Transferred interbacterial antagonism genes augment eukaryotic innate immune function

Seemay Chou, Matthew D. Daugherty, S. Brook Peterson, Jacob Biboy, Youyun Yang, Brandon L. Jutras, Lillian K. Fritz-Laylin, Michael A. Ferrin, Brittany N. Harding, Christine Jacobs-Wagner, X. Frank Yang, Waldemar Vollmer, Harmit S. Malik, Joseph D. Mougous

Research output: Contribution to journalArticle

30 Citations (Scopus)

Abstract

Horizontal gene transfer allows organisms to rapidly acquire adaptive traits. 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. 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. 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.

Original languageEnglish (US)
Pages (from-to)98-101
Number of pages4
JournalNature
Volume518
Issue number7537
DOIs
StatePublished - Feb 5 2015

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amidase
Eukaryota
Horizontal Gene Transfer
Ixodes
Genes
Bacteria
Bacterial Genes
Borrelia burgdorferi
Lyme Disease
Substrate Specificity
Cell Wall
Immune System
Proteins
Enzymes

ASJC Scopus subject areas

  • General

Cite this

Chou, S., Daugherty, M. D., Peterson, S. B., Biboy, J., Yang, Y., Jutras, B. L., ... Mougous, J. D. (2015). Transferred interbacterial antagonism genes augment eukaryotic innate immune function. Nature, 518(7537), 98-101. https://doi.org/10.1038/nature13965

Transferred interbacterial antagonism genes augment eukaryotic innate immune function. / Chou, Seemay; Daugherty, Matthew D.; Peterson, S. Brook; Biboy, Jacob; Yang, Youyun; Jutras, Brandon L.; Fritz-Laylin, Lillian K.; Ferrin, Michael A.; Harding, Brittany N.; Jacobs-Wagner, Christine; Yang, X. Frank; Vollmer, Waldemar; Malik, Harmit S.; Mougous, Joseph D.

In: Nature, Vol. 518, No. 7537, 05.02.2015, p. 98-101.

Research output: Contribution to journalArticle

Chou, S, Daugherty, MD, Peterson, SB, Biboy, J, Yang, Y, Jutras, BL, Fritz-Laylin, LK, Ferrin, MA, Harding, BN, Jacobs-Wagner, C, Yang, XF, Vollmer, W, Malik, HS & Mougous, JD 2015, 'Transferred interbacterial antagonism genes augment eukaryotic innate immune function', Nature, vol. 518, no. 7537, pp. 98-101. https://doi.org/10.1038/nature13965
Chou S, Daugherty MD, Peterson SB, Biboy J, Yang Y, Jutras BL et al. Transferred interbacterial antagonism genes augment eukaryotic innate immune function. Nature. 2015 Feb 5;518(7537):98-101. https://doi.org/10.1038/nature13965
Chou, Seemay ; Daugherty, Matthew D. ; Peterson, S. Brook ; Biboy, Jacob ; Yang, Youyun ; Jutras, Brandon L. ; Fritz-Laylin, Lillian K. ; Ferrin, Michael A. ; Harding, Brittany N. ; Jacobs-Wagner, Christine ; Yang, X. Frank ; Vollmer, Waldemar ; Malik, Harmit S. ; Mougous, Joseph D. / Transferred interbacterial antagonism genes augment eukaryotic innate immune function. In: Nature. 2015 ; Vol. 518, No. 7537. pp. 98-101.
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