Bacterial colonization and succession in a newly opened hospital

Science Translational Medicine

Volumn 9, Issue 391, 2017, Pages

  Lax, Simon ^a,b   Sangwan, Naseer ^b,c   Smith, Daniel ^d   Larsen, Peter ^b   Handley, Kim M ^a,i   Richardson, Miles ^a   Guyton, Kristina ^c   Krezalek, Monika ^c   Shogan, Benjamin D ^c,j   Defazio, Jennifer ^c   Flemming, Irma ^c,k   Shakhsheer, Baddr ^c   Weber, Stephen ^a   Landon, Emily ^a   Garcia Houchins, Sylvia ^a   Siegel, Jeffrey ^e   Alverdy, John ^c   Knight, Rob ^f,g   Stephens, Brent ^h   Gilbert, Jack A ^a,b,c  

^a UNIVERSITY OF CHICAGO   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

^c University of Chicago   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h Illinois Institute of Technology   (United States)

ⁱ UNIVERSITY OF AUCKLAND   (New Zealand)

^j MAYO CLINIC   (United States)

^k VANDERBILT UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ACINETOBACTER; AMBULATORY CARE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL TRANSMISSION; BACTERIUM IDENTIFICATION; CHEMOTHERAPY; COMMUNITY STRUCTURE; CONTROLLED STUDY; CORYNEBACTERIUM; DRUG USE; ENTEROBACTERIACEAE; ENTEROCOCCUS; FINEGOLDIA; GENOTYPE; HOSPITAL; HOSPITAL BED; HOSPITAL PATIENT; HOSPITAL PERSONNEL; HOSPITALIZATION; HUMAN; MAJOR CLINICAL STUDY; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; PREVOTELLA; PRIORITY JOURNAL; PROPIONIBACTERIUM; PSEUDOMONAS; RISK FACTOR; ROOM TEMPERATURE; ROTHIA; SKIN FLORA; SPHINGOMONAS; STAPHYLOCOCCUS; STREPTOCOCCUS; SURFACE AREA; BACTERIUM; BAYES THEOREM; GENETICS; ISOLATION AND PURIFICATION; MICROFLORA;

BACTERIA; BAYES THEOREM; HOSPITALS; HUMANS; MICROBIOTA; PROPIONIBACTERIUM; STAPHYLOCOCCUS;

EID: 85019993393     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aah6500     Document Type: Article

References (47)

