Abstract

The potential use of a novel multichannel optical system towards fast and non-destructive bacteria identification and its application for environmental bacteria characterisation on the strain level is presented. It is the first attempt to use the proposed optical method to study various bacteria species (Gram-negative, Gram-positive) commonly present in the environment. The novel configuration of the optical system enables multichannel examination of bacterial colonies and provides additional functionality such as registration of two-dimensional (2D) distribution of monochromatic transmission coefficient of examined colonies, what can be used as a novel optical signature for bacteria characterization. Performed statistical analysis indicates that it is possible to identify representatives of environmental soil bacteria on the species level with the 98.51% accuracy and in case of two strains of Rahnella aquatilis bacteria on the strain level with the 98.8% accuracy. The proposed method is an alternative to the currently used preliminary bacteria examination in environment safety control with the advantage of being fast, reliable, non-destructive and requiring minimal sample preparation.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2017 (1)

H. Kim, B. Rajwa, A. K. Bhunia, J. P. Robinson, and E. Bae, “Development of a multispectral light-scatter sensor for bacterial colonies,” J. Biophotonics 10(5), 634–644 (2017).
[Crossref] [PubMed]

2016 (1)

I. Buzalewicz, M. Kujawińska, W. Krauze, and H. Podbielska, “Novel perspectives on the characterization of species-dependent optical signatures of bacterial colonies by digital holography,” PLoS One 11(3), e0150449 (2016).
[Crossref] [PubMed]

2015 (2)

U. Minoni, A. Signoroni, and G. Nassini, “On the application of optical forward-scattering to bacterial identification in an automated clinical analysis perspective,” Biosens. Bioelectron. 68, 536–543 (2015).
[Crossref] [PubMed]

S. W. Wessel, H. C. van der Mei, D. Morando, A. M. Slomp, B. van de Belt-Gritter, A. Maitra, and H. J. Busscher, “Quantification and qualification of bacteria trapped in chewed gum,” PLoS One 10(1), e0117191 (2015).
[Crossref] [PubMed]

2014 (3)

Y. Tang, H. Kim, A. K. Singh, A. Aroonnual, E. Bae, B. Rajwa, P. M. Fratamico, and A. K. Bhunia, “Light scattering sensor for direct identification of colonies of Escherichia coli serogroups O26, O45, O103, O111, O121, O145 and O157,” PLoS One 9(8), e105272 (2014).
[Crossref] [PubMed]

P. R. Marcoux, M. Dupoy, A. Cuer, J. L. Kodja, A. Lefebvre, F. Licari, R. Louvet, A. Narassiguin, and F. Mallard, “Optical forward-scattering for identification of bacteria within microcolonies,” Appl. Microbiol. Biotechnol. 98(5), 2243–2254 (2014).
[Crossref] [PubMed]

A. Suchwałko, I. Buzalewicz, and H. Podbielska, “Bacteria identification in an optical system with optimized diffraction pattern registration condition supported by enhanced statistical analysis,” Opt. Express 22(21), 26312–26327 (2014).
[Crossref] [PubMed]

2013 (5)

A. Suchwalko, I. Buzalewicz, A. Wieliczko, and H. Podbielska, “Bacteria species identification by the statistical analysis of bacterial colonies Fresnel patterns,” Opt. Express 21(9), 11322–11337 (2013).
[Crossref] [PubMed]

I. Buzalewicz, K. Liżewski, M. Kujawińska, and H. Podbielska, “Degeneration of Fraunhofer diffraction on bacterial colonies due to their light focusing properties examined in the digital holographic microscope system,” Opt. Express 21(22), 26493–26505 (2013).
[Crossref] [PubMed]

H. Kim, N. Bai, A. K. Bhunia, G. B. King, E. D. Hirleman, and E. Bae, “Development of an integrated optical analyzer for characterization of growth dynamics of bacterial colonies,” J. Biophotonics 6(11-12), 929–937 (2013).
[Crossref] [PubMed]

D. I. Cattoni, J.-B. Fiche, A. Valeri, T. Mignot, and M. Nöllmann, “Super-resolution imaging of bacteria in a microfluidics device,” PLoS One 8(10), e76268 (2013).
[Crossref] [PubMed]

L. R. Dartnell, T. A. Roberts, G. Moore, J. M. Ward, and J.-P. Muller, “Fluorescence characterization of clinically-important bacteria,” PLoS One 8(9), e75270 (2013).
[Crossref] [PubMed]

2012 (3)

D. Ziegler, A. Mariotti, V. Pflüger, M. Saad, G. Vogel, M. Tonolla, and X. Perret, “In situ identification of plant-invasive bacteria with MALDI-TOF mass spectrometry,” PLoS One 7(5), e37189 (2012).
[Crossref] [PubMed]

E. Bae, D. Ying, D. Kramer, V. Patsekin, B. Rajwa, C. Holdman, J. Sturgis, V. J. Davisson, and J. P. Robinson, “Portable bacterial identification system based on elastic light scatter patterns,” J. Biol. Eng. 6(1), 12 (2012).
[Crossref] [PubMed]

A. Croxatto, G. Prod’hom, and G. Greub, “Applications of MALDI-TOF mass spectrometry in clinical diagnostic microbiology,” FEMS Microbiol. Rev. 36(2), 380–407 (2012).
[Crossref] [PubMed]

2011 (2)

