Antibacterial Activity and Characterization of Bacteria Isolated from Diverse Types of Greek Honey against Nosocomial and Foodborne Pathogens
Abstract
:1. Introduction
2. Materials and Methods
2.1. Honey Samples
2.2. Bacterial Isolation
2.3. Pathogenic Bacterial Strains
2.4. Dual Culture Overlay Assay
2.5. Grouping and Identification of Bacteria Exerting Antibacterial Activity
2.6. NRPS and PKS Gene Screening
3. Results
3.1. Isolation of Bacteria from Honey
3.2. Antimicrobial Activity of Bacterial Isolates
3.3. Grouping and Identification of Bacterial Isolates Exerting Antibacterial Activity
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Sample No | S. aureus1 | P. aeruginosa1 | S. Typhimurium 1 | A. baumannii1 | C. freundii1 | 1/5 2 | 2/5 2 | 3/5 2 | 4/5 2 | 5/5 2 | Total | % |
---|---|---|---|---|---|---|---|---|---|---|---|---|
1 | 25 | 23 | 26 | 6 | 25 | 23 | 17 | 12 | 3 | - | 55/127 | 43.3 |
2 | 8 | 7 | 5 | 7 | 8 | 11 | 6 | 4 | - | - | 21/77 | 27.3 |
3 | 17 | 9 | 7 | 10 | 12 | 19 | 10 | 4 | 1 | - | 34/118 | 28.8 |
4 | 33 | 19 | 11 | 23 | 22 | 26 | 14 | 14 | 3 | - | 57/112 | 50.9 |
5 | 18 | 8 | 9 | 9 | 12 | 15 | 10 | 4 | 1 | 1 | 31/90 | 34.4 |
6 | 17 | 8 | 3 | 4 | 5 | 12 | 8 | 3 | - | - | 23/70 | 32.9 |
7 | 15 | 15 | 8 | 11 | 18 | 24 | 12 | 5 | 1 | - | 42/117 | 35.9 |
8 | 5 | 5 | 7 | 8 | 7 | 7 | 9 | 1 | 1 | - | 18/62 | 29.0 |
9 | 8 | 3 | 1 | 4 | 4 | 12 | 4 | - | - | - | 16/81 | 19.8 |
10 | 13 | 6 | 11 | 5 | 5 | 17 | 6 | 2 | - | 1 | 26/83 | 31.3 |
11 | 8 | 5 | 4 | 10 | 6 | 9 | 6 | 1 | 1 | 1 | 18/56 | 32.1 |
12 | 7 | 4 | 4 | 3 | 6 | 6 | 2 | 2 | 2 | - | 12/41 | 29.3 |
13 | 18 | 7 | 9 | 11 | 14 | 22 | 5 | 6 | 1 | 1 | 35/112 | 31.3 |
14 | 35 | 15 | 19 | 25 | 27 | 51 | 22 | 6 | 2 | - | 81/190 | 42.6 |
15 | 4 | 3 | 5 | 5 | 4 | - | - | 2 | - | 3 | 5/19 | 26.3 |
16 | 3 | 2 | 3 | 2 | 2 | - | 2 | 1 | - | 1 | 4/30 | 13.3 |
17 | 1 | 1 | 1 | 2 | - | - | 1 | 1 | - | - | 2/27 | 7.4 |
18 | 6 | 7 | 7 | 8 | 6 | 3 | 1 | 2 | 2 | 3 | 11/38 | 28.9 |
19 | 1 | 1 | - | 1 | - | - | - | 1 | - | - | 1/7 | 14.3 |
20 | 2 | 3 | 2 | 3 | 1 | - | - | 1 | 2 | - | 3/20 | 15.0 |
21 | 3 | 7 | 8 | 9 | 4 | - | 6 | 5 | 1 | - | 12/38 | 31.6 |
22 | 2 | 2 | 2 | 2 | 1 | - | 1 | 1 | 1 | - | 3/24 | 12.5 |
23 | 3 | 3 | 3 | 2 | 4 | 1 | 1 | 4 | - | - | 6/9 | 66.7 |
24 | 3 | 3 | 3 | 1 | 3 | 4 | 1 | 1 | 1 | - | 7/36 | 19.4 |
25 | - | - | - | - | - | - | - | - | - | - | 0/22 | 0,0 |
26 | 11 | 5 | - | 2 | 2 | 9 | 4 | 1 | - | - | 14/40 | 35.0 |
27 | 2 | 2 | 1 | 1 | 2 | 5 | - | 1 | - | - | 6/43 | 14.0 |
28 | - | 1 | - | - | - | 1 | - | - | - | - | 1/28 | 3.6 |
29 | 17 | 17 | 15 | 22 | 13 | 2 | 4 | 7 | 7 | 5 | 25/57 | 43.9 |