1. S. Lax, J. A. Gilbert, Hospital-associated microbiota and implications for nosocomial infections. Trends Mol. Med. 21, 427-432 (2015).
2. S. Lax, D. P. Smith, J. Hampton-Marcell, S. M. Owens, K. M. Handley, N. M. Scott, S. M. Gibbons, P. Larsen, B. D. Shogan, S. Weiss, J. L. Metcalf, L. K. Ursell, Y. Vázquez-Baeza, W. Van Treuren, N. A. Hasan, M. K. Gibson, R. Colwell, G. Dantas, R. Knight, J. A. Gilbert, Longitudinal analysis of microbial interaction between humans and the indoor environment. Science 345, 1048-1052 (2014).
3. R. I. Adams, A. C. Bateman, H. M. Bik, J. F. Meadow, Microbiota of the indoor environment: A meta-analysis. Microbiome 3, 1-18 (2015).
4. M. Wood, S. M. Gibbons, S. Lax, T. W. Eshoo-Anton, S. M. Owens, S. Kennedy, J. A. Gilbert, J. T. Hampton-Marcell, Athletic equipment microbiota are shaped by interactions with human skin. Microbiome 3, 25 (2015).
5. S. Lax, C. R. Nagler, J. A. Gilbert, Our interface with the built environment: Immunity and the indoor microbiota. Trends Immunol. 36, 121-123 (2015).
6. K. E. Fujimura, T. Demoor, M. Rauch, A. A. Faruqi, S. Jang, C. C. Johnson, H. A. Boushey, E. Zoratti, D. Ownby, N. W. Lukacs, S. V. Lynch, House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection. Proc. Natl. Acad. Sci. U.S.A. 111, 805-810 (2014).
7. A. T. Stefka, T. Feehley, P. Tripathi, J. Qiu, K. McCoy, S. K. Mazmanian, M. Y. Tjota, G.-Y. Seo, S. Cao, B. R. Theriault, D. A. Antonopoulos, L. Zhou, E. B. Chang, Y.-X. Fu, C. R. Nagler, Commensal bacteria protect against food allergen sensitization. Proc. Natl. Acad. Sci. U.S.A. 111, 13145-13150 (2014).
8. M. J. Blaser, S. Falkow, What are the consequences of the disappearing human microbiota? Nat. Rev. Microbiol. 7, 887-894 (2009).
9. Department of Health and Human Services, Summary of Notifiable Diseases-United States, 2007 (Centers for Disease Control and Prevention, 2009).
10. R. N. Anderson, B. L. Smith, Deaths: Leading causes for 2002. Natl. Vital Stat. Rep. 53, 67-70 (2005).
11. S. L. Groseclose, W. S. Brathwaite, P. A. Hall, D. A. Adams, F. J. Connor, P. Sharp, W. J. Anderson, R. F. Fagan, J. Javier Aponte, G. F. Jones, D. A. Nitschke, C. A.Worsham, N. Adekoya, M.-H. Chang, T. Doyle, R. Dhara, R. Ann Jajosky, Summary of notifiable diseases-United States, 2002. MMWR Morb. Mortal. Wkly Rep. 51, 1-84 (2004).
12. E. C. Pehrsson, P. Tsukayama, S. Patel, M. Mejía-Bautista, G. Sosa-Soto, K. M. Navarrete, M. Calderon, L. Cabrera, W. Hoyos-Arango, M. Teresita Bertoli, D. E. Berg, R. H. Gilman, G. Dantas, Interconnected microbiomes and resistomes in low-income human habitats. Nature 533, 212-216 (2016).
13. E. S. Snitkin, A. M. Zelazny, P. J. Thomas, F. Stock; NISC Comparative Sequencing Program, D. K. Henderson, T. N. Palmore, J. A. Segre, Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci. Transl. Med. 4, 148ra116 (2012).
14. J. Quick, P. Ashton, S. Calus, C. Chatt, S. Gossain, J. Hawker, S. Nair, K. Neal, K. Nye, T. Peters, E. De Pinna, E. Robinson, K. Struthers, M. Webber, A. Catto, T. J. Dallman, P. Hawkey, N. J. Loman, Rapid draft sequencing and real-time nanopore sequencing in a hospital outbreak of Salmonella. Genome Biol. 16, 114 (2015).
15. S. R. Harris, E. J. Feil, M. T. G. Holden, M. A. Quail, E. K. Nickerson, N. Chantratita, S. Gardete, A. Tavares, N. Day, J. A. Lindsay, J. D. Edgeworth, H. de Lencastre, J. Parkhill, S. J. Peacock, S. D. Bentley, Evolution of MRSA during hospital transmission and intercontinental spread. Science 327, 469-474 (2010).
16. P. R. McAdam, K. E. Templeton, G. F. Edwards, M. T. G. Holden, E. J. Feil, D. M. Aanensen, H. J. A. Bargawi, B. G. Spratt, S. D. Bentley, J. Parkhill, M. C. Enright, A. Holmes, E. K. Girvan, P. A. Godfrey, M. Feldgarden, A. M. Kearns, A. Rambaut, D. A. Robinson, J. R. Fitzgerald, Molecular tracing of the emergence, adaptation, and transmission of hospital-associated methicillin-resistant Staphylococcus aureus. Proc. Natl. Acad. Sci. U.S.A. 109, 9107-9112 (2012).
17. B. Brooks, B. A. Firek, C. S. Miller, I. Sharon, B. C. Thomas, R. Baker, M. J. Morowitz, J. F. Banfield, Microbes in the neonatal intensive care unit resemble those found in the gut of premature infants. Microbiome 2, 1 (2014).
18. K. M. Hewitt, F. L. Mannino, A. Gonzalez, J. H. Chase, J. Gregory Caporaso, R. Knight, S. T. Kelley, Bacterial diversity in two neonatal intensive care units (NICUs). PLOS ONE 8, e54703 (2013).
19. M. Poza, C. Gayoso, M. J. Gómez, S. Rumbo-Feal, M. Tomás, J. Aranda, A. Fernández, G. Bou, Exploring bacterial diversity in hospital environments by GS-FLX Titanium pyrosequencing. PLOS ONE 7, e44105 (2012).
20. J. Oh, A. L. Byrd, M. Park; NISC Comparative Sequencing Program, H. H. Kong, J. A. Segre, Temporal stability of the human skin microbiome. Cell 165, 854-866 (2016).
