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Transferred interbacterial antagonism genes augment eukaryotic innate immune function

Lookup NU author(s): Dr Jacob BiboyORCiD, Professor Waldemar Vollmer

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Abstract

Horizontal gene transfer allows organisms to rapidly acquire adaptive traits(1). Although documented instances of horizontal gene transfer from bacteria to eukaryotes remain rare, bacteria represent a rich source of new functions potentially available for co-option(2). One benefit that genes of bacterial origin could provide to eukaryotes is the capacity to produce antibacterials, which have evolved in prokaryotes as the result of eons of interbacterial competition. The type VI secretion amidase effector (Tae) proteins are potent bacteriocidal enzymes that degrade the cell wall when delivered into competing bacterial cells by the type VI secretion system(3). Here we show that tae genes have been transferred to eukaryotes on at least six occasions, and that the resulting domesticated amidase effector (dae) genes have been preserved for hundreds of millions of years through purifying selection. We show that the dae genes acquired eukaryotic secretion signals, are expressed within recipient organisms, and encode active antibacterial toxins that possess substrate specificity matching extant Tae proteins of the same lineage. Finally, we show that a dae gene in the deer tick Ixodes scapularis limits proliferation of Borrelia burgdorferi, the aetiologic agent of Lyme disease. Our work demonstrates that a family of horizontally acquired toxins honed to mediate interbacterial antagonism confers previously undescribed antibacterial capacity to eukaryotes. We speculate that the selective pressure imposed by competition between bacteria has produced a reservoir of genes encoding diverse antimicrobial functions that are tailored for co-option by eukaryotic innate immune systems.


Publication metadata

Author(s): Chou S, Daugherty MD, Peterson SB, Biboy J, Yang YY, Jutras BL, Fritz-Laylin LK, Ferrin MA, Harding BN, Jacobs-Wagner C, Yang XF, Vollmer W, Malik HS, Mougous JD

Publication type: Article

Publication status: Published

Journal: Nature

Year: 2015

Volume: 518

Issue: 7537

Pages: 98-101

Print publication date: 05/02/2015

Online publication date: 24/11/2014

Acceptance date: 13/10/2014

ISSN (print): 0028-0836

ISSN (electronic): 1476-4687

Publisher: Nature Publishing Group

URL: http://dx.doi.org/10.1038/nature13965

DOI: 10.1038/nature13965


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Funding

Funder referenceFunder name
American Society for Microbiology Undergraduate Research Fellowship
Burroughs Wellcome Fund
Howard Hughes Medical Institute (HHMI)
Irvington Institute Fellowship from the Cancer Research Institute
AI083640National Institutes of Health
BB/I020012/1BBSRC
AI080609National Institutes of Health
HDTRA-1-13-014Defense Threat Reduction Agency

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