30 | 5 | 2 | 1 | 1 | 2 | 2 | 3 | 1 | - | - | 6/42 | 14.3 |
31 | - | - | - | 1 | 1 | - | 1 | - | - | - | 1/29 | 3.4 |
32 | 1 | 2 | 3 | 5 | 3 | 2 | - | 1 | 1 | 1 | 5/34 | 14.7 |
33 | 2 | 4 | 1 | 5 | 3 | 2 | 2 | 3 | - | - | 7/37 | 18.9 |
34 | 1 | 1 | 1 | 1 | 1 | - | - | - | - | 1 | 1/1 | 100 |
35 | 3 | 5 | 4 | 3 | 4 | 4 | 1 | - | 2 | 1 | 8/10 | 80.0 |
36 | 2 | 4 | 3 | 2 | 3 | 1 | - | 3 | 1 | - | 5/17 | 29.4 |
37 | - | - | 1 | - | 1 | - | 1 | - | - | - | 1/1 | 100 |
38 | 1 | 1 | 1 | 1 | - | - | - | - | 1 | - | 1/2 | 50.0 |
39 | - | 1 | - | - | - | 1 | - | - | - | - | 1/4 | 25.0 |
40 | 1 | - | - | - | - | 1 | - | - | - | - | 1/2 | 50.0 |
41 | 10 | 10 | 8 | 6 | 9 | 1 | 5 | 5 | 3 | 1 | 15/17 | 88.2 |
42 | - | - | - | - | - | - | - | - | - | - | 0/0 | - |
43 | 1 | - | - | 2 | - | 3 | - | - | - | - | 3/27 | 11.1 |
44 | - | - | - | - | - | - | - | - | - | - | 0/1 | 0.0 |
45 | 11 | 4 | 9 | 2 | 9 | - | 2 | 6 | 2 | 1 | 11/14 | 78.6 |
46 | - | - | - | - | - | - | - | - | - | - | 0/2 | 0.0 |
Total | 323 | 225 | 206 | 225 | 249 | 296 | 167 | 111 | 40 | 21 | 635/2014 | |
Total % | 14.7 | 8.3 | 5.5 | 1.99 | 1.04 | 31.5 |
Group | Strain | bp | % Identity | Antibacterial Activity 1 | Bacteria | Accession Number | NRPS | PKS |
---|---|---|---|---|---|---|---|---|
A | CTA1 | 1381 | 100 | 1,2,3,4,5 | B. pumilus | MW700012 | + * | - |
CTA2 | 1395 | 100 | 1,2,3,4,5 | B.pumilus | MW700013 | + | - | |
CTA15 | 1376 | 100 | 2,3,5 | B.pumilus | MW700019 | + | - | |
CTA16 | 1389 | 99.6 | 2,3,5 | B.vallismortis | MW700020 | + | + * | |
CTA31 | 1347 | 100 | 1,2,5 | Bacillus sp. (B. aerius/B. altitudinis/ B. aerophilus/B. stratosphericus) | MW700025 | + | - | |
CTA57 | 1385 | 100 | 2,3,4 | B.safensis | MW700028 | + | + | |
CTA146 | 1419 | 100 | 4,5 | B.safensis | MW700038 | - | + | |
CTA163 | 1311 | 99.9 | 3,5 | B.licheniformis | MW700039 | + * | - | |
CTB7 | 1400 | 100 | 1,2,3,4,5 | B.safensis | MW700041 | - | + | |
CTB16 | 1403 | 100 | 1,2,3,4,5 | B.safensis | MW700043 | + | - | |
CTB21 | 1300 | 100 | 1,2,3,4 | B.pumilus | MW700044 | + | - | |
CTB26 | 1340 | 99.9 | 1,2,4,5 | B.pumilus | MW700045 | - | - | |
CTB31 | 1094 | 99.9 | 1,3,4,5 | Bacillus sp. (B. amyloliquefaciens/B. velezensis) | MW700046 | + | + * | |
CTB43 | 1403 | 100 | 2,3,4 | B.safensis | MW700049 | + | + | |
CTB89 | 1132 | 100 | 1,5 | B.safensis | MW700053 | + | + | |
CTB120 | 1369 | 100 | 3,4 | B.safensis | MW700057 | + | - | |
B | CTA5 | 1396 | 99.9 | 1,2,3,5 | B.subtilis | MW700014 | + | + * |
CTA9 | 1384 | 100 | 2,3,4,5 | B.subtilis | MW700016 | + | + * | |
CTA10 | 1373 | 100 | 2,3,4,5 | B.subtilis | MW700017 | + * | + * | |
