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A Family of Anti-Bacteroidales Peptide Toxins Wide-Spread in the Human Gut Microbiota

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A Family of Anti-Bacteroidales Peptide Toxins Wide-Spread in the Human Gut Microbiota ARTICLE https://doi.org/10.1038/s41467-019-11494-1 OPEN A family of anti-Bacteroidales peptide toxins wide-spread in the human gut microbiota Michael J. Coyne1,5, Nathalie Béchon 1,2,3,5, Leigh M. Matano1, Valentina Laclare McEneany1, Maria Chatzidaki-Livanis1,4 & Laurie E. Comstock1 Bacteria often produce antimicrobial toxins to compete in microbial communities. Here we identify a family of broad-spectrum peptide toxins, named bacteroidetocins, produced by 1234567890():,; Bacteroidetes species. We study this toxin family using phenotypic, mutational, bioinformatic, and human metagenomic analyses. Bacteroidetocins are related to class IIa bacteriocins of Gram-positive bacteria and kill members of the Bacteroidetes phylum, including Bacteroides, Parabacteroides, and Prevotella gut species, as well as pathogenic Prevotella species. The bacteroidetocin biosynthesis genes are found in horizontally acquired mobile elements, which likely allow dissemination within the gut microbiota and may explain their wide distribution in human populations. Bacteroidetocins may have potential applications in microbiome engineering and as therapeutics for polymicrobial diseases such as bacterial vaginosis and periodontal disease. 1 Division of Infectious Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA. 2 Institut Pasteur, Genetics of Biofilms Unit, 75015 Paris, cedex 15, 25-28 rue du Docteur Roux, France. 3 Ecole Doctorale Bio Sorbonne Paris Cité (BioSPC), Paris Diderot University, 75013, Cellule Pasteur, Paris, cedex, France. 4Present address: Department of Biological Sciences, University of Ohio, Athens, OH 45701, USA. 5These authors contributed equally: Michael J. Coyne, Nathalie Béchon. Correspondence and requests for materials should be addressed to L.E.C. (email: [email protected]) NATURE COMMUNICATIONS | (2019) 10:3460 | https://doi.org/10.1038/s41467-019-11494-1 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-11494-1 acteroidetes is a diverse phylum containing several orders four toxin-producing strains include a Bacteroides ovatus Bof bacteria, some of which are aerobes that live in marine (BoCL02T12C04), a Bacteroides thetaiotaomicron (BtCL15T12C11), and soil environments, and others, such as the Bacteroi- and two Bacteroides vulgatus strains (BvCL01T12C17 and dales, which are largely anaerobes. The order Bacteroidales BvCL14T03C19). As shown in these assays, the secreted toxin that includes several families and genera of bacteria that are typically remains on the plate after the producing bacteria are removed often members of host-associated microbial communities. The best travels along the surface of the plate in irregular patterns when the studied Bacteroidales include the Bacteroides and Para- second strain is added to the plate in the overlay. This phenomenon bacterioides, which are abundant members of the healthy human results in growth inhibition streaks and spots stemming from the gut microbiota, Porphyromonas gingivalis, which is an important original spot and at times distant from the dotted producer strain periodontal pathogen, and Prevotella spp., which occupy diverse (Fig. 1, Supplementary Fig. 1). We have not seen this phenomenon ecosystems including the human gut, vagina, oral cavity, cow in other secreted antibacterial toxins produced by Bacteroides spe- rumen, as well as environmental sites. Long before the advent of cies12–15 suggesting that these toxins possess different physical the microbiome era, microbiologists studied several species of properties further supported by the fact that they do not penetrate Bacteroidales due to their involvement in disease1–5. and diffuse well in the agar. These toxin-producing strains also Bacteroidetes members typically live in complex microbial inhibit their own growth in these assays, suggesting that they do not communities where the production of antibacterial molecules produce immunity proteins (Fig. 1b). against related members provides a competitive advantage. We also tested a commensal E. coli strain (phylum Proteo- Compared to some members of the Firmicutes and Proteo- bacteria), a Lactobacillus rhamnosus and Enterococcus faecium bacteria phyla where antimicrobial molecules have been studied strain (phylum Firmicutes), and a Bifidobacterium breve strain for decades6,7, there are still few studies that have analyzed the (phylum Actinobacteria). None of these gut bacteria were growth production of antimicrobial molecules by the Bacteroidetes. It is inhibited by a molecule secreted by these four strains (Fig. 1c). only within the last five years that antibacterial toxins have