|
|
Culturomics and metagenomics: In understanding of environmental resistome |
Monika Nowrotek1, Łukasz Jałowiecki1, Monika Harnisz2, Grażyna Anna Płaza3() |
1. Microbiology Unit, Institute for Ecology of Industrial Areas, Kossutha 6 Str., 40-844 Katowice, Poland 2. Department of Environmental Microbiology, Faculty of Environmental Sciences, University of Warmia and Mazury, Prawocheńskiego 1 Str., 10-720 Olsztyn, Poland 3. Silesian University of Technology, Faculty of Organization and Management, Institute of Engineering Production, Roosevelta 26 Str., 41-800 Zabrze, Poland |
|
|
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.
|
Keywords
Culturomics
Metagenomics
Antibiotic resistance
Resistome
|
Corresponding Author(s):
Grażyna Anna Płaza
|
Issue Date: 11 June 2019
|
|
1 |
R A Abdallah, M Beye, A Diop, S Bakour, D Raoult, P E Fournier (2017). The impact of culturomics on taxonomy in clinical microbiology. Antonie van Leeuwenhoek, 110(10): 1327–1337
https://doi.org/10.1007/s10482-017-0871-1
pmid: 28389704
|
2 |
T Akiyama, M C Savin (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
https://doi.org/10.1016/j.scitotenv.2010.08.055
pmid: 20888028
|
3 |
E Allan (2014). Metagenomics: unrestricted access to microbial communities. Virulence, 5(3): 397–398
https://doi.org/10.4161/viru.28057
pmid: 24521706
|
4 |
L F Alves, C A Westmann, G L Lovate, G M V de Siqueira, T C Borelli, M E Guazzaroni (2018). Metagenomic approaches for understanding new concepts in microbial science. International Journal of Genomics, 2018: 1
https://doi.org/10.1155/2018/2312987
pmid: 30211213
|
5 |
G C A Amos, L Zhang, P M Hawkey, W H Gaze, E M Wellington (2014). Functional metagenomic analysis reveals rivers are a reservoir for diverse antibiotic resistance genes. Veterinary Microbiology, 171(3-4): 441–447
https://doi.org/10.1016/j.vetmic.2014.02.017
pmid: 24636906
|
6 |
S Amrane, J C Lagier (2018). Metagenomic and clinical microbiology. Human Microbiome Journal, 9(1): 1–6
https://doi.org/10.1016/j.humic.2018.06.001
|
7 |
M F Anjum (2015). Screening methods for the detection of antimicrobial resistance genes present in bacterial isolates and the microbiota. Future Microbiology, 10(3): 317–320
https://doi.org/10.2217/fmb.15.2
pmid: 25812454
|
8 |
M Bilen, J C Dufour, J C Lagier, F Cadoret, Z Daoud, G Dubourg, D Raoult (2018). The contribution of culturomics to the repertoire of isolated human bacterial and archaeal species. Microbiome, 6(1): 94
https://doi.org/10.1186/s40168-018-0485-5
pmid: 29793532
|
9 |
B Chen, Y Yang, X Liang, K Yu, T Zhang, X Li (2013). Metagenomic profiles of antibiotic resistance genes (ARGs) between human impacted estuary and deep ocean sediments. Environmental Science & Technology, 47(22): 12753–12760
https://doi.org/10.1021/es403818e
pmid: 24125531
|
10 |
L Chistoserdova (2010). Functional metagenomics: recent advances and future challenges. Biotechnology & Genetic Engineering Reviews, 26(1): 335–352
https://doi.org/10.5661/bger-26-335
pmid: 21415887
|
11 |
B Christgen, Y Yang, S Z Ahammad, B Li, D C Rodriquez, T Zhang, D W Graham (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
https://doi.org/10.1021/es505521w
pmid: 25603149
|
12 |
B T T Chu, M L Petrovich, A Chaudhary, D Wright, B Murphy, G Wells, R Poretsky (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
pmid: 29269503
|
13 |
T S Crofts, A J Gasparrini, G Dantas (2017). Next-generation approaches to understand and combat the antibiotic resistome. Nature Reviews. Microbiology, 15(7): 422–434
https://doi.org/10.1038/nrmicro.2017.28
pmid: 28392565
|
14 |
J Davies, D Davies (2010). Origins and evolution of antibiotic resistance. Microbiology Molecular Reports, 74(3): 417–433
https://doi.org/10.1128/MMBR.00016-10
pmid: 20805405
|
15 |
J M Di Bella, Y Bao, G B Gloor, J P Burton, G Reid (2013). High throughput sequencing methods and analysis for microbiome research. Journal of Microbiological Methods, 95(3): 401–414