J. Kok, L. C. Thomas, T. Olma, S. C. A. Chen, and J. R. Iredell, “Identification of bacteria in blood culture broths using matrix-assisted laser desorption-ionization Sepsityper™ and time of flight mass spectrometry,” PLoS One 6(8), e23285 (2011).
[Crossref] [PubMed]

I. Buzalewicz, A. Wieliczko, and H. Podbielska, “Influence of various growth conditions on Fresnel diffraction patterns of bacteria colonies examined in the optical system with converging spherical wave illumination,” Opt. Express 19(22), 21768–21785 (2011).
[Crossref] [PubMed]

2009 (1)

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

2008 (1)

S. Sauer, A. Freiwald, T. Maier, M. Kube, R. Reinhardt, M. Kostrzewa, and K. Geider, “Classification and identification of bacteria by mass spectrometry and computational analysis,” PLoS One 3(7), e2843 (2008).
[Crossref] [PubMed]

2006 (1)

B. Bayraktar, P. P. Banada, E. D. Hirleman, A. K. Bhunia, J. P. Robinson, and B. Rajwa, “Feature extraction from light-scatter patterns of Listeria colonies for identification and classification,” J. Biomed. Opt. 11(3), 034006 (2006).
[Crossref] [PubMed]

2004 (1)

M. D. Abràmoff, P. J. Magalhães, and S. J. Ram, “Image processing with ImageJ,” Biophoton. Int. 11(7), 36–42 (2004).

2003 (1)

J. Vessey, “Plant growth promoting rhizobacteria as biofertilizers,” Plant Soil 255(2), 571–586 (2003).
[Crossref]

2002 (1)

P. H. Janssen, P. S. Yates, B. E. Grinton, P. M. Taylor, and M. Sait, “Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia,” Appl. Environ. Microbiol. 68(5), 2391–2396 (2002).
[Crossref] [PubMed]

2001 (2)

P. Marschner, D. Crowley, and R. Lieberei, “Arbuscular mycorrhizal infection changes the bacterial 16 S rDNA community composition in the rhizosphere of maize,” Mycorrhiza 11(6), 297–302 (2001).
[Crossref] [PubMed]

P. Marschner, C.-H. Yang, R. Lieberei, and D. Crowley, “Soil and plant specific effects on bacterial community composition in the rhizosphere,” Soil Biol. Biochem. 33(11), 1437–1445 (2001).
[Crossref]

1999 (1)

C. H. Jaeger, S. E. Lindow, W. Miller, E. Clark, and M. K. Firestone, “Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan,” Appl. Environ. Microbiol. 65(6), 2685–2690 (1999).
[PubMed]

1995 (1)

R. I. Amann, W. Ludwig, and K. H. Schleifer, “Phylogenetic identification and in situ detection of individual microbial cells without cultivation,” Microbiol. Rev. 59(1), 143–169 (1995).
[PubMed]

Abràmoff, M. D.

M. D. Abràmoff, P. J. Magalhães, and S. J. Ram, “Image processing with ImageJ,” Biophoton. Int. 11(7), 36–42 (2004).

Adil, A.

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

Amann, R. I.

R. I. Amann, W. Ludwig, and K. H. Schleifer, “Phylogenetic identification and in situ detection of individual microbial cells without cultivation,” Microbiol. Rev. 59(1), 143–169 (1995).
[PubMed]

Aroonnual, A.

Y. Tang, H. Kim, A. K. Singh, A. Aroonnual, E. Bae, B. Rajwa, P. M. Fratamico, and A. K. Bhunia, “Light scattering sensor for direct identification of colonies of Escherichia coli serogroups O26, O45, O103, O111, O121, O145 and O157,” PLoS One 9(8), e105272 (2014).
[Crossref] [PubMed]

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

Bae, E.

H. Kim, B. Rajwa, A. K. Bhunia, J. P. Robinson, and E. Bae, “Development of a multispectral light-scatter sensor for bacterial colonies,” J. Biophotonics 10(5), 634–644 (2017).
[Crossref] [PubMed]

Y. Tang, H. Kim, A. K. Singh, A. Aroonnual, E. Bae, B. Rajwa, P. M. Fratamico, and A. K. Bhunia, “Light scattering sensor for direct identification of colonies of Escherichia coli serogroups O26, O45, O103, O111, O121, O145 and O157,” PLoS One 9(8), e105272 (2014).
[Crossref] [PubMed]

H. Kim, N. Bai, A. K. Bhunia, G. B. King, E. D. Hirleman, and E. Bae, “Development of an integrated optical analyzer for characterization of growth dynamics of bacterial colonies,” J. Biophotonics 6(11-12), 929–937 (2013).
[Crossref] [PubMed]

E. Bae, D. Ying, D. Kramer, V. Patsekin, B. Rajwa, C. Holdman, J. Sturgis, V. J. Davisson, and J. P. Robinson, “Portable bacterial identification system based on elastic light scatter patterns,” J. Biol. Eng. 6(1), 12 (2012).
[Crossref] [PubMed]

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

Bai, N.

H. Kim, N. Bai, A. K. Bhunia, G. B. King, E. D. Hirleman, and E. Bae, “Development of an integrated optical analyzer for characterization of growth dynamics of bacterial colonies,” J. Biophotonics 6(11-12), 929–937 (2013).
[Crossref] [PubMed]

Banada, P. P.

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

B. Bayraktar, P. P. Banada, E. D. Hirleman, A. K. Bhunia, J. P. Robinson, and B. Rajwa, “Feature extraction from light-scatter patterns of Listeria colonies for identification and classification,” J. Biomed. Opt. 11(3), 034006 (2006).
[Crossref] [PubMed]

Bayraktar, B.