been identified from members of this phylum. Most Bacteroides fragilis Genetic regions involved in toxin production. To identify the strains synthesize contact dependent Type VI secretion systems gene(s) involved in toxin production and to determine if the four whose toxins kill diverse Bacteroides and Parabacteroides spe- – strains produce the same secreted toxin, random transposon cies8 11. Several diffusible antibacterial toxins have also been mutagenesis was performed using strain BoCL02T12C04 identified, the most wide-spread being the membrane attack (BoCL02). Four transposon mutants were identified that abro- comlex/perforin (MACPF) proteins, for which there are hundreds gated the inhibitory activity using B. thetaiotaomicron VPI-5482 of proteins encoded by diverse Bacteroidetes genomes. Several as the sensitive strain in the screening assay (Fig. 2a). The four MACPF proteins have been shown to have toxin activity and are – transposon insertions were mapped and found to span an specific for intra-species killing12 14. A secreted eukaryotic-like approximately 3-kb region (Fig. 2b). Of the four toxin-producing ubiquitin molecule produced exclusively by a subset of B. fragilis strains, only the genome sequence of BoCL02 was available; strains specifically antagonizes other B. fragilis strains15. therefore, we sequenced the genomes of the other three strains. In this study, we identify a family of peptide toxins produced DNA-level comparative analysis revealed that BtCL15T12C11 by diverse members of the Gram-negative Bacteroidetes phylum. (BtCL15) has a 100% identical region to this 3-kb region of We show that these bacteriocin genes are widely disseminated in BoCL02 (Fig. 2b) but the two B. vulgatus strains do not have a human gut microbiomes and target a broad-spectrum of diverse region similar at the DNA level. Analysis of the interrupted genes Bacteroidetes species including environmental, symbiotic and showed that one encodes a protein similar to an ABC-like bac- pathogenic members. teriocin transporter with an N-terminal double-glycine peptidase domain. Proteins of this family are involved in removing the Results leader peptide following a GG motif of class IIa bacteriocins and Strains producing anti-Bacteroides/Parabacteroides toxin(s).A their subsequent secretion across the membrane of Gram-positive screen of 140 different human gut Bacteroides and Parabacteroides bacteria16,17. Indeed, a gene encoding a small protein with strains of 15 different species revealed that four of the strains characteristics similar to class IIa-like bacteriocins is also included produce a secreted molecule that targets all Bacteroides and in this region (Fig. 2b)18. Similarity searches using tblastn with Parabacteroides species tested under the conditions of our the proteins encoded by this region revealed similar proteins in agar overlay spot assay (Fig. 1a, Supplementary Fig. 1). These the two B. vulgatus strains, encoded by genes with the same abc BvCL01 BvCL14 BoCL02 BtCL15 BvCL01 BvCL14 BoCL02 BtCL15 BvCL01 BvCL14 BoCL02 BtCL15 B. theta Lactobacillus VPI 5482 BvCL01 rhamnosus B. vulgatus ATCC 8482 BvCL14 E. coli HS B. fragilis 638R Enterococcus faecium P. johnsonii BoCL02 CL02T12C29 Bifidobacterium P. merdae breve CL03T12C32 BtCL15 P. goldsteinii CL02T12C30 Fig. 1 Agar spot overlay assays demonstrating broad-spectrum toxin production by four Bacteroides strains. The four toxin-producing strains are shown at the top and were cultured on plates overnight and removed, then the plates were overlaid with top agar containing the strains shown on the left to test for growth inhibition. A dark spot indicates growth inhibition of the overlaid strain. a Six Bacteroides and Parabacteroides strains used in the overlays. b The toxin-producing strains used in the overlays. c Non-Bacteroidetes gut strains from three different phyla used in the overlays 2 NATURE COMMUNICATIONS | (2019) 10:3460 | https://doi.org/10.1038/s41467-019-11494-1 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-11494-1 ARTICLE a b Bacteroides ovatus CL02T12C04 Bacteroides thetaiotaomicron CL15T12C11 tn 512 tn 724 tn 206 tn 363 BoCL02tn 206 tn 512 tn 363 tn 724 01845 01843 01842 B. theta VPI-5482 61.1% 67.2% 57.8% 66.5% Protein similarity B. vulgatus 03824 03826 03827 ATCC 8482 ABC transporter with GG peptidase domain Thiol-disulfide oxidoreductase Class IIa-Iike bacteriocin 5 TM region protein Bacteroides vulgatus CL01T12C17 Bacteroides vulgatus CL14T03C19 c d 1845 1844 1843 Δ1845 Δ Δ1844 Δ Δ1843 Δ BtCL15 vector p1845 BtCL15 vector p1844 BtCL15 vector p1843 BvCL01 BtCL15 B. theta B. theta VPI-5482 VPI-5482 vector B. vulgatus B. theta VPI-5482 ATCC 8482 p1845 B. theta VPI-5482 p1843 efE. coli E. coli 1844 BtCL15 Δ Vector Vector only 1845–1842 only 1845–1842 Δ1844 B. theta VPI-5482 No IPTG With IPTG
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