https://doi.org/10.1016/j.mimet.2013.08.011
pmid: 24029734
|
16 |
A H A Elbehery, R K Aziz, R Siam (2016). Antibiotic resistome: Improving detection and quantification accuracy for comparative metagenomics. OMICS: A Journal of Integrative Biology, 20(4): 229–238
https://doi.org/10.1089/omi.2015.0191
pmid: 27031878
|
17 |
A Escobar-Zepeda, A Vera-Ponce de Leon, A Sanchez-Flores (2015). The road to metagenomics: From microbiology to DNA sequencing technologies and bioinformatics. Froniers in Genetics, 6: 348
https://doi.org/10.3389/fgene.2015.00348
pmid: 26734060
|
18 |
D Fitzpatrick, F Walsh (2016). Antibiotic resistance genes across a wide variety of metagenomes. FEMS Microbiology Ecology, 92(2): 11–21
https://doi.org/10.1093/femsec/fiv168
pmid: 26738556
|
19 |
J Gatica, V Tripathi, S Green, C M Manaia, T Berendonk, D Cacace, C Merlin, N Kreuzinger, T Schwartz, D Fatta-Kassinos, L Rizzo, C U Schwermer, H Garelick, E Jurkevitch, E Cytryn (2016). High throughput analysis of integrin gene cassettes in wastewater environments. Environmental Science & Technology, 50(21): 11825–11836
https://doi.org/10.1021/acs.est.6b03188
pmid: 27689892
|
20 |
G Greub (2012). Culturomics: A new approach to study the human microbiome. Clinical Microbiology and Infection, 18(12): 1157–1159
https://doi.org/10.1111/1469-0691.12032
pmid: 23148445
|
21 |
J Guo, J Li, H Chen, P L Bond, Z Yuan (2017). Metagenomic analysis reveals wastewater treatment plants as hotspots of antibiotic resistance genes and mobile genetic elements. Water Research, 123(3): 468–478
https://doi.org/10.1016/j.watres.2017.07.002
pmid: 28689130
|
22 |
S K Gupta, H Shin, D Han, H G Hur, T Unno (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
https://doi.org/10.1007/s12275-018-8195-z
pmid: 29858829
|
23 |
I Hamad, S Ranque, E I Azhar, M Yasir, A A Jiman-Fatani, H Tissot-Dupont, D Raoult, F Bittar, F Bittar (2017). Culturomics and Amplicon-based Metagenomic Approaches for the Study of Fungal Population in Human Gut Microbiota. Scientific Reports, 7(1): 16788
https://doi.org/10.1038/s41598-017-17132-4
pmid: 29196717
|
24 |
J Handelsman, M R Rondon, S F Brady, J Clardy, R M Goodman (1998). Molecular biological access to the chemistry of unknown soil microbes: A new frontier for natural products. Chemistry & Biology, 5(10): R245–R249
https://doi.org/10.1016/S1074-5521(98)90108-9
pmid: 9818143
|
25 |
Q Hu, X X Zhang, S Jia, K Huang, J Tang, P Shi, L Ye, H Ren (2016). Metagenomic insights into ultraviolet disinfection effects on antibiotic resistome in biologically treated wastewater. Water Research, 101(3): 309–317
https://doi.org/10.1016/j.watres.2016.05.092
pmid: 27267479
|
26 |
P Hugon, J C Dufour, P Colson, P E Fournier, K Sallah, D Raoult (2015). A comprehensive repertoire of prokaryotic species identified in human beings. The Lancet. Infectious Diseases, 15(10): 1211–1219
https://doi.org/10.1016/S1473-3099(15)00293-5
pmid: 26311042
|
27 |
R W Jackson, B Vinatzer, D L Arnold, S Dorus, J Murillo (2011). The influence of the accessory genome on bacterial pathogen evolution. Mobile Genetic Elements, 1(1): 55–65
https://doi.org/10.4161/mge.1.1.16432
pmid: 22016845
|
28 |
Ł Jałowiecki, J Chojniak, E Dorgeloh, B Hegedusova, H Ejhed, J Magnér, G Płaza (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
https://doi.org/10.1007/s12223-017-0516-9
pmid: 28451946
|
29 |
M E Kambouris, C Pavlidis, E Skoufas, M Arabatzis, M Kantzanou, A Velegraki, G P Patrinos (2018). Culturomics: A new kid on the block of OMICS to enable personalized medicine. OMICS: A Journal of Integrative Biology, 22(2), 234–245
https://doi.org/10.1089/omi.2017.0017
pmid: 28402209
|
30 |
S Khelaifia, J Ch Lagier, F Bibi, E I Azhar, O Croce, R Padmanabhan, A A Jiman-Fatani, M Yasir, C Robert, C Andrieu, P E Fournier, D Raoult (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
