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References

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    Pubmed PMC CrossRef
  2. Zhu F, Qin C, Tao L, Liu X, Shi Z, Ma X, et al. 2011. Clustered patterns of species origins of nature-derived drugs and clues for future bioprospecting. Proc. Natl. Acad. Sci. USA 108: 12943-12948.
    Pubmed PMC CrossRef
  3. Austin B. 1989. Novel pharmaceutical compounds from marine bacteria. J. Appl. Bacteriol. 67: 461-470.
    Pubmed CrossRef
  4. Darabpour E, Roayaei AM, Motamedi H, Ronagh M. 2011. Isolation of a broad spectrum antibiotic producer bacterium, Pseudoalteromonas piscicida PG-02, from the Persian Gulf. Bangladesh J. Pharmacol. 6: 74-83.
    CrossRef
  5. Jensen P, Fenical W. 1996. Marine bacterial diversity as a resource for novel microbial products. J. Ind. Microbiol. Biotechnol. 17: 346-351.
    CrossRef
  6. Vigneshwari R, Sally RA, Jayapradha R. 2015. Cocultivation powerful tool for the production of secondary metabolites. J. Chem. Pharm. Res. 7: 481-485.
  7. Valgas C, Souza S, Smânia E, Smânia JA. 2007. Screening methods to determine antibacterial activity of natural products. Braz. J. Microbiol. 38: 369-380.
    CrossRef
  8. Balouiri M, Sadiki M, Ibnsouda S. 2016. Methods for in vitro evaluating antimicrobial activity: a review. J. Pharm. Anal. 6: 71-79.
    Pubmed PMC CrossRef
  9. Pikkemaat M. 2009. Microbial screening methods for detection of antibiotic residues in slaughter animals. Anal. Bioanal. Chem. 395: 893-905.
    Pubmed PMC CrossRef
  10. Zhang J, Liu X, Liu S. 2009. Agrococcus terreus sp. nov. and Micrococcus terreus sp. nov., isolated from forest soil. Int. J. Syst. Evol. Microbiol. 60: 1897-1903.
    Pubmed CrossRef
  11. Ivanova E, Alexeeva Y, Zhukova N, Gorshkova N, Buljan V, Nicolau D, et al. 2004. Bacillus algicola sp. nov., a novel filamentous organism isolated from brown alga Fucus evanescens. Syst. Appl. Microbiol. 27: 301-307.
    Pubmed CrossRef
  12. Asker D, Beppu T, Ueda K. 2007. Mesoflavibacter zeaxanthinifaciens gen. nov., sp. nov., a novel zeaxanthin-producing marine bacterium of the family Flavobacteriaceae. Syst. Appl. Microbiol. 30: 291-296.
    Pubmed CrossRef
  13. Romanenko L. 2003. Pseudoalteromonas agarivorans sp. nov., a novel marine agarolytic bacterium. Int. J. Syst. Evol. Microbiol. 53: 125-131.
    Pubmed CrossRef
  14. Shao R, Lai Q, Liu X, Sun F, Du Y, Li G, et al. 2013. Zunongwangia atlantica sp. nov., isolated from deep-sea water. Int. J. Syst. Evol. Microbiol. 64: 16-20.
    Pubmed CrossRef
  15. Bernbom N, Ng Y, Olsen S, Gram L. 2013. Pseudoalteromonas spp. serve as initial bacterial attractants in mesocosms of coastal waters but have subsequent antifouling capacity in mesocosms and when embedded in paint. Appl. Environ. Microbiol. 79: 6885-6893.
    Pubmed PMC CrossRef
  16. Anwar M, Choi S. 2014. Gram-negative marine bacteria:structural features of lipopolysaccharides and their relevance for economically important diseases. Mar. Drugs 12: 2485-2514.
    Pubmed PMC CrossRef
  17. Jung M, Kim J, Paek W, Lim J, Lee H, Kim P, et al. 2011. Bacillus manliponensis sp. nov., a new member of the Bacillus cereus group isolated from foreshore tidal flat sediment. J. Microbiol. 49: 1027-1032.
    Pubmed CrossRef
  18. Roberts M, Nakamura L, Cohan F. 1996. Bacillus vallismortis sp. nov., a close relative of Bacillus subtilis, isolated from soil in Death Valley, California. Int. J. Syst. Evol. Microbiol. 46: 470-475.
    Pubmed CrossRef
  19. Poli A, Nicolaus B, Denizci A, Yavuzturk B, Kazan D. 2012. Halomonas smyrnensis sp. nov., a moderately halophilic, exopolysaccharide-producing bacterium. Int. J. Syst. Evol. Microbiol. 63: 10-18.
    Pubmed CrossRef
  20. Kaneko M, Iwashita M. 1987. Antimicrobial susceptibility of Vibrio parahaemolyticus and Vibrio alginolyticus isolated from human feces and foods. Kansenshogaku Zasshi 61: 9-16.
    Pubmed CrossRef
  21. Bottone E. 2010. Bacillus cereus, a volatile human pathogen. Clin. Microbiol. Rev. 23: 382-398.
    Pubmed PMC CrossRef
  22. Ushakova N, Nekrasov R, Meleshko N, Laptev G, Il’ina L, Kozlova A, et al. 2013. Effect of Bacillus subtilis on the rumen microbial community and its components exhibiting high correlation coefficients with the host nutrition, growth, and development. Microbiology 82: 475-481.