CTA14 | 681 | 99.6 | 2,3,5 | Bacillus sp. (B. haynesii/B. piscis/ B. paralicheniformis/B. licheniformis) | MW700018 | + * | - | |
CTA20 | 1410 | 100 | 1,3,5 | B. subtilis | MW700021 | + * | + * | |
CTA109 | 1414 | 99.9 | 2,5 | Bacillus sp. (B. halotolerans/B. mojavensis) | MW700035 | - | + * | |
CTB11 | 1281 | 99.6 | 1,2,3,4,5 | Bacillus sp. (B. subtilis subsp. Inaquosorum/ B. nakamurai/B. mojavensis/ B. halotolerans) | MW700042 | - | + * | |
C | CTA7 | 1401 | 99.9 | 1,3,4,5 | P. megaterium (B. megaterium) | MW700015 | + * | - |
CTA28 | 1401 | 100 | 1,2,4 | B.paramycoides | MW700024 | + | - | |
CTA46 | 1413 | 99.9 | 3,4,5 | Bacillus sp. (B. proteolyticus/B. wiedmannii) | MW700027 | + * | + | |
CTB34 | 1414 | 99.9 | 1,2,3,5 | B.cereus | MW700048 | - | - | |
CTB116 | 1405 | 100 | 2,5 | B.cereus | MW700056 | - | - | |
F | CTA39 | 1349 | 99.9 | 3,4,5 | S. pasteuri | MW700026 | - | - |
CTA79 | 1370 | 99.9 | 1,5 | S.cohnii | MW700029 | - | - | |
CTB46 | 1411 | 99.9 | 1,2,4 | S.cohnii | MW700050 | - | + | |
G | CTA107 | 897 | 100 | 2,5 | P. stutzeri | MW700034 | - | - |
CT110 | 1322 | 100 | 2,4 | A. lwoffii | MW700055 | - | - | |
H | CTA23 | 1375 | 99.8 | 2,4,5 | P. fulva | MW700022 | + * | - |
CTA90 | 708 | 99.9 | 1,3 | Pseudomonas sp. (P. putida/P.fulva/P.parafulva/ P. guariconensis/P. plecoglossicida/ P. cremoricolorata/P. taiwanensis/ P. donghuensis/P.wadenswilerensis/ P. alkylphenolica) | MW700031 | + * | + | |
I | CTA125 | 1436 | 98.9 | 1,2 | Bacillus sp. | MW700036 | - | + * |
J | CTA25 | 1371 | 99.9 | 2,4,5 | Terribacillus sp. (T. goriensis/T. saccharophylus) | MW700023 | - | - |
K | CTA84 | 1278 | 99.8 | 2,3 | P.coleopterorum | MW700030 | - | - |
L | CTA95 | 1333 | 99.9 | 1,3 | M. imperiale | MW700032 | + * | - |
M | CTA99 | 1349 | 100 | 1,3 | Bacillus sp. (B. proteolyticus/B. wiedmannii) | MW700033 | - | - |
O | CTA138 | 1405 | 99.9 | 2,4 | Bacillus sp. (B. proteolyticus/B. wiedmannii) | MW700037 | - | - |
CTB60 | 1404 | 99.9 | 3,4,5 | L. fusiformis | MW700051 | - | - | |
S | CTA169 | 496 | 99.8 | 3,5 | P. profundus | MW700040 | + * | + * |
T | CTB32 | 1382 | 99.9 | 1,2,3,5 | M. yunnanensis | MW700047 | - | - |
W | CTB93 | 1379 | 99.8 | 1,2 | T. saccharophilus | MW700054 | - | - |
Y | CTB69 | 1416 | 99.6 | 2,4,5 | Paenibacillus sp. (P. cucumis/P. polysaccharolyticus) | MW700052 | + * | + * |
LAB1 | CT2H | 440 | 99.8 | 1,2,3,4 | S. epidermidis | MW700058 | - | - |
CT7C | 580 | 100 | 3,4,5 | S. warneri | MW700060 | - | - | |
LAB2 | CT6C | 563 | 99.6 | 1,2,3,4,5 | S.arlettae | MW700059 | + | - |
LAB3 | CT12B | 432 | 99.8 | 1,2,5 | S.hominis | MW700061 | - | - |
Sample | Species | BLASTN | % Identity | BLASTX | % Identity |
---|---|---|---|---|---|