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

B. Bayraktar, P. P. Banada, E. D. Hirleman, A. K. Bhunia, J. P. Robinson, and B. Rajwa, “Feature extraction from light-scatter patterns of Listeria colonies for identification and classification,” J. Biomed. Opt. 11(3), 034006 (2006).
[Crossref] [PubMed]

Bhunia, A. K.

H. Kim, B. Rajwa, A. K. Bhunia, J. P. Robinson, and E. Bae, “Development of a multispectral light-scatter sensor for bacterial colonies,” J. Biophotonics 10(5), 634–644 (2017).
[Crossref] [PubMed]

Y. Tang, H. Kim, A. K. Singh, A. Aroonnual, E. Bae, B. Rajwa, P. M. Fratamico, and A. K. Bhunia, “Light scattering sensor for direct identification of colonies of Escherichia coli serogroups O26, O45, O103, O111, O121, O145 and O157,” PLoS One 9(8), e105272 (2014).
[Crossref] [PubMed]

H. Kim, N. Bai, A. K. Bhunia, G. B. King, E. D. Hirleman, and E. Bae, “Development of an integrated optical analyzer for characterization of growth dynamics of bacterial colonies,” J. Biophotonics 6(11-12), 929–937 (2013).
[Crossref] [PubMed]

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

B. Bayraktar, P. P. Banada, E. D. Hirleman, A. K. Bhunia, J. P. Robinson, and B. Rajwa, “Feature extraction from light-scatter patterns of Listeria colonies for identification and classification,” J. Biomed. Opt. 11(3), 034006 (2006).
[Crossref] [PubMed]

Busscher, H. J.

S. W. Wessel, H. C. van der Mei, D. Morando, A. M. Slomp, B. van de Belt-Gritter, A. Maitra, and H. J. Busscher, “Quantification and qualification of bacteria trapped in chewed gum,” PLoS One 10(1), e0117191 (2015).
[Crossref] [PubMed]

Buzalewicz, I.

Cattoni, D. I.

D. I. Cattoni, J.-B. Fiche, A. Valeri, T. Mignot, and M. Nöllmann, “Super-resolution imaging of bacteria in a microfluidics device,” PLoS One 8(10), e76268 (2013).
[Crossref] [PubMed]

Chen, S. C. A.

J. Kok, L. C. Thomas, T. Olma, S. C. A. Chen, and J. R. Iredell, “Identification of bacteria in blood culture broths using matrix-assisted laser desorption-ionization Sepsityper™ and time of flight mass spectrometry,” PLoS One 6(8), e23285 (2011).
[Crossref] [PubMed]

Clark, E.

C. H. Jaeger, S. E. Lindow, W. Miller, E. Clark, and M. K. Firestone, “Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan,” Appl. Environ. Microbiol. 65(6), 2685–2690 (1999).
[PubMed]

Crowley, D.

P. Marschner, C.-H. Yang, R. Lieberei, and D. Crowley, “Soil and plant specific effects on bacterial community composition in the rhizosphere,” Soil Biol. Biochem. 33(11), 1437–1445 (2001).
[Crossref]

P. Marschner, D. Crowley, and R. Lieberei, “Arbuscular mycorrhizal infection changes the bacterial 16 S rDNA community composition in the rhizosphere of maize,” Mycorrhiza 11(6), 297–302 (2001).
[Crossref] [PubMed]

Croxatto, A.

A. Croxatto, G. Prod’hom, and G. Greub, “Applications of MALDI-TOF mass spectrometry in clinical diagnostic microbiology,” FEMS Microbiol. Rev. 36(2), 380–407 (2012).
[Crossref] [PubMed]

Cuer, A.

P. R. Marcoux, M. Dupoy, A. Cuer, J. L. Kodja, A. Lefebvre, F. Licari, R. Louvet, A. Narassiguin, and F. Mallard, “Optical forward-scattering for identification of bacteria within microcolonies,” Appl. Microbiol. Biotechnol. 98(5), 2243–2254 (2014).
[Crossref] [PubMed]

Dartnell, L. R.

L. R. Dartnell, T. A. Roberts, G. Moore, J. M. Ward, and J.-P. Muller, “Fluorescence characterization of clinically-important bacteria,” PLoS One 8(9), e75270 (2013).
[Crossref] [PubMed]

Davisson, V. J.

E. Bae, D. Ying, D. Kramer, V. Patsekin, B. Rajwa, C. Holdman, J. Sturgis, V. J. Davisson, and J. P. Robinson, “Portable bacterial identification system based on elastic light scatter patterns,” J. Biol. Eng. 6(1), 12 (2012).
[Crossref] [PubMed]

Dupoy, M.

P. R. Marcoux, M. Dupoy, A. Cuer, J. L. Kodja, A. Lefebvre, F. Licari, R. Louvet, A. Narassiguin, and F. Mallard, “Optical forward-scattering for identification of bacteria within microcolonies,” Appl. Microbiol. Biotechnol. 98(5), 2243–2254 (2014).
[Crossref] [PubMed]

Fiche, J.-B.

D. I. Cattoni, J.-B. Fiche, A. Valeri, T. Mignot, and M. Nöllmann, “Super-resolution imaging of bacteria in a microfluidics device,” PLoS One 8(10), e76268 (2013).
[Crossref] [PubMed]

Firestone, M. K.