    CrossRef
  23. Stevens D, Hamilton J, Johnson N, Kim K, Lee J. 2009. Halomonas, a newly recognized human pathogen causing infections and contamination in a dialysis center. Medicine 88: 244-249.
    Pubmed CrossRef
  24. Hubálek Z. 2003. Protectants used in the cryopreservation of microorganisms. Cryobiology 46: 205-229.
    CrossRef
  25. Clinical and Laboratory Standards Institute (CLSI). 2015. Performance standard for antimicrobial susceptibility testing;twenty-second informational supplement, pp. 146-156. Clinical and Laboratory Standards Institute, Wayne, PA, USA.
  26. Shank EA, Kolter R. 2009. New developments in microbial interspecies signaling. Curr. Opin. Microbiol. 12: 205-214.
    Pubmed PMC CrossRef
  27. Armstrong E, Yan L, Boyd K, Wright P, Burgess J. 2001. The symbiotic role of marine microbes on living surfaces. Hydrobiologia 461: 37-40.
    CrossRef
  28. Sánchez J, Kouznetsov V. 2010. Antimycobacterial susceptibility testing methods for natural products research. Braz. J. Microbiol. 41: 270-277
    Pubmed PMC CrossRef
  29. Pauli G , C ase R, I nui T, W ang Y, C ho S , Fischer N, et al. 2005. New perspectives on natural products in TB drug research. Life Sci. 78: 485-494.
    Pubmed CrossRef
  30. Balouiri M, Sadiki M, Ibnsouda S. 2016. Methods for in vitro evaluating antimicrobial activity: a review. J. Pharm. Anal. 6: 71-79.
    Pubmed PMC CrossRef
  31. Gibb A. 1999. Plates are better than broth for recovery of fastidious organisms from some specimen material. J. Clin. Microbiol. 37: 875.
  32. Dheilly A, Soum-Soutera E, Klein G, Bazire A, Compere C, Haras D, et al. 2010. Antibiofilm activity of the marine bacterium Pseudoalteromonas sp. strain 3J6. Appl. Environ. Microbiol. 76: 3452-3461.
    Pubmed PMC CrossRef
  33. Wilson G, Raftos D, Nair S. 2011. Antimicrobial activity of surface attached marine bacteria in biofilms. Microbiol. Res. 166: 437-448.
    Pubmed CrossRef
  34. Goers L, Freemont P, Polizzi K. 2014. Co-culture systems and technologies: taking synthetic biology to the next level. J. R. Soc. Interface 11: 20140065.
    Pubmed PMC CrossRef
  35. Fukuda T, Tsutsumi K, Morita H. 2008. Antibiotic activity in co-culture: influence of Bacillus subtilis on the antibiotic activity of Rhizopus peka. Japan J. Food Eng. 9: 99-106.
    CrossRef
  36. Dopazo C, Lemos M, Lodeiros C, Bolinches J, Barja J, Toranzo A. 1988. Inhibitory activity of antibiotic-producing marine bacteria against fish pathogens. J. Appl. Bacteriol. 65: 97-101.
    Pubmed CrossRef
  37. Yu M, Wang J, Tang K, Shi X, Wang S, Zhu W, Zhang X. 2011. Purification and characterization of antibacterial compounds of Pseudoalteromonas flavipulchra JG1. Microbiology 158: 835-842.
    Pubmed CrossRef
  38. Gauthier G, Gauthier M, Christen R. 1995. Phylogenetic analysis of the genera Alteromonas, Shewanella, and Moritella using genes coding for small-subunit rRNA sequences and division of the genus Alteromonas into two genera, Alteromonas (Emended) and Pseudoalteromonas gen. nov., and proposal of twelve new species combinations. Int. J. Syst. Bacteriol. 45: 755-761.
    Pubmed CrossRef
  39. Bowman J. 2007. Bioactive compound synthetic capacity and ecological significance of marine bacterial genus Pseudoalteromonas. Mar. Drugs 5: 220-241.
    Pubmed PMC CrossRef
  40. Jin G, Wang S, Yu M, Yan S, Zhang X. 2010. Identification of a marine antagonistic strain JG1 and establishment of a polymerase chain reaction detection technique based on the gyrB gene. Aquac. Res. 41: 1867-1874.
    CrossRef
  41. Hayashida-Soiza G, Uchida A, Mori N, Kuwahara Y, Ishida Y. 2008. Purification and characterization of antibacterial substances produced by a marine bacterium Pseudoalteromonas haloplanktis strain. J. Appl. Microbiol. 105: 1672-1677.
    Pubmed CrossRef
  42. Offret C, Desriac F, Le Chevalier P, Mounier J, Jégou C, Fleury Y. 2016. Spotlight on antimicrobial metabolites from the marine bacteria Pseudoalteromonas: chemodiversity and ecological significance. Mar. Drugs 14: 129.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(8): 1441-1448

