Culturomics and metagenomics: In understanding of environmental resistome

Abstract

State of the art of culturomics and metagenomics to study resistome was presented.

The combination of culturomics and metagenomics approaches was proposed.

The research directions of antibiotic resistance study has been suggested.

Pharmaceutical residues, mainly antibiotics, have been called “emerging contaminants” in the environment because of their increasing frequency of detection in aquatic and terrestrial systems and their sublethal ecological effects. Most of them are undiscovered. Both human and veterinary pharmaceuticals, including antibiotics, are introduced into the environment via many different routes, including discharges from municipal wastewater treatment plants and land application of animal manure and biosolids to fertilize croplands. To gain a comprehensive understanding of the widespread problem of antibiotic resistance, modern and scientific approaches have been developed to gain knowledge of the entire antibiotic-resistant microbiota of various ecosystems, which is called the resistome. In this review, two omics methods, i.e. culturomics, a new approach, and metagenomics, used to study antibiotic resistance in environmental samples, are described. Moreover, we discuss how both omics methods have become core scientific tools to characterize microbiomes or resistomes, study natural communities and discover new microbes and new antibiotic resistance genes from environments. The combination of the method for get better outcome of both culturomics and metagenomics will significantly advance our understanding of the role of microbes and their specific properties in the environment.

Graphical abstract

Keywords

Culturomics / Metagenomics / Antibiotic resistance / Resistome

References

[1] Abdallah R A, Beye M, Diop A, Bakour S, Raoult D, Fournier P E (2017). The impact of culturomics on taxonomy in clinical microbiology. Antonie van Leeuwenhoek, 110(10): 1327–1337

[2] Akiyama T, Savin M C (2010). Populations of antibiotic-resistant coliform bacteria change rapidly in a wastewater effluent dominated stream. The Science of the total environment, 408(24): 6192–6201

[3] Allan E (2014). Metagenomics: unrestricted access to microbial communities. Virulence, 5(3): 397–398

[4] Alves L F, Westmann C A, Lovate G L, de Siqueira G M V, Borelli T C, Guazzaroni M E (2018). Metagenomic approaches for understanding new concepts in microbial science. International Journal of Genomics, 2018: 1

[5] Amos G C A, Zhang L, Hawkey P M, Gaze W H, Wellington E M (2014). Functional metagenomic analysis reveals rivers are a reservoir for diverse antibiotic resistance genes. Veterinary Microbiology, 171(3-4): 441–447

[6] Amrane S, Lagier J C (2018). Metagenomic and clinical microbiology. Human Microbiome Journal, 9(1): 1–6

[7] Anjum M F (2015). Screening methods for the detection of antimicrobial resistance genes present in bacterial isolates and the microbiota. Future Microbiology, 10(3): 317–320

[8] Bilen M, Dufour J C, Lagier J C, Cadoret F, Daoud Z, Dubourg G, Raoult D (2018). The contribution of culturomics to the repertoire of isolated human bacterial and archaeal species. Microbiome, 6(1): 94

[9] Chen B, Yang Y, Liang X, Yu K, Zhang T, Li X (2013). Metagenomic profiles of antibiotic resistance genes (ARGs) between human impacted estuary and deep ocean sediments. Environmental Science & Technology, 47(22): 12753–12760

[10] Chistoserdova L (2010). Functional metagenomics: recent advances and future challenges. Biotechnology & Genetic Engineering Reviews, 26(1): 335–352

[11] Christgen B, Yang Y, Ahammad S Z, Li B, Rodriquez D C, Zhang T, Graham D W (2015). Metagenomics shows that low-energy anaerobic-aerobic treatment reactors reduce antibiotic resistance gene levels from domestic wastewater. Environmental Science & Technology, 49(4): 2577–2584

[12] Chu B T T, Petrovich M L, Chaudhary A, Wright D, Murphy B, Wells G, Poretsky R (2018). Metagenomics reveals the impact of wastewater treatment plants on the dispersal of microorganisms and genes in aquatic sediments. Applied and Environmental Microbiology, 84(5): e02168–e17

[13] Crofts T S, Gasparrini A J, Dantas G (2017). Next-generation approaches to understand and combat the antibiotic resistome. Nature Reviews. Microbiology, 15(7): 422–434