C. H. Jaeger, S. E. Lindow, W. Miller, E. Clark, and M. K. Firestone, “Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan,” Appl. Environ. Microbiol. 65(6), 2685–2690 (1999).
[PubMed]

Fratamico, P. M.

Y. Tang, H. Kim, A. K. Singh, A. Aroonnual, E. Bae, B. Rajwa, P. M. Fratamico, and A. K. Bhunia, “Light scattering sensor for direct identification of colonies of Escherichia coli serogroups O26, O45, O103, O111, O121, O145 and O157,” PLoS One 9(8), e105272 (2014).
[Crossref] [PubMed]

Freiwald, A.

S. Sauer, A. Freiwald, T. Maier, M. Kube, R. Reinhardt, M. Kostrzewa, and K. Geider, “Classification and identification of bacteria by mass spectrometry and computational analysis,” PLoS One 3(7), e2843 (2008).
[Crossref] [PubMed]

Geider, K.

S. Sauer, A. Freiwald, T. Maier, M. Kube, R. Reinhardt, M. Kostrzewa, and K. Geider, “Classification and identification of bacteria by mass spectrometry and computational analysis,” PLoS One 3(7), e2843 (2008).
[Crossref] [PubMed]

Greub, G.

A. Croxatto, G. Prod’hom, and G. Greub, “Applications of MALDI-TOF mass spectrometry in clinical diagnostic microbiology,” FEMS Microbiol. Rev. 36(2), 380–407 (2012).
[Crossref] [PubMed]

Grinton, B. E.

P. H. Janssen, P. S. Yates, B. E. Grinton, P. M. Taylor, and M. Sait, “Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia,” Appl. Environ. Microbiol. 68(5), 2391–2396 (2002).
[Crossref] [PubMed]

Hirleman, E. D.

H. Kim, N. Bai, A. K. Bhunia, G. B. King, E. D. Hirleman, and E. Bae, “Development of an integrated optical analyzer for characterization of growth dynamics of bacterial colonies,” J. Biophotonics 6(11-12), 929–937 (2013).
[Crossref] [PubMed]

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

B. Bayraktar, P. P. Banada, E. D. Hirleman, A. K. Bhunia, J. P. Robinson, and B. Rajwa, “Feature extraction from light-scatter patterns of Listeria colonies for identification and classification,” J. Biomed. Opt. 11(3), 034006 (2006).
[Crossref] [PubMed]

Holdman, C.

E. Bae, D. Ying, D. Kramer, V. Patsekin, B. Rajwa, C. Holdman, J. Sturgis, V. J. Davisson, and J. P. Robinson, “Portable bacterial identification system based on elastic light scatter patterns,” J. Biol. Eng. 6(1), 12 (2012).
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C. J. Huberty, Applied Discriminant Analysis (1994).

Huff, K.

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

Iredell, J. R.

J. Kok, L. C. Thomas, T. Olma, S. C. A. Chen, and J. R. Iredell, “Identification of bacteria in blood culture broths using matrix-assisted laser desorption-ionization Sepsityper™ and time of flight mass spectrometry,” PLoS One 6(8), e23285 (2011).
[Crossref] [PubMed]

Jaeger, C. H.

C. H. Jaeger, S. E. Lindow, W. Miller, E. Clark, and M. K. Firestone, “Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan,” Appl. Environ. Microbiol. 65(6), 2685–2690 (1999).
[PubMed]

Janssen, P. H.

P. H. Janssen, P. S. Yates, B. E. Grinton, P. M. Taylor, and M. Sait, “Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia,” Appl. Environ. Microbiol. 68(5), 2391–2396 (2002).
[Crossref] [PubMed]

Kim, H.

H. Kim, B. Rajwa, A. K. Bhunia, J. P. Robinson, and E. Bae, “Development of a multispectral light-scatter sensor for bacterial colonies,” J. Biophotonics 10(5), 634–644 (2017).
[Crossref] [PubMed]

Y. Tang, H. Kim, A. K. Singh, A. Aroonnual, E. Bae, B. Rajwa, P. M. Fratamico, and A. K. Bhunia, “Light scattering sensor for direct identification of colonies of Escherichia coli serogroups O26, O45, O103, O111, O121, O145 and O157,” PLoS One 9(8), e105272 (2014).
[Crossref] [PubMed]

H. Kim, N. Bai, A. K. Bhunia, G. B. King, E. D. Hirleman, and E. Bae, “Development of an integrated optical analyzer for characterization of growth dynamics of bacterial colonies,” J. Biophotonics 6(11-12), 929–937 (2013).
[Crossref] [PubMed]

King, G. B.

H. Kim, N. Bai, A. K. Bhunia, G. B. King, E. D. Hirleman, and E. Bae, “Development of an integrated optical analyzer for characterization of growth dynamics of bacterial colonies,” J. Biophotonics 6(11-12), 929–937 (2013).
[Crossref] [PubMed]

Kodja, J. L.

P. R. Marcoux, M. Dupoy, A. Cuer, J. L. Kodja, A. Lefebvre, F. Licari, R. Louvet, A. Narassiguin, and F. Mallard, “Optical forward-scattering for identification of bacteria within microcolonies,” Appl. Microbiol. Biotechnol. 98(5), 2243–2254 (2014).
[Crossref] [PubMed]

Kok, J.

J. Kok, L. C. Thomas, T. Olma, S. C. A. Chen, and J. R. Iredell, “Identification of bacteria in blood culture broths using matrix-assisted laser desorption-ionization Sepsityper™ and time of flight mass spectrometry,” PLoS One 6(8), e23285 (2011).
[Crossref] [PubMed]

Kostrzewa, M.