Published online August 28, 2017 https://doi.org/10.4014/jmb.1703.03012

Copyright © The Korean Society for Microbiology and Biotechnology.

A Rapid and Efficient Screening Method for Antibacterial Compound-Producing Bacteria

Sachithra Amarin Hettiarachchi 1, 2, Su-Jin Lee 1, Youngdeuk Lee 1, Young-Kyung Kwon 1, Mahanama De Zoysa 3, Song Moon 1, Eunyoung Jo 1, Eunyoung Kim 1, Do-Hyung Kang 1, 2, Soo-Jin Heo 1, 2 and Chulhong Oh 1, 2*

Korea Institute of Ocean Science & Technology, Jeju Special Self-Governing Province 63349, Republic of Korea, 1Department of Marine Biology, Korea University of Science and Technology, Jeju Special Self-Governing Province 63349, Republic of Korea, 2College of Veterinary Medicine, Chungnam National University, Daejeon 34134, Republic of Korea

Received: March 8, 2017; Accepted: June 13, 2017

Abstract

Antibacterial compounds are widely used in the treatment of human and animal diseases. The
overuse of antibiotics has led to a rapid rise in the prevalence of drug-resistant bacteria,
making the development of new antibacterial compounds essential. This study focused on
developing a fast and easy method for identifying marine bacteria that produce antibiotic
compounds. Eight randomly selected marine target bacterial species (Agrococcus terreus,
Bacillus algicola, Mesoflavibacter zeaxanthinifaciens, Pseudoalteromonas flavipulchra, P. peptidolytica,
P. piscicida, P. rubra, and Zunongwangia atlantica) were tested for production of antibacterial
compounds against four strains of test bacteria (B. cereus, B. subtilis, Halomonas smyrnensis, and
Vibrio alginolyticus). Colony picking was used as the primary screening method. Clear zones
were observed around colonies of P. flavipulchra, P. peptidolytica, P. piscicida, and P. rubra tested
against B. cereus, B. subtilis, and H. smyrnensis. The efficiency of colony scraping and broth
culture methods for antimicrobial compound extraction was also compared using a disk
diffusion assay. P. peptidolytica, P. piscicida, and P. rubra showed antagonistic activity against
H. smyrnensis, B. cereus, and B. subtilis, respectively, only in the colony scraping method. Our
results show that colony picking and colony scraping are effective, quick, and easy methods of
screening for antibacterial compound-producing bacteria.

Keywords: Colony picking, colony scraping, broth culture, screening, antibacterial compounds

