Sensitivity of predatory bacteria to different surfactants and their application to check bacterial predation
We evaluated the toxicity of surfactants against different predatory bacteria. Tests with Bdellovibrio bacteriovorus HD100 and SDS, an anionic surfactant, showed the predator was very sensitive; 0.02% SDS completely killed the predatory population (7-log loss; < 10 PFU/ml remaining) both when free-swimming or within the bdelloplast, i.e., intraperiplasmic. Similar results were also observed with B. bacteriovorus 109J and Peredibacter starrii. In contrast, none of the prey (E. coli, Klebsiella pneumoniae, Acinetobacter baumannii, or Pseudomonas sp. DSM 50906) viabilities were negatively affected by SDS. Triton X-100, a nonionic surfactant, was slightly less toxic towards B. bacteriovorus HD100 (viability loss of only 4-log), while two cationic surfactants, i.e., benzalkonium chloride (BZC) and cetyltrimethylammonium bromide (CTAB), were toxic towards both the predator and prey. Based on the above findings, we tested the potential use of SDS as a means to control predation. Addition of 0.02% SDS immediately halted predation based upon the prey bioluminescence, which leveled off and remained steady. This was confirmed using the predator viabilities; no predators were found in any of the samples where SDS was added. Consequently, low concentrations of SDS can be used as a simple means to control B. bacteriovorus HD100 activities.
KeywordsPredation Surfactant Bdellovibrio bacteriovorus SDS
We would like to thank the UNIST Central Research Facilities (ucrf.unist.ac.kr), specifically Jin-Hoe Hur at the UNIST Olympus Bioimaging Center, for use of the microscopes and imaging software. We would also like to thank Dr. Ajay K. Monnappa for discussions related to this study.
GC, JK, and RJM conceived the idea; GC, JK, HJ, and SMS conducted experiments; GC, JK, and RJM performed statistical analyses; and GC, JK, SMS, and RJM wrote the paper.
Funding for this study was from the National Research Foundation of Korea within the Korea-Israel Collaborative Research Program (Grant No. 2016K1A3A1A31913217) and under the Space Core Technology Development Project (Grant No. 2017M1A3A3A02016642).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
This article does not contain any studies with human participants or animals performed by any of the authors.
- Aspedon A, Nickerson KW (1993) A two-part energy burden imposed by growth of Enterobacter cloacae and Escherichia coli in sodium dodecyl sulfate. Can J Microbiol 39(6):555–561Google Scholar
- Atterbury RJ, Hobley L, Till R, Lambert C, Capeness MJ, Lerner TR, Fenton AK, Barrow P, Sockett RE (2011) Effects of orally administered Bdellovibrio bacteriovorus on the well-being and Salmonella colonization of young chicks. Appl Environ Microbiol 77(16):5794–5803. https://doi.org/10.1128/Aem.00426-11 Google Scholar
- Bagwell CE, Abernathy A, Barnwell R, Milliken CE, Noble PA, Dale T, Beauchesne KR, Moeller PDR (2016) Discovery of bioactive metabolites in biofuel microalgae that offer protection against predatory bacteria. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.00516
- Bowe F, Lipps CJ, Tsolis RM, Groisman E, Heffron F, Kusters JG (1998) At least four percent of the Salmonella typhimurium genome is required for fatal infection of mice. Infect Immun 66(7):3372–3377Google Scholar
- Cascales E, Gavioli M, Sturgis JN, Lloubes R (2000) Proton motive force drives the interaction of the inner membrane TolA and outer membrane pal proteins in Escherichia coli. Mol Microbiol 38(4):904–915Google Scholar
- Cascales E, Bernadac A, Gavioli M, Lazzaroni JC, Lloubes R (2002) Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J Bacteriol 184(3):754–759Google Scholar
- Dwidar M, Leung BM, Yaguchi T, Takayama S, Mitchell RJ (2013) Patterning bacterial communities on epithelial cells. PLoS One 8(6). https://doi.org/10.1371/journal.pone.0067165
- Ganuza E, Sellers CE, Bennett BW, Lyons EM, Carney LT (2016) A novel treatment protects Chlorella at commercial scale from the predatory bacterium Vampirovibrio chlorellavorus. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.00848
