Prey killing without invasion by Bdellovibrio bacteriovorus defective for a MIDAS-family adhesin

Jess Tyson; Paul Radford; Carey Lambert; Rob Till; Simona G. Huwiler; Andrew L. Lovering; R. Elizabeth Sockett

doi:10.1038/s41467-024-47412-3

Prey killing without invasion by Bdellovibrio bacteriovorus defective for a MIDAS-family adhesin

Jess Tyson, Paul Radford, Carey Lambert, Rob Till, Simona G. Huwiler, Andrew L. Lovering, R. Elizabeth Sockett

Biosciences

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Abstract

The bacterium Bdellovibrio bacteriovorus is a predator of other Gram-negative bacteria. The predator invades the prey's periplasm and modifies the prey's cell wall, forming a rounded killed prey, or bdelloplast, containing a live B. bacteriovorus. Redundancy in adhesive processes makes invasive mutants rare. Here, we identify a MIDAS adhesin family protein, Bd0875, that is expressed at the predator-prey invasive junction and is important for successful invasion of prey. A mutant strain lacking bd0875 is still able to form round, dead bdelloplasts; however, 10% of the bdelloplasts do not contain B. bacteriovorus, indicative of an invasion defect. Bd0875 activity requires the conserved MIDAS motif, which is linked to catch-and-release activity of MIDAS proteins in other organisms. A proteomic analysis shows that the uninvaded bdelloplasts contain B. bacteriovorus proteins, which are likely secreted into the prey by the Δbd0875 predator during an abortive invasion period. Thus, secretion of proteins into the prey seems to be sufficient for prey killing, even in the absence of a live predator inside the prey periplasm.

Original language	English
Article number	3078
Number of pages	11
Journal	Nature Communications
Volume	15
Issue number	1
DOIs	https://doi.org/10.1038/s41467-024-47412-3
Publication status	Published - 9 Apr 2024

Bibliographical note

Acknowledgements:
J.T., P.R., C.L., R.T., A.L.L., and R.E.S. were funded by the Wellcome Trust Investigator Award in Science (209437/Z/17/Z) (R.E.S. and A.L.L.). S.G.H. is funded by the Swiss National Science Foundation (PZ00P3_193401) (S.G.H.). For the purposes of open access, the corresponding author has applied a CC BY public copyright licence to the Author Accepted Manuscript version arising from this submission. We thank Marjorie Fournier and Aygul Malone from the Oxford Advanced Proteomics Facility (https://www.proteomics.ox.ac.uk/) for proteomic analysis. R.E.S. would like to thank her collaborators and the Bdellovibrio community for support and interest in our lab’s research, as she closes her lab for family reasons.

Keywords

Bdellovibrio bacteriovorus/genetics
Bdellovibrio/genetics
Proteomics
Adhesins, Bacterial/genetics

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title = "Prey killing without invasion by Bdellovibrio bacteriovorus defective for a MIDAS-family adhesin",

abstract = "The bacterium Bdellovibrio bacteriovorus is a predator of other Gram-negative bacteria. The predator invades the prey's periplasm and modifies the prey's cell wall, forming a rounded killed prey, or bdelloplast, containing a live B. bacteriovorus. Redundancy in adhesive processes makes invasive mutants rare. Here, we identify a MIDAS adhesin family protein, Bd0875, that is expressed at the predator-prey invasive junction and is important for successful invasion of prey. A mutant strain lacking bd0875 is still able to form round, dead bdelloplasts; however, 10% of the bdelloplasts do not contain B. bacteriovorus, indicative of an invasion defect. Bd0875 activity requires the conserved MIDAS motif, which is linked to catch-and-release activity of MIDAS proteins in other organisms. A proteomic analysis shows that the uninvaded bdelloplasts contain B. bacteriovorus proteins, which are likely secreted into the prey by the Δbd0875 predator during an abortive invasion period. Thus, secretion of proteins into the prey seems to be sufficient for prey killing, even in the absence of a live predator inside the prey periplasm.",

