Brief Communication | Published:

Bdellovibrio bacteriovorus HD100, a predator of Gram-negative bacteria, benefits energetically from Staphylococcus aureus biofilms without predation

The ISME Journalvolume 12pages20902095 (2018) | Download Citation


Bdellovibrio bacteriovorus HD100 is a predatory bacterium which lives by invading the periplasm of Gram-negative bacteria and consuming them from within. Although B. bacteriovorus HD100 attacks only Gram-negative bacterial strains, our work here shows attack-phase predatory cells also benefit from interacting with Gram-positive biofilms. Using Staphylococcus aureus biofilms, we show this predator degrades the biofilm matrix, obtains nutrients and uses these to produce and secrete proteolytic enzymes to continue this process. When exposed to S. aureus biofilms, the transcriptome of B. bacteriovorus HD100 was analogous to that seen when present intraperiplasmically, suggesting it is responding similarly as when in a prey. Moreover, two of the induced proteases (Bd2269 and Bd2692) were purified and their activities against S. aureus biofilms verified. In addition, B. bacteriovorus HD100 gained several clear benefits from its interactions with S. aureus biofilms, including increased ATP pools and improved downstream predatory activities when provided prey.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.


  1. 1.

    Dwidar M, Monnappa AK, Mitchell RJ. The dual probiotic and antibiotic nature of Bdellovibrio bacteriovorus. BMB Rep. 2012;45:71–78.

  2. 2.

    Dashiff A, Junka RA, Libera M, Kadouri DE. Predation of human pathogens by the predatory bacteria Micavibrio aeruginosavorus and Bdellovibrio bacteriovorus. J Appl Microbiol. 2011;110:431–44.

  3. 3.

    Dashiff A, Kadouri DE. Predation of oral pathogens by Bdellovibrio bacteriovorus 109J. Mol Oral Microbiol. 2011;26:19–34.

  4. 4.

    Im H, Choi SY, Son S, Mitchell RJ. Combined application of bacterial predation and violacein to kill polymicrobial pathogenic communities. Sci Rep. 2017;7:14415.

  5. 5.

    Monnappa AK, Dwidar M, Seo JK, Hur JH, Mitchell RJ. Bdellovibrio bacteriovorus inhibits Staphylococcus aureus biofilm formation and invasion into human epithelial cells. Sci Rep. 2014;4:3811.

  6. 6.

    Chu WH, Zhu W. Isolation of Bdellovibrio as biological therapeutic agents used for the treatment of Aeromonas hydrophila infection in fish. Zoonoses Public Health. 2010;57:258–64.

  7. 7.

    Stolp H, Starr MP. Bdellovibrio bacteriovorus Gen. Et Sp. N., a predatory, ectoparasitic, and bacteriolytic microorganism. Antonie Leeuwenhoek. 1963;29:217–48.

  8. 8.

    Hespell RB, Rosson RA, Thomashow MF, Rittenberg SC. Respiration of Bdellovibrio bacteriovorus strain 109J and its energy substrates for intraperiplasmic growth. J Bacteriol. 1973;113:1280–88.

  9. 9.

    Chanyi RM, Koval SF, Brooke JS. Stenotrophomonas maltophilia biofilm reduction by Bdellovibrio exovorus. Env Microbiol Rep. 2016;8:343–51.

  10. 10.

    Kadouri D, O’Toole GA. Susceptibility of biofilms to Bdellovibrio bacteriovorus attack. Appl Environ Microb. 2005;71:4044–51.

  11. 11.

    Kelley JI, Turng B, Williams HN, Baer ML. Effects of temperature, salinity, and substrate on the colonization of surfaces in situ by aquatic bdellovibrios. Appl Environ Microbiol. 1997;63:84–90.

  12. 12.

    Williams HN, Schoeffield AJ, Guether D, Kelley J, Shah D, Falkler WA. Recovery of bdellovibrios from submerged surfaces and other aquatic habitats. Microb Ecol. 1995;29:39–48.

  13. 13.

    Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature. 2010;465:346–U100.

  14. 14.

    Lauderdale KJ, Malone CL, Boles BR, Morcuende J, Horswill AR. Biofilm dispersal of community-associated methicillin-resistant Staphylococcus aureus on orthopedic implant material. J Orthop Res. 2010;28:55–61.

  15. 15.

    Elchinger PH, Delattre C, Faure S, Roy O, Badel S, Bernardi T, et al. Effect of proteases against biofilms of Staphylococcus aureus and Staphylococcus epidermidis. Lett Appl Microbiol. 2014;59:507–13.

  16. 16.

    Teplitski M, Al-Agely A, Ahmer BMM. Contribution of the SirA regulon to biofilm formation in Salmonella enterica serovar Typhimurium. Microbiol-Sgm. 2006;152:3411–23.

  17. 17.

    Karunker I, Rotem O, Dori-Bachash M, Jurkevitch E, Sorek R. A global transcriptional switch between the attack and growth forms of Bdellovibrio bacteriovorus. PLoS ONE. 2013;8:e61850.

  18. 18.

    Dwidar M, Im H, Seo JK, Mitchell RJ. Attack-phase Bdellovibrio bacteriovorus responses to extracellular nutrients are analogous to those seen during late intraperiplasmic growth. Microb Ecol. 2017;74:937–46.

  19. 19.

    LaMarre AG, Straley SC, Conti SF. Chemotaxis toward amino acids by Bdellovibrio bacteriovorus. J Bacteriol. 1977;131:201–7.

  20. 20.

    Im H, Kim D, Ghim CM, Mitchell RJ. Shedding light on microbial predator-prey population dynamics using a quantitative bioluminescence assay. Microb Ecol. 2014;67:167–76.

  21. 21.

    Iebba V, Totino V, Santangelo F, Gagliardi A, Ciotoli L, Virga A, et al. Bdellovibrio bacteriovorus directly attacks Pseudomonas aeruginosa and Staphylococcus aureus Cystic fibrosis isolates. Front Microbiol. 2014;5:280.

Download references


Funding for this research was sponsored by the National Research Foundation of Korea within the General Research Program (Grant No. 2016R1D1A1A09919912). We thank them for the financial support. The following reagent was provided by the Network on Antimicrobial Resistance in Staphylococcus aureus (NARSA) for distribution by BEI Resources, NIAID, NIH: Staphylococcus aureus subsp. aureus Strain JE2 (NR-46543)

Author contributions

MD and HI designed and carried out the experiments. RJM supervised the experimental work. MD, HI, and RJM evaluated the data. MD, HI, and RJM wrote the manuscript.

Author information

Author notes


    1. School of Life Sciences, Ulsan National Institute of Science and Technology (UNIST), 50 UNIST-gil, Ulsan, 44919, Republic of Korea

      • Hansol Im
      •  & Robert J. Mitchell
    2. Nucleic Acid Chemistry and Engineering Unit, Okinawa Institute of Science and Technology (OIST), 1919-1 Tancha, Onna-son, Kunigami-gun, Okinawa, Japan, 904-0495

      • Mohammed Dwidar


    1. Search for Hansol Im in:

    2. Search for Mohammed Dwidar in:

    3. Search for Robert J. Mitchell in:

    Conflict of interest

    The authors declare that they have no conflict of interest.

    Corresponding authors

    Correspondence to Mohammed Dwidar or Robert J. Mitchell.

    Electronic supplementary material

    About this article

    Publication history






    Article notes

    These authors contributed equally: Hansol Im and Mohammed Dwidar