Staphylococcus prevails in the skin microbiota of long-term immunodeficient mice

Environmental Microbiology

Volumn 14, Issue 8, 2012, Pages 2087-2098

  Garcia Garcerà, Marc ^a,d   Coscollà, Mireia ^a,b   Garcia Etxebarria, Koldo ^a   Martín Caballero, Juan ^c   González Candelas, Fernando ^d   Latorre, Amparo ^d   Calafell, Francesc ^a  

^a INSTITUTE OF EVOLUTIONARY BIOLOGY CSIC UNIVERSITAT POMPEU FABRA   (Spain)

^b SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^c Animal Facility   (Spain)

^d UNIVERSITY OF VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

ANIMAL; ARTICLE; BIODIVERSITY; C57BL MOUSE; GENETICS; IMMUNOLOGY; MALE; METAGENOME; MICROBIOLOGY; MOUSE; MOUSE MUTANT; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REPRODUCIBILITY; SKIN; STAPHYLOCOCCUS; STAPHYLOCOCCUS EPIDERMIDIS;

ANIMALS; BASE SEQUENCE; BIODIVERSITY; MALE; METAGENOME; MICE; MICE, INBRED C57BL; MICE, SCID; REPRODUCIBILITY OF RESULTS; RNA, RIBOSOMAL, 16S; SKIN; STAPHYLOCOCCUS; STAPHYLOCOCCUS EPIDERMIDIS;

BACTERIA (MICROORGANISMS); MUS; STAPHYLOCOCCUS; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 84864383614     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02756.x     Document Type: Article

References (64)

