Isolation and Characterization of Bacteria Resistant to Metallic Copper Surfaces

Christophe Espírito Santo; Paula Vasconcelos Morais; Gregor Grass

doi:10.1128/AEM.01952-09

DOI: 10.1128/AEM.01952-09

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FIG. 1.
Relative abundances of bacteria isolated from copper coins and their resistance to metallic copper surfaces. The relative abundances of 294 bacterial strains isolated from European copper coins at time zero and the relative abundances of copper surface-resistant isolates after exposure to experimental pure metallic copper surfaces for 1, 2, and 7 days are shown.

TABLE 1.

Strains isolated from copper coins

Species	Family	No. of isolates	No. of isolates surviving at day:
Species	Family	No. of isolates	1	2	7
Brachybacterium conglomeratum	Dermabacteraceae	2	1	1	1
Dermacoccus nishinomiyaensis		2	0	0	0
Agrococcus jenensis	Microbacteriaceae	1	0	0	0
Curtobacterium flaccumfaciens		2	0	0	0
Frigoribacterium faeni		1	0	0	0
Microbacterium insulae, Microbacterium lacticum, Microbacterium oxydans, Microbacterium ulmi		4	1	0	0
Micrococcus luteus, Micrococcus lylae	Micrococcaceae	59	23	8	5
Pseudoclavibacter helvolus		1	1	0	0
Arthrobacter chlorophenolicus, Arthrobacter oxydans		2	0	0	0
Kocuria marina, Kocuria palustris, Kocuria rhizophila, Kocuria sp.		10	4	1	0
Aeromicrobium sp.	Nocardioidaceae	1	0	0	0
Propioniferax innocua	Propionibacteriaceae	1	0	0	0
Bacillus anthracis, Bacillus benzoevorans, Bacillus cereus, Bacillus circulans, Bacillus insolitus, Bacillus licheniformis, Bacillus macroides, Bacillus megaterium, Bacillus mycoides, Bacillus nealsonii, Bacillus phychrodurans, Bacillus pumilus, Bacillus silvestris, Bacillus simplex, Bacillus sp., Bacillus thuringiensis, Bacillus weihenstephanensis	Bacillaceae	50	0	0	0
Paenibacillus cineris, Paenibacillus favisporus, Paenibacillus rhizosphaerae	Paenibacillaceae	1	0	0	0
Lysinibacillus fusiformis, Lysinibacillus sphaericus	Planococcaceae	1	1	0	0
Staphylococcus capitis, Staphylococcus equorum, Staphylococcus epidermidis, Staphylococcus haemolyticus, Staphylococcus hominis, Staphylococcus lugdunensis, Staphylococcus pasteuri, Staphylococcus sp., Staphylococcus vitulinus, Staphylococcus warneri	Staphylococcaceae	115	27	11	0
Leuconostoc citreum	Leuconostocaceae	2	1	0	0
Brevundimonas bullata	Caulobacteraceae	4	0	0	0
Roseomonas pecunia	Acetobacteraceae	1	0	0	0
Sphingomonas panni, Sphingomonas sp.	Sphingomonadaceae	2	1	1	0
Cupriavidus metallidurans	Burkholderiaceae	1	0	0	0
Massilia aurea, Massilia timonae	Oxalobacteraceae	2	0	0	0
Enterobacter cowanii	Enterobacteriaceae	1	1	0	0
Erwinia persicina		1	1	0	0
Pantoea agglomerans, Pantoea ananatis, Pantoea stewartii, Pantoea vagans		13	5	0	0
Acinetobacter iwoffii, Acinetobacter johnsonii, Acinetobacter ursingii	Moraxellaceae	4	1	0	0
Moraxella osloensis		2	1	0	0
Psychrobacter faecalis		3	1	0	0
Pseudomonas asplenii, Pseudomonas fragi, Pseudomonas oleovorans, Pseudomonas putida	Pseudomonadaceae	5	1	1	0
Stenotrophomonas maltophilia	Xanthomonadaceae	1	0	0	0

TABLE 2.

Resistance of representative copper coin isolates to dry or moist copper surfaces and ionic copper

Type or control strain or coin isolate^a	Survival time on:		MIC (mM CuCl₂)
Type or control strain or coin isolate^a	Dry copper surfaces	Moist copper surfaces	MIC (mM CuCl₂)
Escherichia coli W3110^b	>30 s	>1 h	3.5
Pantoea stewartii DSM 30176	>30 s	>48 h	1.5
P. stewartii L10	>24 h	>1 h	4.5
Acinetobacter johnsonii DSM 6963	>1 min	>1 h	2.5
A. johnsonii L18	>24 h	>1 h	3.0
Pseudomonas oleovorans DSM 1045	>30 s	>1 h	2.5
P. oleovorans L19	>48 h	>24 h	3.5
Sphingomonas panni DSM 15761	>48 h	>48 h	2.0
S. panni R65P	>48 h	>1 h	0.75
Staphylococcus haemolyticus DSM 20263	>1 h	>3 h	3.5
S. haemolyticus L70	>48 h	>3 h	2.0
Staphylococcus epidermidis DSM 20044	>1 h	>1 h	1.0
S. epidermidis L77	>24 h	>24 h	1.5
Staphylococcus warnerii DSM 20316	>1 min	>1 h	2.5
S. warnerii L47	>48 h	>24 h	2.0
Brachybacterium conglomeratum DSM 10241	>10 min	>1 h	0.5
B. conglomeratum N96	>7 days	>1 h	0.5
Micrococcus luteus DSM 20030	>3 h	>24 h	2.0
M. luteus L51	>48 h	>3 h	1.5
Kocuria marina JCM 13363	>48 h	>1 h	2.0
K. marina L73	>24 h	>24 h	2.0
K. palustris R40	>48 h	>1 h	0.75

↵ a In each group, the first strain is a type or control strain and the second and/or third strain is a coin isolate.
↵ b Lab strain of E. coli, included as an example of a copper-sensitive bacterium.

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Supplemental file 1 - Antibiotics used for the BioMérieux antibiotic disk assay (Table S1) and resistances of staphylococcal copper coin isolates to antibiotics in the BioMérieux antibiotic disk assay (Table S2).
MS Word document, 352K.