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Environmental Microbiology | Spotlight

Myxococcus xanthus Predation of Gram-Positive or Gram-Negative Bacteria Is Mediated by Different Bacteriolytic Mechanisms

Kirstin I. Arend, Janka J. Schmidt, Tim Bentler, Carina Lüchtefeld, Daniel Eggerichs, Hannah M. Hexamer, Christine Kaimer
Gladys Alexandre, Editor
Kirstin I. Arend
aMicrobial Biology, Ruhr University, Bochum, Germany
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Janka J. Schmidt
aMicrobial Biology, Ruhr University, Bochum, Germany
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Tim Bentler
aMicrobial Biology, Ruhr University, Bochum, Germany
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Carina Lüchtefeld
aMicrobial Biology, Ruhr University, Bochum, Germany
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Daniel Eggerichs
aMicrobial Biology, Ruhr University, Bochum, Germany
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Hannah M. Hexamer
aMicrobial Biology, Ruhr University, Bochum, Germany
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Christine Kaimer
aMicrobial Biology, Ruhr University, Bochum, Germany
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  • ORCID record for Christine Kaimer
Gladys Alexandre
University of Tennessee at Knoxville
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DOI: 10.1128/AEM.02382-20
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ABSTRACT

Myxococcus xanthus kills other species to use their biomass as an energy source. Its predation mechanisms allow feeding on a broad spectrum of bacteria, but the identity of predation effectors and their mode of action remain largely unknown. We initially focused on the role of hydrolytic enzymes for prey killing and compared the activities of secreted M. xanthus proteins against four prey strains. Seventy-two secreted proteins were identified by mass spectrometry; among them is a family 19 glycoside hydrolase that displayed bacteriolytic activity in vivo and in vitro. This enzyme, which we name LlpM (lectin/lysozyme-like protein of M. xanthus), was not essential for predation, indicating that additional secreted components are required to disintegrate prey. Furthermore, secreted proteins lysed only Gram-positive, not Gram-negative, species. We thus compared the killing of different prey by cell-associated mechanisms: individual M. xanthus cells killed all four test strains in a cell contact-dependent manner but were only able to disintegrate Gram-negative, not Gram-positive, cell envelopes. Thus, our data indicate that M. xanthus uses different multifactorial mechanisms for killing and degrading different prey. Besides secreted enzymes, cell-associated mechanisms that have not been characterized so far appear to play a major role in prey killing.

IMPORTANCE Predation is an important survival strategy of the widespread myxobacteria, but it remains poorly understood on the mechanistic level. Without a basic understanding of how prey cell killing and consumption is achieved, it also remains difficult to investigate the role of predation for the complex myxobacterial lifestyle, reciprocal predator-prey relationships, or the impact of predation on complex bacterial soil communities. We study predation in the established model organism Myxococcus xanthus, aiming to dissect the molecular mechanisms of prey cell lysis. In this study, we addressed the role of secreted bacteriolytic proteins, as well as potential mechanistic differences in the predation of Gram-positive and Gram-negative bacteria. Our observation shows that secreted enzymes are sufficient for killing and degrading Gram-positive species but that cell-associated mechanisms may play a major role in killing Gram-negative and Gram-positive prey on fast timescales.

FOOTNOTES

    • Received 27 September 2020.
    • Accepted 1 December 2020.
    • Accepted manuscript posted online 11 December 2020.
  • Supplemental material is available online only.

  • Copyright © 2021 American Society for Microbiology.

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Myxococcus xanthus Predation of Gram-Positive or Gram-Negative Bacteria Is Mediated by Different Bacteriolytic Mechanisms
Kirstin I. Arend, Janka J. Schmidt, Tim Bentler, Carina Lüchtefeld, Daniel Eggerichs, Hannah M. Hexamer, Christine Kaimer
Applied and Environmental Microbiology Feb 2021, 87 (5) e02382-20; DOI: 10.1128/AEM.02382-20

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Myxococcus xanthus Predation of Gram-Positive or Gram-Negative Bacteria Is Mediated by Different Bacteriolytic Mechanisms
Kirstin I. Arend, Janka J. Schmidt, Tim Bentler, Carina Lüchtefeld, Daniel Eggerichs, Hannah M. Hexamer, Christine Kaimer
Applied and Environmental Microbiology Feb 2021, 87 (5) e02382-20; DOI: 10.1128/AEM.02382-20
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KEYWORDS

bacterial behavior
bacteriolytic enzymes
glycoside hydrolase
outer membrane vesicles

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