A1 | B. pumilus | P. monteilii (AMA45849.1 hypothetical protein) | 84.4 | amino acid adenylation domain-containing protein (P. monteilii) | 78.7 |
A7 | P. megaterium | P. monteilii (Gene APT63_12835, AMA46431.1 hypothetical protein) | 67.2 | NRPS (P. monteilii) | 41.7 |
A10 | B. subtilis | B. subtilis strain JCL16 chromosome (Gene srfAA), QKJ76470.1 surfactin NRPS SrfAA | 84.2 | Surfactin NRPS SrfAA (B. subtilis) | 72.7 |
A14 | Bacillus sp. | B. licheniformis strain P8_B2 chromosome, QGI45530.1 D-alanine--poly(phosphoribitol) ligase subunit DltA | 95.9 | D-alanine--poly(phosphoribitol) ligase subunit DltA (B. licheniformis) | 91.1 |
A20 | B. subtilis | B. subtilis subsp. subtilis str. 168 chromosome (QJR44804.1 surfactin NRPS SrfAA | 98.1 | surfactin NRPS SrfAA (B. subtilis) | 98.6 |
A23 | P. fulva | P. monteilii strain USDA-ARS-USMARC-56711 (Gene APT63_09540, AMA45849.1, hypothetical protein | 96.5 | amino acid adenylation domain-containing protein (P. monteilii) | 98.4 |
A46 | Bacillus sp. | B. safensis strain PgKB20 chromosome Surfactin synthase subunit 2 (gene srfAB_2) | 96.5 | NRPS (B. safensis) | 99.49 |
A90.2 | Pseudomonas sp. | P. monteilii strain USDA-ARS-USMARC-56711, gene APT63_09540, hypothetical protein | 91.8 | amino acid adenylation domain-containing protein (P. monteilii) | 87.7 |
A95 | M. imperiale | M. oleivorans strain I46 chromosome DNA gyrase subunit A | 68.1 | no | no |
A163 | B. licheniformis | B. haynesii strain P19 chromosome | 73.2 | no | no |
A169 | P. profundus | P. thiaminolyticus strain NRRL B-4156 amino acid adenylation domain-containing protein FLT43_25335 | 71.8 | NRPS/PKS (P. apiarius) | 56.5 |
B69 | Paenibacillus sp. | P. polymyxa E681 isolate type B chromosome Linear gramicidin synthase subunit B, lgrB_2 | 83.5 | AMP-binding protein (P. amylolyticus) | 96.6 |
Sample | Species | BLASTN | % Identity | BLASTX | % Identity |
---|---|---|---|---|---|
A5 | B. subtilis | B. subtilis subsp. subtilis str. 168 chromosome amino acid adenylation domain-containing protein, HIR77_09320 | 81.8 | ketosynthase, partial (Bacillus sp.) | 82.7 |
A9 | B. subtilis | B. subtilis subsp. subtilis strain UCMB5021 Malonyl CoA-acyl carrier protein PksN transacylase involved in nonribosomal synthesis of bacillaene, gene pksN | 77.1 | ketosynthase, partial (Bacillus sp.) | 76.1 |
A10 | B. subtilis | B. subtilis strain JCL16 chromosome, amino acid adenylation domain-containing protein, gene HR084_09185 | 78.9 | ketosynthase, partial (Bacillus sp.) | 78.2 |
A16 | B. vallismortis | B. amyloliquefaciens strain R8-25 chromosome (or valezensis) amino acid adenylation domain-containing protein, gene HT132_11940 | 76.4 | amino acid adenylation domain-containing protein (B. amyloliquefaciens) | 93.2 |