References

  1. Newman D J, C ragg GM. 2012. Natural products as sources of new drugs over the 30 years from 1981 to 2010. J. Nat. Prod. 75: 311-335.
    Pubmed KoreaMed CrossRef
  2. Zhu F, Qin C, Tao L, Liu X, Shi Z, Ma X, et al. 2011. Clustered patterns of species origins of nature-derived drugs and clues for future bioprospecting. Proc. Natl. Acad. Sci. USA 108: 12943-12948.
    Pubmed KoreaMed CrossRef
  3. Austin B. 1989. Novel pharmaceutical compounds from marine bacteria. J. Appl. Bacteriol. 67: 461-470.
    Pubmed CrossRef
  4. Darabpour E, Roayaei AM, Motamedi H, Ronagh M. 2011. Isolation of a broad spectrum antibiotic producer bacterium, Pseudoalteromonas piscicida PG-02, from the Persian Gulf. Bangladesh J. Pharmacol. 6: 74-83.
    CrossRef
  5. Jensen P, Fenical W. 1996. Marine bacterial diversity as a resource for novel microbial products. J. Ind. Microbiol. Biotechnol. 17: 346-351.
    CrossRef
  6. Vigneshwari R, Sally RA, Jayapradha R. 2015. Cocultivation powerful tool for the production of secondary metabolites. J. Chem. Pharm. Res. 7: 481-485.
  7. Valgas C, Souza S, Smânia E, Smânia JA. 2007. Screening methods to determine antibacterial activity of natural products. Braz. J. Microbiol. 38: 369-380.
    CrossRef
  8. Balouiri M, Sadiki M, Ibnsouda S. 2016. Methods for in vitro evaluating antimicrobial activity: a review. J. Pharm. Anal. 6: 71-79.
    Pubmed KoreaMed CrossRef
  9. Pikkemaat M. 2009. Microbial screening methods for detection of antibiotic residues in slaughter animals. Anal. Bioanal. Chem. 395: 893-905.
    Pubmed KoreaMed CrossRef
  10. Zhang J, Liu X, Liu S. 2009. Agrococcus terreus sp. nov. and Micrococcus terreus sp. nov., isolated from forest soil. Int. J. Syst. Evol. Microbiol. 60: 1897-1903.
    Pubmed CrossRef
  11. Ivanova E, Alexeeva Y, Zhukova N, Gorshkova N, Buljan V, Nicolau D, et al. 2004. Bacillus algicola sp. nov., a novel filamentous organism isolated from brown alga Fucus evanescens. Syst. Appl. Microbiol. 27: 301-307.
    Pubmed CrossRef
  12. Asker D, Beppu T, Ueda K. 2007. Mesoflavibacter zeaxanthinifaciens gen. nov., sp. nov., a novel zeaxanthin-producing marine bacterium of the family Flavobacteriaceae. Syst. Appl. Microbiol. 30: 291-296.
    Pubmed CrossRef
  13. Romanenko L. 2003. Pseudoalteromonas agarivorans sp. nov., a novel marine agarolytic bacterium. Int. J. Syst. Evol. Microbiol. 53: 125-131.
    Pubmed CrossRef
  14. Shao R, Lai Q, Liu X, Sun F, Du Y, Li G, et al. 2013. Zunongwangia atlantica sp. nov., isolated from deep-sea water. Int. J. Syst. Evol. Microbiol. 64: 16-20.
    Pubmed CrossRef
  15. Bernbom N, Ng Y, Olsen S, Gram L. 2013. Pseudoalteromonas spp. serve as initial bacterial attractants in mesocosms of coastal waters but have subsequent antifouling capacity in mesocosms and when embedded in paint. Appl. Environ. Microbiol. 79: 6885-6893.