S. Sauer, A. Freiwald, T. Maier, M. Kube, R. Reinhardt, M. Kostrzewa, and K. Geider, “Classification and identification of bacteria by mass spectrometry and computational analysis,” PLoS One 3(7), e2843 (2008).
[Crossref] [PubMed]

Kramer, D.

E. Bae, D. Ying, D. Kramer, V. Patsekin, B. Rajwa, C. Holdman, J. Sturgis, V. J. Davisson, and J. P. Robinson, “Portable bacterial identification system based on elastic light scatter patterns,” J. Biol. Eng. 6(1), 12 (2012).
[Crossref] [PubMed]

Krauze, W.

I. Buzalewicz, M. Kujawińska, W. Krauze, and H. Podbielska, “Novel perspectives on the characterization of species-dependent optical signatures of bacterial colonies by digital holography,” PLoS One 11(3), e0150449 (2016).
[Crossref] [PubMed]

Kube, M.

S. Sauer, A. Freiwald, T. Maier, M. Kube, R. Reinhardt, M. Kostrzewa, and K. Geider, “Classification and identification of bacteria by mass spectrometry and computational analysis,” PLoS One 3(7), e2843 (2008).
[Crossref] [PubMed]

Kujawinska, M.

I. Buzalewicz, M. Kujawińska, W. Krauze, and H. Podbielska, “Novel perspectives on the characterization of species-dependent optical signatures of bacterial colonies by digital holography,” PLoS One 11(3), e0150449 (2016).
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I. Buzalewicz, K. Liżewski, M. Kujawińska, and H. Podbielska, “Degeneration of Fraunhofer diffraction on bacterial colonies due to their light focusing properties examined in the digital holographic microscope system,” Opt. Express 21(22), 26493–26505 (2013).
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Lefebvre, A.

P. R. Marcoux, M. Dupoy, A. Cuer, J. L. Kodja, A. Lefebvre, F. Licari, R. Louvet, A. Narassiguin, and F. Mallard, “Optical forward-scattering for identification of bacteria within microcolonies,” Appl. Microbiol. Biotechnol. 98(5), 2243–2254 (2014).
[Crossref] [PubMed]

Licari, F.

P. R. Marcoux, M. Dupoy, A. Cuer, J. L. Kodja, A. Lefebvre, F. Licari, R. Louvet, A. Narassiguin, and F. Mallard, “Optical forward-scattering for identification of bacteria within microcolonies,” Appl. Microbiol. Biotechnol. 98(5), 2243–2254 (2014).
[Crossref] [PubMed]

Lieberei, R.

P. Marschner, D. Crowley, and R. Lieberei, “Arbuscular mycorrhizal infection changes the bacterial 16 S rDNA community composition in the rhizosphere of maize,” Mycorrhiza 11(6), 297–302 (2001).
[Crossref] [PubMed]

P. Marschner, C.-H. Yang, R. Lieberei, and D. Crowley, “Soil and plant specific effects on bacterial community composition in the rhizosphere,” Soil Biol. Biochem. 33(11), 1437–1445 (2001).
[Crossref]

Lindow, S. E.

C. H. Jaeger, S. E. Lindow, W. Miller, E. Clark, and M. K. Firestone, “Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan,” Appl. Environ. Microbiol. 65(6), 2685–2690 (1999).
[PubMed]

Lizewski, K.

Louvet, R.

P. R. Marcoux, M. Dupoy, A. Cuer, J. L. Kodja, A. Lefebvre, F. Licari, R. Louvet, A. Narassiguin, and F. Mallard, “Optical forward-scattering for identification of bacteria within microcolonies,” Appl. Microbiol. Biotechnol. 98(5), 2243–2254 (2014).
[Crossref] [PubMed]

Ludwig, W.

R. I. Amann, W. Ludwig, and K. H. Schleifer, “Phylogenetic identification and in situ detection of individual microbial cells without cultivation,” Microbiol. Rev. 59(1), 143–169 (1995).
[PubMed]

Magalhães, P. J.

M. D. Abràmoff, P. J. Magalhães, and S. J. Ram, “Image processing with ImageJ,” Biophoton. Int. 11(7), 36–42 (2004).

Maier, T.

S. Sauer, A. Freiwald, T. Maier, M. Kube, R. Reinhardt, M. Kostrzewa, and K. Geider, “Classification and identification of bacteria by mass spectrometry and computational analysis,” PLoS One 3(7), e2843 (2008).
[Crossref] [PubMed]

Maitra, A.

S. W. Wessel, H. C. van der Mei, D. Morando, A. M. Slomp, B. van de Belt-Gritter, A. Maitra, and H. J. Busscher, “Quantification and qualification of bacteria trapped in chewed gum,” PLoS One 10(1), e0117191 (2015).
[Crossref] [PubMed]

Mallard, F.

P. R. Marcoux, M. Dupoy, A. Cuer, J. L. Kodja, A. Lefebvre, F. Licari, R. Louvet, A. Narassiguin, and F. Mallard, “Optical forward-scattering for identification of bacteria within microcolonies,” Appl. Microbiol. Biotechnol. 98(5), 2243–2254 (2014).
[Crossref] [PubMed]

Marcoux, P. R.