A20 | B. subtilis | B. subtilis subsp. subtilis str. 168 chromosome, amino acid adenylation domain-containing protein, gene HIR77_09320 | 85.7 | ketosynthase, partial (Bacillus sp.) | 87.86 |
A109 | Bacillus sp. | P. thiaminolyticus strain NRRL B-4156 chromosome acyltransferase domain-containing protein, gene FLT43_06730 | 81.2 | acyltransferase domain-containing protein (P. apiaries) | 100 |
A125 | Bacillus sp. | B. subtilis strain JCL16 chromosome amino acid adenylation domain-containing protein, gene HR084_09185 | 79.2 | ketosynthase, partial (Bacillus sp.) | 77.7 |
A169 | P. profundus | P. thiaminolyticus strain NRRL B-4156 chromosome acyltransferase domain-containing protein, gene FLT43_06730 | 81.1 | acyltransferase domain-containing protein (P. apiarius) | 100 |
B11 | Bacillus sp. | B. halotolerans strain KKD1 chromosome NRPS, gene HT135_09465 | 99 | type I ketosynthase (Bacillus sp. LX-99) | 97.4 |
B31 | Bacillus sp. | Bacillus sp. AM1(2019) chromosome zinc-binding dehydrogenase, gene GNE05_12430 | 72.9 | PKS (B. velezensis) | 60 |
B69 | Paenibacillus sp. | Paenibacillus sp. B37 PKS gene, PKS | 94.2 | PKS (Paenibacillus sp. B15) | 98.5 |
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Tsadila, C.; Nikolaidis, M.; Dimitriou, T.G.; Kafantaris, I.; Amoutzias, G.D.; Pournaras, S.; Mossialos, D. Antibacterial Activity and Characterization of Bacteria Isolated from Diverse Types of Greek Honey against Nosocomial and Foodborne Pathogens. Appl. Sci. 2021, 11, 5801. https://doi.org/10.3390/app11135801
Tsadila C, Nikolaidis M, Dimitriou TG, Kafantaris I, Amoutzias GD, Pournaras S, Mossialos D. Antibacterial Activity and Characterization of Bacteria Isolated from Diverse Types of Greek Honey against Nosocomial and Foodborne Pathogens. Applied Sciences. 2021; 11(13):5801. https://doi.org/10.3390/app11135801
Chicago/Turabian StyleTsadila, Christina, Marios Nikolaidis, Tilemachos G. Dimitriou, Ioannis Kafantaris, Grigoris D. Amoutzias, Spyros Pournaras, and Dimitris Mossialos. 2021. "Antibacterial Activity and Characterization of Bacteria Isolated from Diverse Types of Greek Honey against Nosocomial and Foodborne Pathogens" Applied Sciences 11, no. 13: 5801. https://doi.org/10.3390/app11135801
APA StyleTsadila, C., Nikolaidis, M., Dimitriou, T. G., Kafantaris, I., Amoutzias, G. D., Pournaras, S., & Mossialos, D. (2021). Antibacterial Activity and Characterization of Bacteria Isolated from Diverse Types of Greek Honey against Nosocomial and Foodborne Pathogens. Applied Sciences, 11(13), 5801. https://doi.org/10.3390/app11135801