[14] Davies J, Davies D (2010). Origins and evolution of antibiotic resistance. Microbiology Molecular Reports, 74(3): 417–433

[15] Di Bella J M, Bao Y, Gloor G B, Burton J P, Reid G (2013). High throughput sequencing methods and analysis for microbiome research. Journal of Microbiological Methods, 95(3): 401–414

[16] Elbehery A H A, Aziz R K, Siam R (2016). Antibiotic resistome: Improving detection and quantification accuracy for comparative metagenomics. OMICS: A Journal of Integrative Biology, 20(4): 229–238

[17] Escobar-Zepeda A, Vera-Ponce de Leon A, Sanchez-Flores A (2015). The road to metagenomics: From microbiology to DNA sequencing technologies and bioinformatics. Froniers in Genetics, 6: 348

[18] Fitzpatrick D, Walsh F (2016). Antibiotic resistance genes across a wide variety of metagenomes. FEMS Microbiology Ecology, 92(2): 11–21

[19] Gatica J, Tripathi V, Green S, Manaia C M, Berendonk T, Cacace D, Merlin C, Kreuzinger N, Schwartz T, Fatta-Kassinos D, Rizzo L, Schwermer C U, Garelick H, Jurkevitch E, Cytryn E (2016). High throughput analysis of integrin gene cassettes in wastewater environments. Environmental Science & Technology, 50(21): 11825–11836

[20] Greub G (2012). Culturomics: A new approach to study the human microbiome. Clinical Microbiology and Infection, 18(12): 1157–1159

[21] Guo J, Li J, Chen H, Bond P L, Yuan Z (2017). Metagenomic analysis reveals wastewater treatment plants as hotspots of antibiotic resistance genes and mobile genetic elements. Water Research, 123(3): 468–478

[22] Gupta S K, Shin H, Han D, Hur H G, Unno T (2018). Metagenomic analysis reveals the prevalence and persistence of antibiotic- and heavy metal-resistance genes in wastewater treatment plant. Journal of Microbiology (Seoul, Korea), 56(6): 408–415

[23] Hamad I, Ranque S, Azhar E I, Yasir M, Jiman-Fatani A A, Tissot-Dupont H, Raoult D, Bittar F, Bittar F (2017). Culturomics and Amplicon-based Metagenomic Approaches for the Study of Fungal Population in Human Gut Microbiota. Scientific Reports, 7(1): 16788

[24] Handelsman J, Rondon M R, Brady S F, Clardy J, Goodman R M (1998). Molecular biological access to the chemistry of unknown soil microbes: A new frontier for natural products. Chemistry & Biology, 5(10): R245–R249

[25] Hu Q, Zhang X X, Jia S, Huang K, Tang J, Shi P, Ye L, Ren H (2016). Metagenomic insights into ultraviolet disinfection effects on antibiotic resistome in biologically treated wastewater. Water Research, 101(3): 309–317

[26] Hugon P, Dufour J C, Colson P, Fournier P E, Sallah K, Raoult D (2015). A comprehensive repertoire of prokaryotic species identified in human beings. The Lancet. Infectious Diseases, 15(10): 1211–1219

[27] Jackson R W, Vinatzer B, Arnold D L, Dorus S, Murillo J (2011). The influence of the accessory genome on bacterial pathogen evolution. Mobile Genetic Elements, 1(1): 55–65

[28] Jałowiecki Ł, Chojniak J, Dorgeloh E, Hegedusova B, Ejhed H, Magnér J, Płaza G (2017). Using phenotype microarrays in the assessment of the antibiotic susceptibility profile of bacteria isolated from wastewater in on-site treatment facilities. Folia Microbiologica, 62(6): 453–461

[29] Kambouris M E, Pavlidis C, Skoufas E, Arabatzis M, Kantzanou M, Velegraki A, Patrinos G P (2018). Culturomics: A new kid on the block of OMICS to enable personalized medicine. OMICS: A Journal of Integrative Biology, 22(2), 234–245