1. Alstrup, S., Gavoille, C., and Kaplan, H. (2004) Nearest common ancestors: a survey and a new algorithm for a distributed environment. Theory of Computing Systems.
2. Amann, R.I., Ludwig, W., and Schleifer, K.H. (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59: 143-169.
3. Bäckhed, F., Ley, R.E., Sonnenburg, J.L., Peterson, D.A., and Gordon, J.I. (2005) Host-bacterial mutualism in the human intestine. Science 307: 1915-1920.
4. Bosma, G.C., Custer, R.P., and Bosma, M.J. (1983) A severe combined immunodeficiency mutation in the mouse. Nature 301: 527-530.
5. Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., etal. (2009) The MIQE Guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments. Clin Chem 55: 611-622.
6. Capella-Gutierrez, S., Silla-Martinez, J.M., and Gabaldon, T. (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973.
7. Castillo, M., Martín-Orúe, S.M., Manzanilla, E.G., Badiola, I., Martín, M., and Gasa, J. (2006) Quantification of total bacteria, enterobacteria and lactobacilli populations in pig digesta by real-time PCR. Vet Microbiol 114: 165-170.
8. Cogen, A., Nizet, V., and Gallo, R. (2008) Skin microbiota: a source of disease or defence? Br J Dermatol 158: 442-455.
9. Cole, J.R., Chai, B., Farris, R.J., Wang, Q., Kulam-Syed-Mohideen, A.S., McGarrell, D.M., etal. (2007) The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35: D169-D172.
10. Cole, J.R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R.J., etal. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145.
11. Costello, E.K., Lauber, C.L., Hamady, M., Fierer, N., Gordon, J.I., and Knight, R. (2009) Bacterial community variation in human body habitats across space and time. Science 326: 1694-1697.
12. Dekio, I., Sakamoto, M., Hayashi, H., Amagai, M., Suematsu, M., and Benno, Y. (2007) Characterization of skin microbiota in patients with atopic dermatitis and in normal subjects using 16S rRNA gene-based comprehensive analysis. J Med Microbiol 56: 1675-1683.
13. Fierer, N., Lauber, C.L., Zhou, N., Mcdonald, D., Costello, E.K., and Knight, R. (2010) From the Cover: forensic identification using skin bacterial communities. Proc Natl Acad Sci 107: 6477-6481.
14. Fredricks, D.N. (2001) Microbial ecology of human skin in health and disease. J Investig Dermatol Symp Proc 6: 167-169.
15. Galdbart, J., Allignet, J., and Tung, H. (2000) Screening for Staphylococcus epidermidis Markers Discriminating between Skin-Flora Strains and Those Responsible for Infections of Joint Prostheses. J Infect Dis 182: 351-355.
16. Gao, Z., Tseng, C.-H., Strober, B.E., Pei, Z., and Blaser, M.J. (2008) Substantial alterations of the cutaneous bacterial biota in psoriatic lesions. PLoS ONE 3: e2719.
17. Gotelli, N.J., and Colwell, R.K. (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4: 379-391.
18. Grice, E.A., and Segre, J.A. (2011) The skin microbiome. Nat Rev Microbiol 9: 244-253.
19. Grice, E.A., Kong, H.H., Renaud, G., Young, A.C., Bouffard, G.G., Blakesley, R.W., etal. (2008) A diversity profile of the human skin microbiota. Genome Res 18: 1043-1050.
20. Grice, E.A., Kong, H.H., Conlan, S., Deming, C.B., Davis, J., Young, A.C., etal. (2009) Topographical and temporal diversity of the human skin microbiome. Science 324: 1190-1192.
21. Grice, E.A., Snitkin, E.S., Yockey, L.J., Bermudez, D.M., NISC Comparative Sequencing Program, Liechty, K.W., etal. (2010) Longitudinal shift in diabetic wound microbiota correlates with prolonged skin defense response. Proc Natl Acad Sci 107: 14799-14804.
22. Higuchi, R., Fockler, C., Dollinger, G., and Watson, R. (1993) Kinetic PCR analysis: real-time monitoring of DNA amplification reactions. Biotechnology 11: 1026-1030.
23. Huerta-Cepas, J., Dopazo, J., and Gabaldón, T. (2010) ETE: a python environment for tree exploration. BMC Bioinformatics 11: 24.
24. Hugenholtz, P., and Pace, N.R. (1996) Identifying microbial diversity in the natural environment: a molecular phylogenetic approach. Trends Biotechnol 14: 190-197.
25. Ikaha, R., and Gentleman, R. (1996) A language for data analysis and graphics. J Comp Graph Stat 5: 299-314.
26. Jean-Baptiste, N., Benjamin, D.K., Cohen-Wolkowiez, M., Fowler, V.G., Laughon, M., Clark, R.H., etal. (2011) Coagulase-negative staphylococcal infections in the neonatal intensive care unit. Infect Control Hosp Epidemiol 32: 679-686.
27. Keane, T.M., Goodstadt, L., Danecek, P., White, M.A., Wong, K., Yalcin, B., etal. (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477: 289-294.
28. von Köckritz-Blickwede, M., Rohde, M., Oehmcke, S., Miller, L.S., Cheung, A.L., Herwald, H., etal. (2008) Immunological mechanisms underlying the genetic predisposition to severe Staphylococcus aureus infection in the mouse model. Am J Pathol 173: 1657-1668.
29. Kolbe, D. (2009) Local RNA structure alignment with incomplete sequence. Bioinformatics 25: 1236-1243.
30. Lai, Y., Cogen, A.L., Radek, K.A., Park, H.J., MacLeod, D.T., Leichtle, A., etal. (2010) Activation of TLR2 by a small molecule produced by Staphylococcus epidermidis increases antimicrobial defense against bacterial skin infections. J Invest Dermatol 130: 2211-2221.
31. Lande, R., Gregorio, J., Facchinetti, V., Chatterjee, B., Wang, Y.-H., Homey, B., etal. (2007) Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 449: 564-569.
32. Ley, R.E., Bäckhed, F., Turnbaugh, P., Lozupone, C.A., Knight, R.D., and Gordon, J.I. (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102: 11070-11075.