    Pubmed KoreaMed CrossRef
  16. Anwar M, Choi S. 2014. Gram-negative marine bacteria:structural features of lipopolysaccharides and their relevance for economically important diseases. Mar. Drugs 12: 2485-2514.
    Pubmed KoreaMed CrossRef
  17. Jung M, Kim J, Paek W, Lim J, Lee H, Kim P, et al. 2011. Bacillus manliponensis sp. nov., a new member of the Bacillus cereus group isolated from foreshore tidal flat sediment. J. Microbiol. 49: 1027-1032.
    Pubmed CrossRef
  18. Roberts M, Nakamura L, Cohan F. 1996. Bacillus vallismortis sp. nov., a close relative of Bacillus subtilis, isolated from soil in Death Valley, California. Int. J. Syst. Evol. Microbiol. 46: 470-475.
    Pubmed CrossRef
  19. Poli A, Nicolaus B, Denizci A, Yavuzturk B, Kazan D. 2012. Halomonas smyrnensis sp. nov., a moderately halophilic, exopolysaccharide-producing bacterium. Int. J. Syst. Evol. Microbiol. 63: 10-18.
    Pubmed CrossRef
  20. Kaneko M, Iwashita M. 1987. Antimicrobial susceptibility of Vibrio parahaemolyticus and Vibrio alginolyticus isolated from human feces and foods. Kansenshogaku Zasshi 61: 9-16.
    Pubmed CrossRef
  21. Bottone E. 2010. Bacillus cereus, a volatile human pathogen. Clin. Microbiol. Rev. 23: 382-398.
    Pubmed KoreaMed CrossRef
  22. Ushakova N, Nekrasov R, Meleshko N, Laptev G, Il’ina L, Kozlova A, et al. 2013. Effect of Bacillus subtilis on the rumen microbial community and its components exhibiting high correlation coefficients with the host nutrition, growth, and development. Microbiology 82: 475-481.
    CrossRef
  23. Stevens D, Hamilton J, Johnson N, Kim K, Lee J. 2009. Halomonas, a newly recognized human pathogen causing infections and contamination in a dialysis center. Medicine 88: 244-249.
    Pubmed CrossRef
  24. Hubálek Z. 2003. Protectants used in the cryopreservation of microorganisms. Cryobiology 46: 205-229.
    CrossRef
  25. Clinical and Laboratory Standards Institute (CLSI). 2015. Performance standard for antimicrobial susceptibility testing;twenty-second informational supplement, pp. 146-156. Clinical and Laboratory Standards Institute, Wayne, PA, USA.
  26. Shank EA, Kolter R. 2009. New developments in microbial interspecies signaling. Curr. Opin. Microbiol. 12: 205-214.
    Pubmed KoreaMed CrossRef
  27. Armstrong E, Yan L, Boyd K, Wright P, Burgess J. 2001. The symbiotic role of marine microbes on living surfaces. Hydrobiologia 461: 37-40.
    CrossRef
  28. Sánchez J, Kouznetsov V. 2010. Antimycobacterial susceptibility testing methods for natural products research. Braz. J. Microbiol. 41: 270-277
    Pubmed KoreaMed CrossRef
  29. Pauli G , C ase R, I nui T, W ang Y, C ho S , Fischer N, et al. 2005. New perspectives on natural products in TB drug research. Life Sci. 78: 485-494.
    Pubmed CrossRef