[30] Khelaifia S, Lagier J Ch, Bibi F, Azhar E I, Croce O, Padmanabhan R, Jiman-Fatani A A, Yasir M, Robert C, Andrieu C, Fournier P E, Raoult D (2016). Microbial culturomics to map halophilic bacterium in human gut: genome sequence and description of Oceanobacillus jeddahense sp. nov. Journal of Integrative Biolology, 20(4): 248–258

[31] Lagier J C, Armougom F, Million M, Hugon P, Pagnier I, Robert C, Bittar F, Fournous G, Gimenez G, Maraninchi M, Trape J F, Koonin E V, La Scola B, Raoult D (2012). Microbial culturomics: paradigm shift in the human gut microbiome study. Clinical Microbiology and Infection, 18(12): 1185–1193

[32] Lagier J C, Dubourg G, Million M, Cadoret F, Bilen M, Fenollar F, Levasseur A, Rolain J M, Fournier P E, Raoult D (2018). Culturing the human microbiota and culturomics. Nature Reviews. Microbiology, 16(9): 540–550

[33] Lagier J C, Hugon P, Khelaifia S, Fournier P E, La Scola B, Raoult D (2015). The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota. Clinical Microbiology Reviews, 28(1): 237–264

[34] Lagier J C, Khelaifia S, Alou M T, Ndongo S, Dione N, Hugon P, Caputo A, Cadoret F, Traore S I, Seck E H, Dubourg G, Durand G, Mourembou G, Guilhot E, Togo A, Bellali S, Bachar D, Cassir N, Bittar F, Delerce J, Mailhe M, Ricaboni D, Bilen M, Dangui Nieko N P, Dia Badiane N M, Valles C, Mouelhi D, Diop K, Million M, Musso D, Abrahão J, Azhar E I, Bibi F, Yasir M, Diallo A, Sokhna C, Djossou F, Vitton V, Robert C, Rolain J M, La Scola B, Fournier P E, Levasseur A, Raoult D (2016). Culture of previously uncultured members of the human gut microbiota by culturomics. Nature Microbiology, 1(2): 16203

[35] Lam K N, Cheng J, Engel K, Neufeld J D, Charles T C (2015). Current and future resources for functional metagenomics. Frontiers in Microbiology, 6: article1196

[36] Lanza V F, Baquero F, Martínez J L, Ramos-Ruíz R, González-Zorn B, Andremont A, Sánchez-Valenzuela A, Ehrlich S D, Kennedy S, Ruppé E, van Schaik W, Willems R J, de la Cruz F, Coque T M (2018). In-depth resistome analysis by targeted metagenomics. Microbiome, 6(1): 11

[37] Lee J, Jeon J H, Shin J, Jang H M, Kim S, Song M S, Kim Y M (2017). Quantitative and qualitative changes in antibiotic resistance genes after passing through treatment processes in municipal wastewater treatment plants. Science of the Total Environment, 605-606: 906–914

[38] Lefkowitz J R, Duran M (2009). Changes in antibiotic resistance patterns of Escherichia coli during domestic wastewater treatment. Water Environment Research, 81(9): 878–885

[39] Luby E, Ibekwe A M, Zilles J, Pruden A (2016). Molecular methods for assessment of antibiotic resistance in agricultural ecosystems: prospects and challenges. Journal of Environmental Quality, 45(2): 441–453

[40] Ma Y, Metch JW, Yang Y, Pruden A, Zhang T (2016). Shift in antibiotic resistance gene profiles associated with nanosilver during wastewater treatment. FEMS Microbiology Ecology, 92(3): pii: fiw022

[41] March-Rosselló G A (2017). Rapid methods for detection of bacterial resistance to antibiotics. Enfermedades Infecciosas y Microbiologia Clinica, 35(3): 182–188

[42] Martínez J L, Coque T M, Lanza V F, de la Cruz F, Baquero F (2017). Genomic and metagenomic technologies to explore the antibiotic resistance mobilome. Annals of the New York Academy of Sciences, 1388(1): 26–41

[43] Masucci L, Quaranta G, Nagel D, Primus S, Romano L, Graffeo R, Ianiro G, Gasbarrini A, Cammarota G, Sanguinetti M (2017). Culturomics: Bacterial species isolated in 3 healthy donors for faecal microbiota transplantation in Clostridium difficileinfection. Microbiologia Medica, 32: 6510