21. T. Ramos, S. Dedesko, J. A. Siegel, J. A. Gilbert, B. Stephens, Spatial and temporal variations in indoor environmental conditions, human occupancy, and operational characteristics in a new hospital building. PLOS ONE 10, e0118207 (2015).
22. S. Dedesko, B. Stephens, J. A. Gilbert, J. A. Siegel, Methods to assess human occupancy and occupant activity in hospital patient rooms. Build. Environ. 90, 136-145 (2015).
23. J. S. Meisel, G. D. Hannigan, A. S. Tyldsley, A. J. SanMiguel, B. P. Hodkinson, Q. Zheng, E. A. Grice, Skin microbiome surveys are strongly influenced by experimental design. J. Invest. Dermatol. 136, 947-956 (2016).
24. S. Lax, J. T. Hampton-Marcell, S. M. Gibbons, G. B. Colares, D. Smith, J. A. Eisen, J. A. Gilbert, Forensic analysis of the microbiome of phones and shoes. Microbiome 3, 21 (2015).
25. J. F. Meadow, A. E. Altrichter, J. L. Green, Mobile phones carry the personal microbiome of their owners. Peer J. 2, e447 (2014).
26. D. Knights, J. Kuczynski, E. S. Charlson, J. Zaneveld, M. C. Mozer, R. G. Collman, F. D. Bushman, R. Knight, S. T. Kelley, Bayesian community-wide culture-independent microbial source tracking. Nat. Methods 8, 761-763 (2011).
27. D. P. Faith, Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1-10 (1992).
28. A. M. Eren, L. Maignien, W. J. Sul, L. G. Murphy, S. L. Grim, H. G. Morrison, M. L. Sogin, Oligotyping: Differentiating between closely related microbial taxa using 16S rRNA gene data. Methods Ecol. Evol. 4, 1111-1119 (2013).
29. W. Ran, D. M. Kristensen, E. V. Koonin, Coupling between protein level selection and codon usage optimization in the evolution of bacteria and archaea. MBio 5, e00956-14 (2014).
30. Y. Yao, D. E. Sturdevant, A. Villaruz, L. Xu, Q. Gao, M. Otto, Factors characterizing Staphylococcus epidermidis invasiveness determined by comparative genomics. Infect. Immun. 73, 1856-1860 (2005).
31. J. G. Caporaso, C. L. Lauber, W. A. Walters, D. Berg-Lyons, J. Huntley, N. Fierer, S. M. Owens, J. Betley, L. Fraser, M. Bauer, N. Gormley, J. A. Gilbert, G. Smith, R. Knight, Ultra-highthroughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621-1624 (2012).
32. J. G. Caporaso, J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. G. Peña, J. K. Goodrich, J. I. Gordon, G. A. Huttley, S. T. Kelley, D. Knights, J. E. Koenig, R. E. Ley, C. A. Lozupone, D. McDonald, B. D. Muegge, M. Pirrung, J. Reeder, J. R. Sevinsky, P. J. Turnbaugh, W. A. Walters, J. Widmann, T. Yatsunenko, J. Zaneveld, R. Knight, QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
33. J. G. Caporaso, K. Bittinger, F. D. Bushman, T. Z. DeSantis, G. L. Andersen, R. Knight, PyNAST: A flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266-267 (2010).
34. S. Guindon, J.-F. Dufayard, V. Lefort, M. Anisimova, W. Hordijk, O. Gascuel, New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321 (2010).
35. R. C. Edgar, Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).
36. C. Lozupone, R. Knight, UniFrac: A new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228-8235 (2005).
37. N. Segata, L. Waldron, A. Ballarini, V. Narasimhan, O. Jousson, C. Huttenhower, Metagenomic microbial community profiling using unique clade-specific marker genes. Nat. Methods 9, 811-814 (2012).
38. Y. Peng, H. C. M. Leung, S. M. Yiu, F. Y. L. Chin, IDBA-UD: A de novo assembler for singlecell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420-1428 (2012).
39. D. D. Kang, J. Froula, R. Egan, Z. Wang, MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. Peer J. 3, e1165 (2015).
40. C. Kerepesi, D. Bánky, V. Grolmusz, AmphoraNet: The webserver implementation of the AMPHORA2 metagenomic workflow suite. Gene 533, 538-540 (2014).
41. D. P. Wall, H. B. Fraser, A. E. Hirsh, Detecting putative orthologs. Bioinformatics 19, 1710-1711 (2003).
42. M. A. Larkin, G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, D. G. Higgins, Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007).
43. M. Suyama, D. Torrents, P. Bork, PAL2NAL: Robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, W609-W612 (2006).
44. Z. Yang, PAML 4: Phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591 (2007).
45. Z. Zhang, J. Li, P. Cui, F. Ding, A. Li, J. P. Townsend, J. Yu, Codon deviation coefficient: A novel measure for estimating codon usage bias and its statistical significance. BMC Bioinformatics 13, 43 (2012).
46. R. K. Aziz, D. Bartels, A. A. Best, M. DeJongh, T. Disz, R. A. Edwards, K. Formsma, S. Gerdes, E. M. Glass, M. Kubal, F. Meyer, G. J. Olsen, R. Olson, A. L. Osterman, R. A. Overbeek, L. K. McNeil, D. Paarmann, T. Paczian, B. Parrello, G. D. Pusch, C. Reich, R. Stevens, O. Vassieva, V. Vonstein, A. Wilke, O. Zagnitko, The RAST server: Rapid annotations using subsystems technology. BMC Genomics 9, 75 (2008).
47. M. K. Gibson, K. J. Forsberg, G. Dantas, Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. ISME J. 9, 207-216 (2015).