P. R. Marcoux, M. Dupoy, A. Cuer, J. L. Kodja, A. Lefebvre, F. Licari, R. Louvet, A. Narassiguin, and F. Mallard, “Optical forward-scattering for identification of bacteria within microcolonies,” Appl. Microbiol. Biotechnol. 98(5), 2243–2254 (2014).
[Crossref] [PubMed]

Mariotti, A.

D. Ziegler, A. Mariotti, V. Pflüger, M. Saad, G. Vogel, M. Tonolla, and X. Perret, “In situ identification of plant-invasive bacteria with MALDI-TOF mass spectrometry,” PLoS One 7(5), e37189 (2012).
[Crossref] [PubMed]

Marschner, P.

P. Marschner, D. Crowley, and R. Lieberei, “Arbuscular mycorrhizal infection changes the bacterial 16 S rDNA community composition in the rhizosphere of maize,” Mycorrhiza 11(6), 297–302 (2001).
[Crossref] [PubMed]

P. Marschner, C.-H. Yang, R. Lieberei, and D. Crowley, “Soil and plant specific effects on bacterial community composition in the rhizosphere,” Soil Biol. Biochem. 33(11), 1437–1445 (2001).
[Crossref]

Mignot, T.

D. I. Cattoni, J.-B. Fiche, A. Valeri, T. Mignot, and M. Nöllmann, “Super-resolution imaging of bacteria in a microfluidics device,” PLoS One 8(10), e76268 (2013).
[Crossref] [PubMed]

Miller, W.

C. H. Jaeger, S. E. Lindow, W. Miller, E. Clark, and M. K. Firestone, “Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan,” Appl. Environ. Microbiol. 65(6), 2685–2690 (1999).
[PubMed]

Minoni, U.

U. Minoni, A. Signoroni, and G. Nassini, “On the application of optical forward-scattering to bacterial identification in an automated clinical analysis perspective,” Biosens. Bioelectron. 68, 536–543 (2015).
[Crossref] [PubMed]

Moore, G.

L. R. Dartnell, T. A. Roberts, G. Moore, J. M. Ward, and J.-P. Muller, “Fluorescence characterization of clinically-important bacteria,” PLoS One 8(9), e75270 (2013).
[Crossref] [PubMed]

Morando, D.

S. W. Wessel, H. C. van der Mei, D. Morando, A. M. Slomp, B. van de Belt-Gritter, A. Maitra, and H. J. Busscher, “Quantification and qualification of bacteria trapped in chewed gum,” PLoS One 10(1), e0117191 (2015).
[Crossref] [PubMed]

Muller, J.-P.

L. R. Dartnell, T. A. Roberts, G. Moore, J. M. Ward, and J.-P. Muller, “Fluorescence characterization of clinically-important bacteria,” PLoS One 8(9), e75270 (2013).
[Crossref] [PubMed]

Narassiguin, A.

P. R. Marcoux, M. Dupoy, A. Cuer, J. L. Kodja, A. Lefebvre, F. Licari, R. Louvet, A. Narassiguin, and F. Mallard, “Optical forward-scattering for identification of bacteria within microcolonies,” Appl. Microbiol. Biotechnol. 98(5), 2243–2254 (2014).
[Crossref] [PubMed]

Nassini, G.

U. Minoni, A. Signoroni, and G. Nassini, “On the application of optical forward-scattering to bacterial identification in an automated clinical analysis perspective,” Biosens. Bioelectron. 68, 536–543 (2015).
[Crossref] [PubMed]

Nöllmann, M.

D. I. Cattoni, J.-B. Fiche, A. Valeri, T. Mignot, and M. Nöllmann, “Super-resolution imaging of bacteria in a microfluidics device,” PLoS One 8(10), e76268 (2013).
[Crossref] [PubMed]

Olma, T.

J. Kok, L. C. Thomas, T. Olma, S. C. A. Chen, and J. R. Iredell, “Identification of bacteria in blood culture broths using matrix-assisted laser desorption-ionization Sepsityper™ and time of flight mass spectrometry,” PLoS One 6(8), e23285 (2011).
[Crossref] [PubMed]

Patsekin, V.

E. Bae, D. Ying, D. Kramer, V. Patsekin, B. Rajwa, C. Holdman, J. Sturgis, V. J. Davisson, and J. P. Robinson, “Portable bacterial identification system based on elastic light scatter patterns,” J. Biol. Eng. 6(1), 12 (2012).
[Crossref] [PubMed]

Perret, X.

D. Ziegler, A. Mariotti, V. Pflüger, M. Saad, G. Vogel, M. Tonolla, and X. Perret, “In situ identification of plant-invasive bacteria with MALDI-TOF mass spectrometry,” PLoS One 7(5), e37189 (2012).
[Crossref] [PubMed]

Pflüger, V.

D. Ziegler, A. Mariotti, V. Pflüger, M. Saad, G. Vogel, M. Tonolla, and X. Perret, “In situ identification of plant-invasive bacteria with MALDI-TOF mass spectrometry,” PLoS One 7(5), e37189 (2012).
[Crossref] [PubMed]

Podbielska, H.

Prod’hom, G.

A. Croxatto, G. Prod’hom, and G. Greub, “Applications of MALDI-TOF mass spectrometry in clinical diagnostic microbiology,” FEMS Microbiol. Rev. 36(2), 380–407 (2012).
[Crossref] [PubMed]

Rajwa, B.

