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Attack-Phase Bdellovibrio bacteriovorus Responses to Extracellular Nutrients Are Analogous to Those Seen During Late Intraperiplasmic Growth

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Abstract

Bdellovibrio bacteriovorus is a predatory bacterium which lives by invading the periplasm of gram-negative bacteria and consuming them from within. This predator was thought to be dependent upon prey for nutrients since it lacks genes encoding for critical enzymes involved in amino acid biosynthesis. This study, however, found that planktonic attack-phase predators are not just dependent upon prey for nutrients, but rather, they respond to nutrients in the surrounding medium and, subsequently, synthesize and secrete proteases in a nutrient-dependent manner. The major secreted proteases were identified through mass spectrometry analyses. Subsequent RT-qPCR analyses found that the nutrient-induced proteases are similar to those expressed within the prey periplasm during the late intraperiplasmic growth phase. Furthermore, RNA sequencing found that incubating the planktonic attack-phase cells in a nutritious environment for a short period of time (4 h) changes its gene expression pattern to a status that is akin to the late intraperiplasmic phase, with more than 94% of the genes previously identified as being late intraperiplasmic-specific also being induced by nutrient broth in this study. This strong correlation between the gene expression patterns hints that the availability of hydrolyzed prey cell components to the predator is likely the stimulus controlling the expression of late intraperiplasmic B. bacteriovorus genes during predation.

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Acknowledgements

This work was generously supported by the Korea Health Industry Development Institute (KHIDI) for financial support (Grant No. HI13C13550000). We wish to thank the UNIST Central Research Facilities (UCRF) for their help with the LC-MS/MS data.

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Author notes

  1. Mohammed Dwidar and Hansol Im contributed equally to the work

Authors and Affiliations

  1. School of Life Sciences, Ulsan National Institute of Science and Technology, 50 UNIST-gil, Ulsan, 689-798, Republic of Korea

    Mohammed Dwidar, Hansol Im & Robert J. Mitchell

  2. Nucleic Acid Chemistry and Engineering Unit, Okinawa Institute of Science and Technology (OIST), 1919-1 Tancha, Onna-son, Okinawa, 904-0495, Japan

    Mohammed Dwidar

  3. UNIST Central Research Facility, Ulsan National Institute of Science and Technology, Ulsan, Republic of Korea

    Jeong Kon Seo

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  1. Mohammed Dwidar
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  2. Hansol Im
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Contributions

M.D. and H.I. designed and carried out the experiments. R.J.M. supervised the experimental work. M.D., H.I., and R.J.M. evaluated the data. M.D. and J.S.K. performed the mass spectrometry experiments. J.S.K. performed the mass spectrometry analyses. M.D., H.I., J.S.K., and R.J.M. wrote the manuscript.

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Correspondence to Mohammed Dwidar or Robert J. Mitchell.

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Dwidar, M., Im, H., Seo, J.K. et al. Attack-Phase Bdellovibrio bacteriovorus Responses to Extracellular Nutrients Are Analogous to Those Seen During Late Intraperiplasmic Growth. Microb Ecol 74, 937–946 (2017). https://doi.org/10.1007/s00248-017-1003-1

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