, Nature Biotechnology.

[34]  G. Sumbali,et al.  CONTAMINATED MONEY IN CIRCULATION: A REVIEW , 2014 .

[35]  R. Fairhurst,et al.  Artemisinin-Resistant Plasmodium falciparum Malaria , 2016, Microbiology spectrum.

[36]  W Ferreira,et al.  Origin and progress of the 1968-69 Hong Kong influenza epidemic. , 1969, Bulletin of the World Health Organization.

[37]  S. Schuster,et al.  Integrative analysis of environmental sequences using MEGAN4. , 2011, Genome research.

[38]  A. Kramer,et al.  How long do nosocomial pathogens persist on inanimate surfaces? A systematic review , 2006, BMC infectious diseases.

[39]  K. Bernard The Genus Corynebacterium and Other Medically Relevant Coryneform-Like Bacteria , 2012, Journal of Clinical Microbiology.

[40]  V. Scaria,et al.  Screening Currency Notes for Microbial Pathogens and Antibiotic Resistance Genes Using a Shotgun Metagenomic Approach , 2015, PloS one.

[41]  Yan Zhang,et al.  PATRIC, the bacterial bioinformatics database and analysis resource , 2013, Nucleic Acids Res..

[42]  S. Awe,et al.  Bacteriological quality of some Nigerian currencies in circulation , 2010 .

[43]  M. Khalid,et al.  Idiopathic CD4+ T-lymphocytopenia--a diagnostic dilemma. , 2010, The Journal of the Association of Physicians of India.

[44]  Richa Katiyar,et al.  Prevalence of multidrug-resistant, coagulase-positive Staphylococcus aureus in nasal carriage, food, wastewater and paper currency in Jalandhar city (north-western), an Indian state of Punjab , 2014, Environmental Monitoring and Assessment.

[45]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[46]  Kazuo Kobayashi,et al.  Sphingomonas melonis sp. nov., a novel pathogen that causes brown spots on yellow Spanish melon fruits. , 2002, International journal of systematic and evolutionary microbiology.

[47]  P. Dixon VEGAN, a package of R functions for community ecology , 2003 .

[48]  C. Llor,et al.  Antimicrobial resistance: risk associated with antibiotic overuse and initiatives to reduce the problem , 2014, Therapeutic advances in drug safety.

[49]  Manolis Kellis,et al.  Efficient algorithms for the reconciliation problem with gene duplication, horizontal transfer and loss , 2012, Bioinform..

[50]  Chao Xie,et al.  Fast and sensitive protein alignment using DIAMOND , 2014, Nature Methods.

[51]  M. Raviglione,et al.  Tuberculosis 2015: Burden, Challenges and Strategy for Control and Elimination , 2016, Infectious disease reports.

[52]  Kai Blin,et al.  antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters , 2015, Nucleic Acids Res..

[53]  Andrew C. Pawlowski,et al.  The Comprehensive Antibiotic Resistance Database , 2013, Antimicrobial Agents and Chemotherapy.

[54]  S. Kariuki,et al.  Profile of bacteria and fungi on money coins. , 2009, East African medical journal.

[55]  B. Söderquist,et al.  Propionibacterium avidum as an Etiological Agent of Prosthetic Hip Joint Infection , 2016, PloS one.

[56]  K. Warriner,et al.  Bacterial Contamination of Iranian Paper Currency , 2013, Iranian journal of public health.

[57]  J. Wong,et al.  Influence of livestock activities on residue antibiotic levels of rivers in Hong Kong , 2017, Environmental Science and Pollution Research.

[58]  D. Raoult,et al.  Paper money and coins as potential vectors of transmissible disease. , 2014, Future microbiology.

[59]  A. Voss,et al.  Money and transmission of bacteria , 2013, Antimicrobial Resistance and Infection Control.

[60]  T. Nasreen,et al.  Evaluation of the Microbial Contamination of Bangladesh Paper Currency Notes ( Taka ) in Circulation , 2013 .

[61]  Allyson L. Byrd,et al.  Biogeography and individuality shape function in the human skin metagenome , 2014, Nature.

[62]  M. Bassetti,et al.  Why is community-associated MRSA spreading across the world and how will it change clinical practice? , 2009, International journal of antimicrobial agents.

[63]  Molly K. Gibson,et al.  Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology , 2014, The ISME Journal.

[64]  G. Panagiotou,et al.  COMAN: a web server for comprehensive metatranscriptomics analysis , 2016, BMC Genomics.

[65]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[66]  Mihai Pop,et al.  ARDB—Antibiotic Resistance Genes Database , 2008, Nucleic Acids Res..

[67]  Molly K. Gibson,et al.  Bacterial phylogeny structures soil resistomes across habitats , 2014, Nature.