- Heidari Tajabadi F, Medrano-Soto A, Ahmadzadeh M, Salehi Jouzani G, Saier MH Jr (2017) Comparative analyses of transport proteins encoded within the genomes of Bdellovibrio bacteriovorus HD100 and Bdellovibrio exovorus JSS. J Mol Microbiol Biotechnol 27(6):332–349. https://doi.org/10.1159/000484563 Google Scholar
- Im H, Choi SY, Son S, Mitchell RJ (2017) Combined application of bacterial predation and violacein to kill polymicrobial pathogenic communities. Sci Rep-Uk 7. https://doi.org/10.1038/s41598-017-14567-7
- Jurkevitch E, Minz D, Ramati B, Barel G (2000) Prey range characterization, ribotyping, and diversity of soil and rhizosphere Bdellovibrio spp. isolated on phytopathogenic bacteria. Appl Environ Microbiol 66(6):2365–2371Google Scholar
- Kramer VC, Nickerson KW (1984) A transport-dependent energy burden imposed by growth of Enterobacter cloacae in the presence of 10% sodium dodecyl sulfate. Can J Microbiol 30(5):699–702Google Scholar
- Kramer VC, Calabrese DM, Nickerson KW (1980) Growth of Enterobacter-Cloacae in the presence of 25-percent sodium dodecyl-sulfate. Appl Environ Microbiol 40(5):973–976Google Scholar
- Lazzaroni JC, Germon P, Ray MC, Vianney A (1999) The Tol proteins of Escherichia coli and their involvement in the uptake of biomolecules and outer membrane stability. FEMS Microbiol Lett 177(2):191–197. https://doi.org/10.1111/j.1574-6968.1999.tb13731.x Google Scholar
- Llamas MA, Ramos JL, Rodriguez-Herva JJ (2000) Mutations in each of the tol genes of Pseudomonas putida reveal that they are critical for maintenance of outer membrane stability. J Bacteriol 182(17):4764–4772Google Scholar
- Lloubes R, Cascales E, Walburger A, Bouveret E, Lazdunski C, Bernadac A, Journet L (2001) The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity? Res Microbiol 152(6):523–529Google Scholar
- Lo Sciuto A, Fernandez-Pinar R, Bertuccini L, Iosi F, Superti F, Imperi F (2014) The periplasmic protein TolB as a potential drug target in Pseudomonas aeruginosa. PLoS One 9(8). https://doi.org/10.1371/journal.pone.0103784
- Mamkaeva KA, Plyushch AV, Titova NN, Gromov BV (1988) Dynamics of attack on cells of Chlorella in a culture infected by the parasitic bacterium Vampirovibrio-Chlorellavorus. Microbiology 57(1):116–119Google Scholar
- Monnappa AK, Bari W, Choi SY, Mitchell RJ (2016) Investigating the responses of human epithelial cells to predatory bacteria. Sci Rep-Uk 6. https://doi.org/10.1038/srep33485
- Mun W, Kwon H, Im H, Choi SY, Monnappa AK, Mitchell RJ (2017) Cyanide production by Chromobacterium piscinae shields it from Bdellovibrio bacteriovorus HD100 predation. mBio 8(6). https://doi.org/10.1128/mBio.01370-17
- NIH-Database https://hpd.nlm.nih.gov/cgi-bin/household/brands?tbl=chem&id=78. Accessed March 2019
- Pineiro S, Chauhan A, Berhane TK, Athar R, Zheng G, Wang C, Dickerson T, Liang X, Lymperopoulou DS, Chen H, Christman M, Louime C, Babiker W, Stine OC, Williams HN (2013) Niche partition of Bacteriovorax operational taxonomic units along salinity and temporal gradients in the Chesapeake Bay reveals distinct estuarine strains. Microb Ecol 65(3):652–660. https://doi.org/10.1007/s00248-013-0186-3 Google Scholar
- Schwudke D, Linscheid M, Strauch E, Appel B, Zahringer U, Moll H, Muller M, Brecker L, Gronow S, Lindner B (2003) The obligate predatory Bdellovibrio bacteriovorus possesses a neutral lipid A containing alpha-D-Mannoses that replace phosphate residues: similarities and differences between the lipid As and the lipopolysaccharides of the wild type strain B. bacteriovorus HD100 and its host-independent derivative HI100. J Biol Chem 278(30):27502–27512. https://doi.org/10.1074/jbc.M303012200 Google Scholar
- Stolp H, Starr MP (1963) Bdellovibrio Bacteriovorus Gen. Et Sp. N., a predatory, ectoparasitic, and bacteriolytic microorganism. Antonie Van Leeuwenhoek 29:217–248Google Scholar
- TOXNET https://toxnet.nlm.nih.gov/cgi-bin/sis/search/a?dbs+hsdb:@term+@DOCNO+1315. Accessed March 2019
- Varon M (1981) Interaction of Bdellovibrio with its prey in mixed microbial-populations. Microb Ecol 7(2):97–105Google Scholar
- Yu R, Zhang SW, Chen ZK, Li CY (2017) Isolation and application of predatory Bdellovibrio-and-like organisms for municipal waste sludge biolysis and dewaterability enhancement. Front Environ Sci Eng 11(1). https://doi.org/10.1007/s11783-017-0900-3