33. Ley, R.E., Peterson, D.A., and Gordon, J.I. (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124: 837-848.
34. Ley, R.E., Hamady, M., Lozupone, C., Turnbaugh, P.J., Ramey, R.R., Bircher, J.S., etal. (2008) Evolution of mammals and their gut microbes. Science 320: 1647-1651.
35. Li, M., Cha, D.J., Lai, Y., Villaruz, A.E., Sturdevant, D.E., and Otto, M., (2007) The antimicrobial peptide-sensing system aps of Staphylococcus aureus. Mol Microbiol 66: 1136-1147.
36. Li, W., and Godzik, A. (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
37. Lilliefors, H. (1967) On the Kolmogorov-Smirnov test for normality with mean and variance unknown. J Am Stat Assoc 62: 399-402.
38. Line, J.E., Svetoch, E.A., Eruslanov, B.V., Perelygin, V.V., Mitsevich, E.V., Mitsevich, I.P., etal. (2008) Isolation and purification of enterocin E-760 with broad antimicrobial activity against gram-positive and gram-negative bacteria. Antimicrob Agents Chemother 52: 1094-1100.
39. Maidak, B., Cole, J., and Lilburn, T. (2001) The RDP-II (ribosomal database project). Nucleic Acids Res 29: 173-174.
40. Martineau, F., Picard, F.J., Ke, D., Paradis, S., Roy, P.H., Ouellette, M., etal. (2001) Development of a PCR assay for identification of staphylococci at genus and species levels. J Clin Microbiol 39: 2541-2547.
41. Mehta, P., Goyal, S., Long, T., Bassler, B.L., Wingreen, N.S., (2009) Information processing and signal integration in bacterial quorum sensing. Mol Syst Biol 5: 325.
42. Morot-Bizot, S.C., Talon, R., and Leroy, S. (2004) Development of a multiplex PCR for the identification of Staphylococcus genus and four staphylococcal species isolated from food. J Appl Microbiol 97: 1087-1094.
43. Mouse Genome Sequencing Consortium, Waterston, R.H., Lindblad-Toh, K., Birney, E., Rogers, J., Abril, J.F., etal. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562.
44. Moya, A., Peretó, J., Gil, R., Latorre, A. (2008) Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 9: 218-229.
45. Nawrocki, E.P., Kolbe, D.L., and Eddy, S.R. (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25: 1335-1337.
46. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., O'Hara, R.B., Simpson, G.L., etal. (2011) Vegan: community ecology package. R package version 1.17-10. Available at:.
47. Otto, M. (2001) Staphylococcus aureus and Staphylococcus epidermidis peptide pheromones produced by the accessory gene regulator agr system. Peptides 22: 1603-1608.
48. Otto, M. (2009) Staphylococcus epidermidis - the 'accidental' pathogen. Nat Rev Microbiol 7: 555-567.
49. Otto, M., Echner, H., Voelter, W., and Götz, F. (2001) Pheromone cross-inhibition between Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 69: 1957-1960.
50. Peschel, A., Otto, M., Jack, R.W., Kalbacher, H., Jung, G., and Götz, F. (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274: 8405-8410.
51. Peschel, A., Jack, R.W., Otto, M., Collins, L.V., Staubitz, P., Nicholson, G., etal. (2001) Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with l-lysine. J Exp Med 193: 1067-1076.
52. Posada, D. (2008) jModelTest: Phylogenetic Model Averaging. Mol Biol Evol 25: 1253-1256.
53. Rodrigue, L., and Lavoie, M.C. (1996) Comparison of the proportions of oral bacterial species in BALB/c mice from different suppliers. Lab Anim 30: 108-113.
54. Rodríguez, F., Oliver, J.L., Marín, A., and Medina, J.R. (1990) The general stochastic model of nucleotide substitution. J Theor Biol 142: 485-501.
55. Rosenthal, M., Goldberg, D., Aiello, A., Larson, E., Foxman, B. (2011) Skin microbiota: microbial community structure and its potential association with health and disease. Infect Genet Evol 11: 839-848.
56. Roth, R.R., and James, W.D. (1988) Microbial ecology of the skin. Annu Rev Microbiol 42: 441-464.
57. Sandiford, S., and Upton, M. (2012) Identification, characterization, and recombinant expression of epidermicin NI01, a novel unmodified bacteriocin produced by Staphylococcus epidermidis that displays potent activity against Staphylococci. Antimicrob Agents Chemother 56: 1539-1547.
58. Scharschmidt, T.C., List, K., Grice, E.A., Szabo, R., Renaud, G., Lee, C.-C.R., etal. (2009) Matriptase-deficient mice exhibit ichthyotic skin with a selective shift in skin microbiota. J Invest Dermatol 129: 2435-2442.
59. Stamatakis, A., Ludwig, T., and Meier, H. (2005) RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21: 456-463.
60. Stiller, M., Knapp, M., Stenzel, U., Hofreiter, M., Meyer, M., (2009) Direct multiplex sequencing (DMPS) - a novel method for targeted high-throughput sequencing of ancient and highly degraded DNA. Genome Res 19: 1843-1848.
61. Sun, C., Mathur, P., Dupuis, J., Tizard, R., Ticho, B., Crowell, T., etal. (2006) Peptidoglycan recognition proteins Pglyrp3 and Pglyrp4 are encoded from the epidermal differentiation complex and are candidate genes for the Psors4 locus on chromosome 1q21. Hum Genet 119: 113-125.
62. Turnbaugh, P.J., Ley, R.E., Hamady, M., Fraser-Liggett, C.M., Knight, R., and Gordon, J.I. (2007) The human microbiome project. Nature 449: 804-810.
63. Uçkay, I., Pittet, D., Vaudaux, P., Sax, H., Lew, D., Waldvogel, F. (2009) Foreign body infections due to Staphylococcus epidermidis. Ann Med 41: 109-119.
64. Wang, Q., Garrity, G.M., Tiedje, J.M., and Cole, J.R. (2007) Naive Bayesian classifier for rapid assignment of rrna sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.