https://doi.org/10.1089/omi.2016.0004
pmid: 27093109
|
31 |
J C Lagier, F Armougom, M Million, P Hugon, I Pagnier, C Robert, F Bittar, G Fournous, G Gimenez, M Maraninchi, J F Trape, E V Koonin, B La Scola, D Raoult (2012). Microbial culturomics: paradigm shift in the human gut microbiome study. Clinical Microbiology and Infection, 18(12): 1185–1193
https://doi.org/10.1111/1469-0691.12023
pmid: 23033984
|
32 |
J C Lagier, G Dubourg, M Million, F Cadoret, M Bilen, F Fenollar, A Levasseur, J M Rolain, P E Fournier, D Raoult (2018). Culturing the human microbiota and culturomics. Nature Reviews. Microbiology, 16(9): 540–550
https://doi.org/10.1038/s41579-018-0041-0
pmid: 29937540
|
33 |
J C Lagier, P Hugon, S Khelaifia, P E Fournier, B La Scola, D Raoult (2015). The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota. Clinical Microbiology Reviews, 28(1): 237–264
https://doi.org/10.1128/CMR.00014-14
pmid: 25567229
|
34 |
J C Lagier, S Khelaifia, M T Alou, S Ndongo, N Dione, P Hugon, A Caputo, F Cadoret, S I Traore, E H Seck, G Dubourg, G Durand, G Mourembou, E Guilhot, A Togo, S Bellali, D Bachar, N Cassir, F Bittar, J Delerce, M Mailhe, D Ricaboni, M Bilen, N P Dangui Nieko, N M Dia Badiane, C Valles, D Mouelhi, K Diop, M Million, D Musso, J Abrahão, E I Azhar, F Bibi, M Yasir, A Diallo, C Sokhna, F Djossou, V Vitton, C Robert, J M Rolain, B La Scola, P E Fournier, A Levasseur, D Raoult (2016). Culture of previously uncultured members of the human gut microbiota by culturomics. Nature Microbiology, 1(2): 16203
https://doi.org/10.1038/nmicrobiol.2016.203
pmid: 27819657
|
35 |
K N Lam, J Cheng, K Engel, J D Neufeld, T C Charles (2015). Current and future resources for functional metagenomics. Frontiers in Microbiology, 6: article1196
https://doi.org/10.3389/fmicb.2015.01196
pmid: 26579102
|
36 |
V F Lanza, F Baquero, J L Martínez, R Ramos-Ruíz, B González-Zorn, A Andremont, A Sánchez-Valenzuela, S D Ehrlich, S Kennedy, E Ruppé, W van Schaik, R J Willems, F de la Cruz, T M Coque (2018). In-depth resistome analysis by targeted metagenomics. Microbiome, 6(1): 11
https://doi.org/10.1186/s40168-017-0387-y
pmid: 29335005
|
37 |
J Lee, J H Jeon, J Shin, H M Jang, S Kim, M S Song, Y M Kim (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
https://doi.org/10.1016/j.scitotenv.2017.06.250
pmid: 28686994
|
38 |
J R Lefkowitz, M Duran (2009). Changes in antibiotic resistance patterns of Escherichia coli during domestic wastewater treatment. Water Environment Research, 81(9): 878–885
https://doi.org/10.2175/106143009X426068
pmid: 19860144
|
39 |
E Luby, A M Ibekwe, J Zilles, A Pruden (2016). Molecular methods for assessment of antibiotic resistance in agricultural ecosystems: prospects and challenges. Journal of Environmental Quality, 45(2): 441–453
https://doi.org/10.2134/jeq2015.07.0367
pmid: 27065390
|
40 |
Y Ma, JW Metch, Y Yang, A Pruden, T Zhang (2016). Shift in antibiotic resistance gene profiles associated with nanosilver during wastewater treatment. FEMS Microbiology Ecology, 92(3): pii: fiw022
https://doi.org/10.1093/femsec/fiw022
pmid: 26850160
|
41 |
G A March-Rosselló (2017). Rapid methods for detection of bacterial resistance to antibiotics. Enfermedades Infecciosas y Microbiologia Clinica, 35(3): 182–188
https://doi.org/10.1016/j.eimce.2017.02.007
pmid: 28109552
|
42 |
J L Martínez, T M Coque, V F Lanza, F de la Cruz, F Baquero (2017). Genomic and metagenomic technologies to explore the antibiotic resistance mobilome. Annals of the New York Academy of Sciences, 1388(1): 26–41
https://doi.org/10.1111/nyas.13282
pmid: 27861983
|
43 |
L Masucci, G Quaranta, D Nagel, S Primus, L Romano, R Graffeo, G Ianiro, A Gasbarrini, G Cammarota, M Sanguinetti (2017). Culturomics: Bacterial species isolated in 3 healthy donors for faecal microbiota transplantation in Clostridium difficileinfection. Microbiologia Medica, 32: 6510