H. Kim, B. Rajwa, A. K. Bhunia, J. P. Robinson, and E. Bae, “Development of a multispectral light-scatter sensor for bacterial colonies,” J. Biophotonics 10(5), 634–644 (2017).
[Crossref] [PubMed]

Y. Tang, H. Kim, A. K. Singh, A. Aroonnual, E. Bae, B. Rajwa, P. M. Fratamico, and A. K. Bhunia, “Light scattering sensor for direct identification of colonies of Escherichia coli serogroups O26, O45, O103, O111, O121, O145 and O157,” PLoS One 9(8), e105272 (2014).
[Crossref] [PubMed]

E. Bae, D. Ying, D. Kramer, V. Patsekin, B. Rajwa, C. Holdman, J. Sturgis, V. J. Davisson, and J. P. Robinson, “Portable bacterial identification system based on elastic light scatter patterns,” J. Biol. Eng. 6(1), 12 (2012).
[Crossref] [PubMed]

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

B. Bayraktar, P. P. Banada, E. D. Hirleman, A. K. Bhunia, J. P. Robinson, and B. Rajwa, “Feature extraction from light-scatter patterns of Listeria colonies for identification and classification,” J. Biomed. Opt. 11(3), 034006 (2006).
[Crossref] [PubMed]

Ram, S. J.

M. D. Abràmoff, P. J. Magalhães, and S. J. Ram, “Image processing with ImageJ,” Biophoton. Int. 11(7), 36–42 (2004).

Reinhardt, R.

S. Sauer, A. Freiwald, T. Maier, M. Kube, R. Reinhardt, M. Kostrzewa, and K. Geider, “Classification and identification of bacteria by mass spectrometry and computational analysis,” PLoS One 3(7), e2843 (2008).
[Crossref] [PubMed]

Roberts, T. A.

L. R. Dartnell, T. A. Roberts, G. Moore, J. M. Ward, and J.-P. Muller, “Fluorescence characterization of clinically-important bacteria,” PLoS One 8(9), e75270 (2013).
[Crossref] [PubMed]

Robinson, J. P.

H. Kim, B. Rajwa, A. K. Bhunia, J. P. Robinson, and E. Bae, “Development of a multispectral light-scatter sensor for bacterial colonies,” J. Biophotonics 10(5), 634–644 (2017).
[Crossref] [PubMed]

E. Bae, D. Ying, D. Kramer, V. Patsekin, B. Rajwa, C. Holdman, J. Sturgis, V. J. Davisson, and J. P. Robinson, “Portable bacterial identification system based on elastic light scatter patterns,” J. Biol. Eng. 6(1), 12 (2012).
[Crossref] [PubMed]

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

B. Bayraktar, P. P. Banada, E. D. Hirleman, A. K. Bhunia, J. P. Robinson, and B. Rajwa, “Feature extraction from light-scatter patterns of Listeria colonies for identification and classification,” J. Biomed. Opt. 11(3), 034006 (2006).
[Crossref] [PubMed]

Saad, M.

D. Ziegler, A. Mariotti, V. Pflüger, M. Saad, G. Vogel, M. Tonolla, and X. Perret, “In situ identification of plant-invasive bacteria with MALDI-TOF mass spectrometry,” PLoS One 7(5), e37189 (2012).
[Crossref] [PubMed]

Sait, M.

P. H. Janssen, P. S. Yates, B. E. Grinton, P. M. Taylor, and M. Sait, “Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia,” Appl. Environ. Microbiol. 68(5), 2391–2396 (2002).
[Crossref] [PubMed]

Sauer, S.

S. Sauer, A. Freiwald, T. Maier, M. Kube, R. Reinhardt, M. Kostrzewa, and K. Geider, “Classification and identification of bacteria by mass spectrometry and computational analysis,” PLoS One 3(7), e2843 (2008).
[Crossref] [PubMed]

Schleifer, K. H.

R. I. Amann, W. Ludwig, and K. H. Schleifer, “Phylogenetic identification and in situ detection of individual microbial cells without cultivation,” Microbiol. Rev. 59(1), 143–169 (1995).
[PubMed]

Signoroni, A.

U. Minoni, A. Signoroni, and G. Nassini, “On the application of optical forward-scattering to bacterial identification in an automated clinical analysis perspective,” Biosens. Bioelectron. 68, 536–543 (2015).
[Crossref] [PubMed]

Singh, A. K.

Y. Tang, H. Kim, A. K. Singh, A. Aroonnual, E. Bae, B. Rajwa, P. M. Fratamico, and A. K. Bhunia, “Light scattering sensor for direct identification of colonies of Escherichia coli serogroups O26, O45, O103, O111, O121, O145 and O157,” PLoS One 9(8), e105272 (2014).
[Crossref] [PubMed]

Slomp, A. M.

S. W. Wessel, H. C. van der Mei, D. Morando, A. M. Slomp, B. van de Belt-Gritter, A. Maitra, and H. J. Busscher, “Quantification and qualification of bacteria trapped in chewed gum,” PLoS One 10(1), e0117191 (2015).
[Crossref] [PubMed]

Sturgis, J.

E. Bae, D. Ying, D. Kramer, V. Patsekin, B. Rajwa, C. Holdman, J. Sturgis, V. J. Davisson, and J. P. Robinson, “Portable bacterial identification system based on elastic light scatter patterns,” J. Biol. Eng. 6(1), 12 (2012).
[Crossref] [PubMed]

Suchwalko, A.

Tang, Y.