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author = "Jess Tyson and Paul Radford and Carey Lambert and Rob Till and Huwiler, {Simona G.} and Lovering, {Andrew L.} and {Elizabeth Sockett}, R.",

note = "Acknowledgements: J.T., P.R., C.L., R.T., A.L.L., and R.E.S. were funded by the Wellcome Trust Investigator Award in Science (209437/Z/17/Z) (R.E.S. and A.L.L.). S.G.H. is funded by the Swiss National Science Foundation (PZ00P3_193401) (S.G.H.). For the purposes of open access, the corresponding author has applied a CC BY public copyright licence to the Author Accepted Manuscript version arising from this submission. We thank Marjorie Fournier and Aygul Malone from the Oxford Advanced Proteomics Facility (https://www.proteomics.ox.ac.uk/) for proteomic analysis. R.E.S. would like to thank her collaborators and the Bdellovibrio community for support and interest in our lab{\textquoteright}s research, as she closes her lab for family reasons.",

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AU - Tyson, Jess

AU - Radford, Paul

AU - Lambert, Carey

AU - Till, Rob

AU - Huwiler, Simona G.

AU - Lovering, Andrew L.

AU - Elizabeth Sockett, R.

N1 - Acknowledgements: J.T., P.R., C.L., R.T., A.L.L., and R.E.S. were funded by the Wellcome Trust Investigator Award in Science (209437/Z/17/Z) (R.E.S. and A.L.L.). S.G.H. is funded by the Swiss National Science Foundation (PZ00P3_193401) (S.G.H.). For the purposes of open access, the corresponding author has applied a CC BY public copyright licence to the Author Accepted Manuscript version arising from this submission. We thank Marjorie Fournier and Aygul Malone from the Oxford Advanced Proteomics Facility (https://www.proteomics.ox.ac.uk/) for proteomic analysis. R.E.S. would like to thank her collaborators and the Bdellovibrio community for support and interest in our lab’s research, as she closes her lab for family reasons.

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N2 - The bacterium Bdellovibrio bacteriovorus is a predator of other Gram-negative bacteria. The predator invades the prey's periplasm and modifies the prey's cell wall, forming a rounded killed prey, or bdelloplast, containing a live B. bacteriovorus. Redundancy in adhesive processes makes invasive mutants rare. Here, we identify a MIDAS adhesin family protein, Bd0875, that is expressed at the predator-prey invasive junction and is important for successful invasion of prey. A mutant strain lacking bd0875 is still able to form round, dead bdelloplasts; however, 10% of the bdelloplasts do not contain B. bacteriovorus, indicative of an invasion defect. Bd0875 activity requires the conserved MIDAS motif, which is linked to catch-and-release activity of MIDAS proteins in other organisms. A proteomic analysis shows that the uninvaded bdelloplasts contain B. bacteriovorus proteins, which are likely secreted into the prey by the Δbd0875 predator during an abortive invasion period. Thus, secretion of proteins into the prey seems to be sufficient for prey killing, even in the absence of a live predator inside the prey periplasm.

AB - The bacterium Bdellovibrio bacteriovorus is a predator of other Gram-negative bacteria. The predator invades the prey's periplasm and modifies the prey's cell wall, forming a rounded killed prey, or bdelloplast, containing a live B. bacteriovorus. Redundancy in adhesive processes makes invasive mutants rare. Here, we identify a MIDAS adhesin family protein, Bd0875, that is expressed at the predator-prey invasive junction and is important for successful invasion of prey. A mutant strain lacking bd0875 is still able to form round, dead bdelloplasts; however, 10% of the bdelloplasts do not contain B. bacteriovorus, indicative of an invasion defect. Bd0875 activity requires the conserved MIDAS motif, which is linked to catch-and-release activity of MIDAS proteins in other organisms. A proteomic analysis shows that the uninvaded bdelloplasts contain B. bacteriovorus proteins, which are likely secreted into the prey by the Δbd0875 predator during an abortive invasion period. Thus, secretion of proteins into the prey seems to be sufficient for prey killing, even in the absence of a live predator inside the prey periplasm.

KW - Bdellovibrio bacteriovorus/genetics

KW - Bdellovibrio/genetics

KW - Proteomics

KW - Adhesins, Bacterial/genetics

U2 - 10.1038/s41467-024-47412-3

DO - 10.1038/s41467-024-47412-3

M3 - Article

C2 - 38594280

SN - 2041-1723

VL - 15

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 3078

ER -

Prey killing without invasion by Bdellovibrio bacteriovorus defective for a MIDAS-family adhesin

Abstract

Bibliographical note

Keywords

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