https://doi.org/10.4081/mm.2017.6510
|
44 |
J E McLain, E Cytryn, L M Durso, S Young (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
https://doi.org/10.2134/jeq2015.06.0317
pmid: 27065389
|
45 |
R R Miller, V Montoya, J L Gardy, D M Patrick, P Tang (2013). Metagenomics for pathogen detection in public health. Genome Medicine, 5(9): No article: 81
|
46 |
M Mohammadali, J Davies(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 |
J M Monier, S Demanèche, T O Delmont, A Mathieu, T M Vogel, P Simonet (2011). Metagenomic exploration of antibiotic resistance in soil. Current Opinion in Microbiology, 14(3): 229–235
https://doi.org/10.1016/j.mib.2011.04.010
pmid: 21601510
|
48 |
P Mullany (2014). Functional metagenomics for the investigation of antibiotic resistance. Virulence, 5(3): 443–447
https://doi.org/10.4161/viru.28196
pmid: 24556726
|
49 |
M Nagarajan. (2018). Metagenomics. Perspectives, Methods, and Applications. 1st ed. London: Academic Press, Elsevier, , 1– 10
|
50 |
K Pärnänen, A Karkman, M Tamminen, C Lyra, J Hultman, L Paulin, M Virta (2016). Evaluating the mobility potential of antibiotic resistance genes in environmental resistomes without metagenomics. Scientific Reports, 6(1): 35790
https://doi.org/10.1038/srep35790
pmid: 27767072
|
51 |
J A Perry, E L Westman, G D Wright (2014). The antibiotic resistome: What’s new? Current Opinion in Microbiology, 21: 45–50
https://doi.org/10.1016/j.mib.2014.09.002
pmid: 25280222
|
52 |
G Płaza, A Turek, R Szczygłowska (2013). Characterization of E. coli strains obtained from wastewater effluent. International Journal of Environmental of Research, 2(1): 67–74
|
53 |
L Rizzo, C Manaia, C Merlin, T Schwartz, C Dagot, M C Ploy, I Michael, D Fatta-Kassinos (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
https://doi.org/10.1016/j.scitotenv.2013.01.032
pmid: 23396083
|
54 |
G E Rosso, J A Muday, J F Curran (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
https://doi.org/10.2175/106143017X15054988926352
pmid: 28962671
|
55 |
T M Schmidt, E F DeLong, N R Pace (1991). Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing. Journal of Bacteriology, 173(14): 4371–4378
https://doi.org/10.1128/jb.173.14.4371-4378.1991
pmid: 2066334
|
56 |
R Schmieder, R Edwards (2012). Insights into antibiotic resistance through metagenomic approaches. Future Microbiology, 7(1): 73–89
https://doi.org/10.2217/fmb.11.135
pmid: 22191448
|
57 |
E H Seck, A Diop, N Armstrong, J Delerce, P E Fournier, D Raoult, S Khelaifia (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
https://doi.org/10.1016/j.nmni.2017.12.006
pmid: 29707210
|
58 |
J Tang, Y Bu, X X Zhang, K Huang, X He, L Ye, Z Shan, H Ren (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
https://doi.org/10.1016/j.ecoenv.2016.06.016
pmid: 27340885
|
59 |
J C Venter, K Remington, J F Heidelberg, A L Halpern, D Rusch, J A Eisen, D Wu, I Paulsen, K E Nelson, W Nelson, D E Fouts, S Levy, A H Knap, M W Lomas, K Nealson, O White, J Peterson, J Hoffman, R Parsons, H Baden-Tillson, C Pfannkoch, Y H Rogers, H O Smith (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304(5667): 66–74
https://doi.org/10.1126/science.1093857
pmid: 15001713
|
60 |
Z Wang, X X Zhang, K Huang, Y Miao, P Shi, B Liu, C Long, A Li (2013). Metagenomic profiling of antibiotic resistance genes and mobile genetic elements in a tannery wastewater treatment plant. PLoS One, 8(10): e76079
https://doi.org/10.1371/journal.pone.0076079
pmid: 24098424
|
61 |
K Q Xiao, B Li, L Ma, P Bao, X Xue Zhou, T Zhang, Y G Zhu (2016). Metagenomic profiles of antibiotic resistance genes in paddy soils from South China. FEMS Microbiology Ecology, 92: fiw023
https://doi.org/10.1093/femsec/fiw023
pmid: 26850156
|
62 |
Y Yang, B Li, F Ju, T Zhang (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
https://doi.org/10.1021/es4017365
pmid: 23919449
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|