  30. Balouiri M, Sadiki M, Ibnsouda S. 2016. Methods for in vitro evaluating antimicrobial activity: a review. J. Pharm. Anal. 6: 71-79.
    Pubmed KoreaMed CrossRef
  31. Gibb A. 1999. Plates are better than broth for recovery of fastidious organisms from some specimen material. J. Clin. Microbiol. 37: 875.
  32. Dheilly A, Soum-Soutera E, Klein G, Bazire A, Compere C, Haras D, et al. 2010. Antibiofilm activity of the marine bacterium Pseudoalteromonas sp. strain 3J6. Appl. Environ. Microbiol. 76: 3452-3461.
    Pubmed KoreaMed CrossRef
  33. Wilson G, Raftos D, Nair S. 2011. Antimicrobial activity of surface attached marine bacteria in biofilms. Microbiol. Res. 166: 437-448.
    Pubmed CrossRef
  34. Goers L, Freemont P, Polizzi K. 2014. Co-culture systems and technologies: taking synthetic biology to the next level. J. R. Soc. Interface 11: 20140065.
    Pubmed KoreaMed CrossRef
  35. Fukuda T, Tsutsumi K, Morita H. 2008. Antibiotic activity in co-culture: influence of Bacillus subtilis on the antibiotic activity of Rhizopus peka. Japan J. Food Eng. 9: 99-106.
    CrossRef
  36. Dopazo C, Lemos M, Lodeiros C, Bolinches J, Barja J, Toranzo A. 1988. Inhibitory activity of antibiotic-producing marine bacteria against fish pathogens. J. Appl. Bacteriol. 65: 97-101.
    Pubmed CrossRef
  37. Yu M, Wang J, Tang K, Shi X, Wang S, Zhu W, Zhang X. 2011. Purification and characterization of antibacterial compounds of Pseudoalteromonas flavipulchra JG1. Microbiology 158: 835-842.
    Pubmed CrossRef
  38. Gauthier G, Gauthier M, Christen R. 1995. Phylogenetic analysis of the genera Alteromonas, Shewanella, and Moritella using genes coding for small-subunit rRNA sequences and division of the genus Alteromonas into two genera, Alteromonas (Emended) and Pseudoalteromonas gen. nov., and proposal of twelve new species combinations. Int. J. Syst. Bacteriol. 45: 755-761.
    Pubmed CrossRef
  39. Bowman J. 2007. Bioactive compound synthetic capacity and ecological significance of marine bacterial genus Pseudoalteromonas. Mar. Drugs 5: 220-241.
    Pubmed KoreaMed CrossRef
  40. Jin G, Wang S, Yu M, Yan S, Zhang X. 2010. Identification of a marine antagonistic strain JG1 and establishment of a polymerase chain reaction detection technique based on the gyrB gene. Aquac. Res. 41: 1867-1874.
    CrossRef
  41. Hayashida-Soiza G, Uchida A, Mori N, Kuwahara Y, Ishida Y. 2008. Purification and characterization of antibacterial substances produced by a marine bacterium Pseudoalteromonas haloplanktis strain. J. Appl. Microbiol. 105: 1672-1677.
    Pubmed CrossRef
  42. Offret C, Desriac F, Le Chevalier P, Mounier J, Jégou C, Fleury Y. 2016. Spotlight on antimicrobial metabolites from the marine bacteria Pseudoalteromonas: chemodiversity and ecological significance. Mar. Drugs 14: 129.
    Pubmed KoreaMed CrossRef