Y. Tang, H. Kim, A. K. Singh, A. Aroonnual, E. Bae, B. Rajwa, P. M. Fratamico, and A. K. Bhunia, “Light scattering sensor for direct identification of colonies of Escherichia coli serogroups O26, O45, O103, O111, O121, O145 and O157,” PLoS One 9(8), e105272 (2014).
[Crossref] [PubMed]

Taylor, P. M.

P. H. Janssen, P. S. Yates, B. E. Grinton, P. M. Taylor, and M. Sait, “Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia,” Appl. Environ. Microbiol. 68(5), 2391–2396 (2002).
[Crossref] [PubMed]

Thomas, L. C.

J. Kok, L. C. Thomas, T. Olma, S. C. A. Chen, and J. R. Iredell, “Identification of bacteria in blood culture broths using matrix-assisted laser desorption-ionization Sepsityper™ and time of flight mass spectrometry,” PLoS One 6(8), e23285 (2011).
[Crossref] [PubMed]

Tonolla, M.

D. Ziegler, A. Mariotti, V. Pflüger, M. Saad, G. Vogel, M. Tonolla, and X. Perret, “In situ identification of plant-invasive bacteria with MALDI-TOF mass spectrometry,” PLoS One 7(5), e37189 (2012).
[Crossref] [PubMed]

Valeri, A.

D. I. Cattoni, J.-B. Fiche, A. Valeri, T. Mignot, and M. Nöllmann, “Super-resolution imaging of bacteria in a microfluidics device,” PLoS One 8(10), e76268 (2013).
[Crossref] [PubMed]

van de Belt-Gritter, B.

S. W. Wessel, H. C. van der Mei, D. Morando, A. M. Slomp, B. van de Belt-Gritter, A. Maitra, and H. J. Busscher, “Quantification and qualification of bacteria trapped in chewed gum,” PLoS One 10(1), e0117191 (2015).
[Crossref] [PubMed]

van der Mei, H. C.

S. W. Wessel, H. C. van der Mei, D. Morando, A. M. Slomp, B. van de Belt-Gritter, A. Maitra, and H. J. Busscher, “Quantification and qualification of bacteria trapped in chewed gum,” PLoS One 10(1), e0117191 (2015).
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Figures (8)

Fig. 1
Fig. 1 The functional diagram of the presented method for bacteria identification.
Fig. 2
Fig. 2 The BISLD system configuration: (1) - the laser diode module (635 nm, 1 mW, collimated, Thorlabs), (2) - amplitude filters wheel (OD: 0-2, Thorlabs), (3) - beam expander BE (1.5X, Thorlabs), (4) - iris diaphragm (diameter: 0-2,5 cm, Thorlabs) with automatically controlled diameter, (5) - transforming lens L (f = 12 cm, Thorlabs), (6) - pellicle beam splitter (T:R = 50:50, Thorlabs), (7) - holder with the sample of bacterial colonies in Petri Dish integrated with an automatic X-Y-Z translation stage, (8) – beam splitter (T/R = 50/50, Thorlabs), (9) - CCD camera (EO-1312, Edmund Optics) with imaging objective (f = 3.5 cm, Edmund Optics) for diffraction patterns recording, (10) high-resolution CCD camera (DCU223M, Thorlabs) with imaging objective (f = 12 mm, Edmund Optics), (11) high-sensitivity CMOS camera (DCC1240M, Thorlabs) with imaging microscope objective (Nikon, 4x, WD = 30 mm) and (12) - computer unit.
Fig. 3
Fig. 3 The workflow of the statistical analysis of diffraction patterns.
Fig. 4
Fig. 4 Representative diffraction patterns of bacterial colonies examined in the study (bacterial colonies incubation time:18 hours, exposure time: 2s).
Fig. 5
Fig. 5 Repeatability of diffraction patterns of various colonies (explanation in text): (A) Citrobacter freundii (PCM 531), (B) Rahnella aquatilis (x21N), (C) Rahnella aquatilis (x31E).
Fig. 6
Fig. 6 An exemplary image of the sample plate containing various colonies (Bacillus subtilis (marked red), Citrobacter freundii (green numbers), Escherichia coli (yellow), Proteus mirabilis (blue)) and their Fresnel diffraction patterns enabling identification of indicated colonies. The red-dashed oval indicates the overlapping colonies, which cannot be differentiated.
Fig. 7
Fig. 7 The representative monochromatic 2D transmission coefficient distribution of: (A) Bacillus subtilis, (B) Rahnella aquatilis (x31E), (C) Rahnella aquatilis (x21N), (D) Citrobacter freundii, (E) Escherichia coli, (F) Proteus mirabilis, (G) Pseudomonas aeruginosa, (H) Staphylococcus aureus, (I) Staphylococcus intermedius colonies obtained under monochromatic illumination (color scale represents values of transmission coefficient).
Fig. 8
Fig. 8 ANOVA (a) and SNR (b) based features discriminative power ranking, features are labelled -name.x, where a name is bacteria strain, and x is the ring number starting from the pattern centre.

Tables (2)

Tables Icon

Table 1 Identification results of soil bacteria using two QDA and SVM classifiers and ANOVA and SNR selection methods were used for ranking predictive features. A number of best predictors (features) used in the model building, identification error, multi-class sensitivity and specificity, are depicted. Most relevant results are marked in bold.

Tables Icon

Table 2 Identification results for Rahnella aquatilis strains. Two feature selection methods (ANOVA and SNR) were used for the features predictive properties ranking. A number of best predictors (features) used for the model building, identification error, multi-class sensitivity and specificity, are depicted. Most significant results are marked in bold.