[44] McLain J E, Cytryn E, Durso L M, Young S (2016). Culture-based methods for detection of antibiotic resistance in agroecosystems: Advantages, challenges, and gaps in knowledge. Journal of Environmental Quality, 45(2): 432–440

[45] Miller R R, Montoya V, Gardy J L, Patrick D M, Tang P (2013). Metagenomics for pathogen detection in public health. Genome Medicine, 5(9): No article: 81

[46] Mohammadali M, Davies J(2018). Antimicrobial resistance genes and wastewater treatment. In: Keen P L, Fugère R, eds. Antimicrobial Resistance in Wastewater Treatment Processes. 1st ed. Hoboken: John Wiley & Sons, Inc., 1–14

[47] Monier J M, Demanèche S, Delmont T O, Mathieu A, Vogel T M, Simonet P (2011). Metagenomic exploration of antibiotic resistance in soil. Current Opinion in Microbiology, 14(3): 229–235

[48] Mullany P (2014). Functional metagenomics for the investigation of antibiotic resistance. Virulence, 5(3): 443–447

[49] Nagarajan M. (2018). Metagenomics. Perspectives, Methods, and Applications. 1st ed. London: Academic Press, Elsevier, , 1– 10

[50] Pärnänen K, Karkman A, Tamminen M, Lyra C, Hultman J, Paulin L, Virta M (2016). Evaluating the mobility potential of antibiotic resistance genes in environmental resistomes without metagenomics. Scientific Reports, 6(1): 35790

[51] Perry J A, Westman E L, Wright G D (2014). The antibiotic resistome: What’s new? Current Opinion in Microbiology, 21: 45–50

[52] Płaza G, Turek A, Szczygłowska R (2013). Characterization of E. coli strains obtained from wastewater effluent. International Journal of Environmental of Research, 2(1): 67–74

[53] Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy M C, Michael I, Fatta-Kassinos D (2013). Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: A review. The Science of the total environment, 447: 345–360

[54] Rosso G E, Muday J A, Curran J F (2018). Tools for Metagenomic Analysis at Wastewater Treatment Plants: Application to a Foaming Episode. Water environment research: A research publication of the Water Environment Federation, 90(3): 258–268

[55] Schmidt T M, DeLong E F, Pace N R (1991). Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing. Journal of Bacteriology, 173(14): 4371–4378

[56] Schmieder R, Edwards R (2012). Insights into antibiotic resistance through metagenomic approaches. Future Microbiology, 7(1): 73–89

[57] Seck E H, Diop A, Armstrong N, Delerce J, Fournier P E, Raoult D, Khelaifia S (2018). Microbial culturomics to isolate halophilic bacteria from table salt: genome sequence and description of the moderately halophilic bacterium Bacillus salis sp. nov. New Microbes and New Infections, 23(1): 28–38

[58] Tang J, Bu Y, Zhang X X, Huang K, He X, Ye L, Shan Z, Ren H (2016). Metagenomic analysis of bacterial community composition and antibiotic resistance genes in a wastewater treatment plant and its receiving surface water. Ecotoxicology and Environmental Safety, 132(2): 260–269

[59] Venter J C, Remington K, Heidelberg J F, Halpern A L, Rusch D, Eisen J A, Wu D, Paulsen I, Nelson K E, Nelson W, Fouts D E, Levy S, Knap A H, Lomas M W, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers Y H, Smith H O (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304(5667): 66–74

[60] Wang Z, Zhang X X, Huang K, Miao Y, Shi P, Liu B, Long C, Li A (2013). Metagenomic profiling of antibiotic resistance genes and mobile genetic elements in a tannery wastewater treatment plant. PLoS One, 8(10): e76079

[61] Xiao K Q, Li B, Ma L, Bao P, Xue Zhou X, Zhang T, Zhu Y G (2016). Metagenomic profiles of antibiotic resistance genes in paddy soils from South China. FEMS Microbiology Ecology, 92: fiw023

[62] Yang Y, Li B, Ju F, Zhang T (2013). Exploring variation of antibiotic resistance genes in activated sludge over a four-year period through a metagenomic approach. Environmental Science & Technology, 47(18): 10197–10205

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The Author(s) 2019. This article is published with open access at link.springer.com and journal.hep.com.cn